Anaerobic Biodegradation of Phenol in Wastewater Treatment

Applied Microbiology and Biotechnology (2021) 105:2195–2224
https://doi.org/10.1007/s00253-021-11182-5
MINI-REVIEW
Anaerobic biodegradation of phenol in wastewater treatment:

achievements and limits
M. Concetta Tomei 1 & Domenica Mosca Angelucci 1 & Elisa Clagnan 2 & Lorenzo Brusetti 3
Received: 10 December 2020 / Revised: 9 February 2021 / Accepted: 14 February 2021 / Published online: 25 February 2021
# The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature 2021
Abstract
Anaerobic biodegradation of toxic compounds found in industrial wastewater is an attractive solution allowing the recovery of
energy and resources but it is still challenging due to the low kinetics making the anaerobic process not competitive against the
aerobic one. In this review, we summarise the present state of knowledge on the anaerobic biodegradation process for phenol, a
typical target compound employed in toxicity studies on industrial wastewater treatment. The objective of this article is to provide
an overview on the microbiological and technological aspects of anaerobic phenol degradation and on the research needs to fill
the gaps still hindering the diffusion of the anaerobic process. The first part is focused on the microbiology and extensively
presents and characterises phenol-degrading bacteria and biodegradation pathways. In the second part, dedicated to process
feasibility, anaerobic and aerobic biodegradation kinetics are analysed and compared, and strategies to enhance process perfor-
mance, i.e. advanced technologies, bioaugmentation, and biostimulation, are critically analysed and discussed. The final section
provides a summary of the research needs. Literature data analysis shows the feasibility of anaerobic phenol biodegradation at
laboratory and pilot scale, but there is still a consistent gap between achieved aerobic and anaerobic performance. This is why
current research demand is mainly related to the development and optimisation of powerful technologies and effective operation
strategies able to enhance the competitiveness of the anaerobic process. Research efforts are strongly justified because the
anaerobic process is a step forward to a more sustainable approach in wastewater treatment.
Key points
• Review of phenol-degraders bacteria and biodegradation pathways.
• Anaerobic phenol biodegradation kinetics for metabolic and co-metabolic processes.
• Microbial and technological strategies to enhance process performance.
Keywords Anaerobic phenol biodegradation . Anaerobic phenol-degraders . Biodegradation inhibited kinetics . Advanced
technologies . Bioaugmentation and biostimulation . Aerobic phenol biodegradation
Introduction refinery, pharmaceutical, coal conversion, and chemical

and petro-chemical. A wide range of concentrations from
Phenol and its derivatives are toxic contaminants found in 10 to 17,500 mg L−1 characterises water emissions of
wastewater originated from many industries including oil phenols in industrial effluents (Veeresh et al. 2005).
Half-maximal effective concentrations (EC50) of phenol
measured with Microtox® at 15 °C were 23.28, 25.61,
* M. Concetta Tomei and 26.01 (mg L−1) for 5, 15, and 30 min incubation
tomei@irsa.cnr.it periods respectively (Ghosh and Doctor 1992) and even
lower (< 10 mg L−1) for substituted phenols as chloro-
1
Water Research Institute, C.N.R., Via Salaria km 29.300, CP 10,
phenols (Ribo and Kaiser 1983). Comparison of phenolic
00015 Monterotondo Stazione Rome, Italy compound concentrations in industrial effluents with their
2
Ricicla Group – DiSAA, University of Milan, Via Celoria 2,
EC50 value gives a clear idea of the high toxicity associ-
20133 Milano, Italy ated with these compounds, which are included in priority
3
Faculty of Science and Technology, Free University of Bozen –
pollutant lists of the European Union (EU 2013) and of
Bolzano, Piazza Università 5, 39100 Bolzano, Italy the US Environmental Protection Agency (US-EPA
2196 Appl Microbiol Biotechnol (2021) 105:2195–2224
2013). When discharged into the aquatic environment, and efficient performance. According to this, identification
phenols may constitute a serious ecological hazard even and characterisation of microbial populations resistant to high
at low concentrations in the order of few mg L−1. phenol concentrations are required to define operative control
The widespread presence of phenol and phenolic com- strategies to improve the stability of the system (Franchi et al.
pounds in polluted streams made them one of the most inves- 2020). Among the technologies, high-rate anaerobic bioreac-
tigated groups of toxic compounds. Phenol is a typical target tors are the most promising solutions to improve the anaerobic
employed in toxicity studies and in the testing of processes process performance in degrading phenol and, in general, tox-
and technologies for industrial wastewater treatment. ic compounds, due to their feature of operating at high sludge
Chemical oxidative processes (i.e. ozonation, Fenton’s re- retention time (SRT) (independently on the hydraulic reten-
agent, and hydrogen peroxide) have been demonstrated effec- tion time, HRT). Previous studies on phenol removal of high-
tive for phenolic compound removal in wastewater, but high rate bioreactors, such as up-flow anaerobic sludge blanket
costs, massive employment of reagents, and high environmen- reactor (UASB) and expanded granular sludge bed reactor
tal impact have hindered their application especially for large (EGSB), confirmed their potentialities (Almendariz et al.
wastewater volumes (Li et al. 2019). Moreover, the increasing 2005; Veeresh et al. 2005).
demand of a sustainability-directed research highlighted the The main objective of this review is to present a complete
need of developing processes and technologies for industrial picture of the present state of knowledge on the microbiolog-
wastewater treatment characterised by minimal use of re- ical and technological aspects of anaerobic phenol degrada-
agents and low environmental impact. Biological treatments, tion and on the research needs to fill the gaps still hindering
besides being more sustainable than the chemical and physical the diffusion of the anaerobic process. The first part focuses on
ones, are less expensive and feasible with relatively simple the microbiology and extensively presents and characterises
technologies. The reverse of the medal is the necessity of the anaerobic bacteria degrading phenol and their role in the
microbial cultures able to degrade toxic compounds at rates process. In the second part, dedicated to the process feasibil-
suitable for practical application. In the specific case of phe- ity, anaerobic and aerobic biodegradation kinetics are
nol, aerobic removal processes have been extensively investi- discussed and compared. Lastly, the strategies to enhance
gated with good results (Al-Khalid and El-Naas 2012; the process performance are critically analysed and discussed,
Pradeep et al. 2015; Surkatti and Al-Zuhair 2018), while for while the final section summarises the research needs that
the anaerobic ones, there are still drawbacks to overcome in emerged from literature analysis.
order to optimise their performance.
Why anaerobic treatment? Anaerobic phenol degraders
Aerobic treatment reaches very good effluent quality, but it is Phenol degradation in wastewater treatment plants (WWTPs)
an energy-intensive process that requires oxygen, produces presents numerous challenges derived from the inhibitive
high excess of sludge, and fails in recovering the potential property of phenol on microbial communities both in meta-
resources (nutrients) available in wastewater (Martinez-Sosa bolic and structural terms, which can lead to performance
et al. 2011; Smith et al. 2012). Several motivations justify the failure (Cabrol and Malhautier 2011). Anaerobic microorgan-
investigation of anaerobic processes as alternative to aerobic isms, despite being more sensitive to phenol loads than their
treatment i.e. energy recovered from methane and energy aerobic counterpart and showing a slower growth rate, have
saved from aeration exceeding the thermal energy demand, the advantages of lower sludge production and an easier reac-
lower sludge production, no chemicals added, and the possi- tor setup (Veeresh et al. 2005; Tay et al. 2005; Tauseef et al.
bility to recover valuable resource as nutrients. On the other 2013). The efficiency of an anaerobic system relies on micro-
hand, anaerobic kinetics are slower than the aerobic ones, bial consortia and their adaptation to phenol (Franchi et al.
effluent concentrations are higher, and anaerobic bacteria, es- 2018). Anaerobic phenol degrading biomass has been
pecially methanogens, are strongly affected by toxicity of characterised within multiple studies and used to identify mi-
compounds such as phenol. EC50 values of phenol for anaer- croorganisms that could enhance the performance of the bio-
obic biomass are in the range of 120 and 225 mg gVSS−1 reactor (Franchi et al. 2018) and to develop resistant microbial
(Hernandez and Edyvean 2008; Wirth et al. 2015) and even communities (Madigou et al. 2016). Developed microbial
for phenol-acclimated sludge, increasing dynamic load leads communities often differ in composition when compared with
to a worsening of both removal efficiency and methane pro- the inoculum (Franchi et al. 2018). The input of different
duction (Fang et al. 2004; Chapleur et al. 2016). phenolic wastewater and the selective pressure of increasing
Effective phenol biodegradation in anaerobic systems re- phenol loads can further affect and shape the composition of
quires the optimal combination of microbial cultures resistant the microbial community with a progressive adaptation to
to toxicity, and technological solutions able to ensure stable phenol, shorter adaptation time, and higher removal rates
Appl Microbiol Biotechnol (2021) 105:2195–2224 2197
(Rosenkranz et al. 2013; Na et al. 2016). The morphology of (Thomas et al. 2002) and Candida albicans isolated from
the community plays a further role in removal rates. In terms activated sludge of a refinery plant (Wang et al. 2008) were
of phenol degradation, the granulation of sludge, for example, demonstrated to be also able to anaerobically degrade phenol.
has shown to accelerate adaptation times with degradation rate In a salinity fluctuation study, an anaerobic membrane biore-
and community structure directly correlated to sludge granule actor (AnMBR) treating synthetic phenolic wastewater
size as the high mass transfer resistance of granules reduces showed better stability and performance than the UASBs pos-
phenol toxicity (Wang et al. 2020). sibly due to higher homogeneity and methanogenic activity
Biodegradation of aromatic compounds such as phenol has leading to a higher functionality and resilience (Muñoz Sierra
been found in nitrate, sulphate, and iron-reducing bacteria. et al. 2018). These two systems were both characterised by the
The first bacteria that have been studied for the chemical presence of Clostridium and Thermovirgaceae among anaer-
and genomic characterisation of anaerobic phenol degraders obic phenol degraders; however, syntrophic phenol degraders
were Rhodopseudomonas palustris, Magnetospirillum spp., ( e . g . Sy ntr op hor hab da ce ae, P e l o t o m a c u l u m an d
Thauera aromatica, Azoarcus spp., Geobacter Syntrophaceae (Sieber et al. 2012) were found when the max-
metallireducens, and Syntrophus aciditrophicus (Tschech imum phenol conversion rate was reached, especially in the
and Fuchs 1987, 1989; He and Wiegel 1995; Rabus and AnMBR (Muñoz Sierra et al. 2018). Syntrophic phenol de-
Widdel 1995; van Schie and Young 1998). Further organisms graders include genera such as Desulfotomaculum,
such as iron reducers (Geobacter metallireducens) and sul- Syntrophus, Desulfovibrio, Syntrophorhabdus, and
phate reducers (Desulfobacterium phenolicum and Pelotomaculum (Ju et al. 2018; Muñoz Sierra et al. 2018);
Desulfovibrio species) have been studied for their ability to these genera are capable of anaerobic degradation of aromatic
carry out the first step of phenol carboxylation (Lovley and compounds in syntrophic association with methanogens (phe-
Lonergan 1990; Bak and Widdel 1986). nol degradation under methanogenic conditions) (Qiu et al.
A first attempt at community studies on phenol degraders 2008; Nobu et al. 2014; Narihiro et al. 2015). From a UASB
was carried out on a denitrifying bacterial consortium treating brewery wastewater, Syntrophorhabdus and
degrading phenol under anaerobic conditions (Khouri et al. Clostridium were again the most abundant genera and both
1992). Here, three bacteria (i.e. an unidentified gram- highlighted to be phenol degraders, with a consistent increase
negative bacteria, Acinetobacter johnsonii and Pseudomonas of Deltaproteobacteria with acclimation to phenol (Na et al.
fluorescens III) were identified with the unknown bacteria 2016). Among other genera, Desulfotomaculum was an abun-
being the anaerobic phenol degrader. Although phylogenic dant phenol degrader, which however showed a decrease in
analysis on phenol-fed bioreactors have shown that most ge- abundance across time (Na et al. 2016).
nomes belong to uncultured bacteria (Ju et al. 2018), in recent Full-scale studies on phenol degrading communities are far
years, a set of multiple phyla was almost ubiquitously found less numerous. In full-scale (9903–1600 m3) anaerobic di-
within anaerobic phenol-fed bioreactors treating wastewater gesters (continuously stirred tank reactors, CSTRs) treating
both at lab- and full-scale (i.e. Bacteroidetes, Chloroflexi, sewage sludge, the genera Syntrophorhabdus was found and
Proteobacteria, and Firmicutes) (Chen et al. 2009; accounted for the anaerobic phenol degradation of the systems
Rosenkranz et al. 2013; Na et al. 2016; Li et al. 2016; Joshi (Shin et al. 2016). In another full-scale granular activated
et al. 2016; Shin et al. 2016). Other commonly and abundantly carbon-anaerobic fluidised bed reactor (GAC-AFBR) treating
phyla found in communities acclimated to phenol were wastewater from manufacturing of phenolic resin,
Thermotogae, Cloacimonetes, Synergistetes, and Syntrophorhabdus was again, together with Syntrophus and
Euryarchaeaota (Wang et al. 2017). Desulfovibrio, the main responsible for phenol degradation
In lab-scale and pilot studies, several bacterial genera were (Chen et al. 2009).
identified within anoxic granular denitrifying reactor (UASB) Anaerobic degradation pathways of phenol have been re-
treating synthetic wastewater with phenol as the sole C-source ported either via 4-hydroxybenzoate (Kobayashi et al. 1989)
for their ability to use aromatic compounds as electron donors. or via n-caproate (Bakker 1977) (Fig. 1).
These include Ignavibacterium, Denitratisoma, and Thaurea
(Ramos et al. 2016), and Desulfotomaculum, Clostridium, and Anaerobic phenol degradation pathways via 4-
Syntrophus (Fang et al. 2004). In another coking wastewater hydroxybenzoate
treating UASB, Ottowia was reported as the most abundant
genera of phenol degraders together with Advenella, Under anaerobic conditions, phenol can be converted cost-
Corynebacterium and Sphingobium (Joshi et al. 2016). effectively into butyrate and acetate and eventually methane
Pseudomonas, expecially the species Putida, is another ubiq- under anaerobic conditions (Ju et al. 2018). Bacteria involved
uitously found phenol degrader (Bakhshi et al. 2011) and ad- in phenol degradation, and previously highlighted, possess
ditionally, Enterobacter and Alcaligenes faecalis isolated specific sets of genes located in a cluster grouping multiple
from a slurry bioreactor treating coking oven wastewater genes for the phenol degradation pathway. This cluster is
generally surrounded by other clusters for the degradation of phenol regulation mechanism (Breinig et al. 2000; Schleinitz
benzoate and 4-hydroxybenzoate within an island of et al. 2009; Lovley et al. 2011). Further down, the 4-
aromatics-degradation genes. The overall organisation of hydroxybenzoate-CoA ligase is an enzyme belonging to the
genes, however, does not seem to be conserved among differ- BCL family and it has been found encoded by genes upregu-
ent organisms (Breinig et al. 2000; Butler et al. 2007; lated by phenol and identified in bclA for T. aromatic, bzdA
Schleinitz et al. 2009; Ju et al. 2018). for Azoarcus spp. and hbaA in R. palustris (Gibson et al. 1997;
Starting from phenol there are two main pathways of an- Holmes et al. 2012). Following, the 4-hydroxybenzoyl-CoA
aerobic degradation via 4-hydroxybenzoate (Fig. 1). Within reductase, a molybdenum-flavin-iron-sulphur protein, is
the first path, phenol is converted to phenylphosphate by an encoded by the hcrABC genes in T. aromatica or hbaBCD
ATP-dependent phenylphosphate synthase and then it is para in R. palustris (Gibson et al. 1997; Breese and Fuchs 1998).
carboxylated to 4-hydroxybenzoate by a phenylphosphate The benzoyl-CoA then enters the anaerobic benzoyl-CoA
carboxylase (Tschech and Fuchs 1987, 1989; Glöckler et al. degradation pathway (Fig. 2). Here the first step is a reductive
1989). This path is present in bacterial genera such as dearomatisation to cyclohexa-1,5-diene-1-carbonyl-CoA
Pseudomonas, Azoarcus, Thauera, and Geobacter, while in catalysed by a benzoyl-CoA reductase (Boll and Fuchs
other bacteria, generally strict anaerobes, such as Clostridium 1995; Boll et al. 2000; Kuntze et al. 2008). Cyclohexa-1,5-
hydroxybenzoicum, when high phenol and CO2 concentra- diene-1-carbonyl-CoA can further take two anaerobic routes
tions are present, phenol is directly converted to 4- leading to the cleavage of the aromatic ring. Within the first
hydroxybenzoate by a 4-hydroxybenzoate decarboxylase route (e.g. T. Aromatica), the cyclohexa-1,5-diene-1-carbon-
(Zhang and Wiegel 1994; He and Wiegel 1995; Huang et al. yl-CoA is firstly hydrated to 6-Hydroxycyclohex-1-ene-1-car-
1999). Subsequently, the two pathways follow the same route bonyl-CoA and reduced to 6-oxocyclohex-1-carbonyl-CoA.
where 4-hydroxybenzoate is firstly activated to a CoA Then the ring is opened by a hydrolase to 3-
thioester, which is then reduced to benzoyl-CoA (van Schie hydroxypimelyl-CoA. In the second route (e.g. R. palustris),
and Young 1998; Schink et al. 2000). cyclohex-1-ene-1-carboxyl-CoA is hydrated and then reduced
Starting from the initial reaction, the enzyme to 2-ketocyclohexane-1-carboxyl-CoA. The ring is then hy-
phenylphosphate synthase is composed of three different sub- drolysed to form pimeloyl-CoA, which is in turn reduced and
units and encoded by the genes ppsAB and often PpsC (e.g. in hydrated to 3-hydroxypimelyl-CoA. The two pathways then
T. aromatica) (Schmeling et al. 2004; Narmandakh et al. proceed with the degradation to acetyl CoA (Laempe et al.
2006; Schleinitz et al. 2009). The phenylphosphate carboxyl- 1998, 1999; Kuntze et al. 2008). The benzoyl-CoA reductase
ase, the second enzyme of the route, is then encoded by the catalysing the first step of the benzoyl-CoA degradation path-
gene ppcABCD, ppcAC genes can be lacking but, for example way is present in two forms: a four subunit class I ATP-
in G. metallireducens, they have been found to be replaced by dependent reductase for facultative anaerobes and encoded
genes located in the genome (Schühle and Fuchs 2004; by bcrABCD in T. aromatica, badDEFG in R. palustris and
Schleinitz et al. 2009). Generally, ppsABC and ppcABCD bzdNOPQ in Azoarcus sp.; or an ATP-independent class II
can be found clustered together in one operon preceded by a reductase within obligate anaerobes (gene bamBCDEFGHI).
gene regulated by the presence of phenol (and/or benzoate in Both classes are extremly sensitive to molecular oxygen
G. metallireducens) with also a possible posttranscriptional (Carmona et al. 2009; Kung et al. 2009; Löffler et al. 2011;
Fig. 1 Anaerobic phenol

degradation pathways via 4-
hydroxybenzoate and via
caproate
Fig. 2 Anaerobic benzoyl-CoA degradation pathways
Boll et al. 2014; Tremblay and Zhang, 2017). Known genes (Karlsson et al. 1999; Fang et al. 2006; Zhang et al. 2005;
for the following part of the first route include dch Levén and Schnürer 2005; Levén et al. 2006; Chen et al.
(T. aromatica)/bamR (G. metallireducens) for the 2008; Limam et al. 2013) but is also possible under thermo-
cyclohexa-1,5-diene-1-carbonyl-CoA hydratase and had philic conditions (Hoyos-Hernandez et al. 2014; Muñoz Sierra
(T. aromatica)/bamQ (G. metallireducens) for the 6- et al. 2020). Within this pathway, phenol is firstly reduced to
hydroxycylohex-1-en-1-carbonyl-CoA dehydrogenase cyclohexanone in the presence of nitrate and secondly to n-
(Schleinitz et al. 2009; Boll et al. 2014). The ring caproate. N-caproate is then β-oxidised to fatty acids (Fig. 1).
hydrolisation carried out by the enzyme 6-oxocylcohex-1- Microbial communities involved in thermophilic degrada-
ene-1-carbonyl-CoA hydrolase is encoded by the gene oah tion have not been yet fully characterised and identified (Fang
(T. aromatica)/bamA (G. metallireducens) (Kuntze et al. et al. 2006). Azoarcus sp. strain CC-26, was a rare case of a
2008, 2011). The second route of the pathway is mainly car- bacterium found to use both phenol and caproate as substrate
ried out in Rhodopseudomonas strains and includes the genes under denitrifying conditions (Shinoda et al. 2000). Chen et al.
badK, badH, and badI, which are organised in a single operon (2008) highlighted the long acclimation times of cultures to
(Egland et al. 1997). Sequence for the benzoyl-CoA reductase thermophilic conditions probably due to the low abundance of
genes of both classes were found in most facultative anaerobes thermophiles and their slow growth. Concerning the degrada-
degrading aromatic compounds (e.g. the genera Azoarcus, tion rates, contrasting results have been reported and further
Magnetospirillum and Thauera) (known exception investigations are required. Mesophilic conditions (37 °C)
Rhodopseudomonas) (Gibson and Harwood 2002; Lopez were found to have a higher phenol degradation in a UASB
Barragan et al. 2004). The bamA gene, mainly, together with reactor (Fang et al. 1996, 2006). This has been also observed
the bamB, bcrC, and bzdN genes, has been therefore used as in a recent study (Khan et al. 2020) and explained by the
an indicator of the ability of the system to degrade phenol higher relative abundance of methanogens
through PCR assays (Hosoda et al. 2005; Kuntze et al. 2011; (Methanomicrobium, Methanosarcina, Methanosaeta, and
Franchi et al. 2018). Methanococcus). However, other studies in high-rate bioreac-
tors observed a higher effluent quality, degradation rate of
phenol, and methane production for thermophilic anaerobic
Anaerobic phenol degradation pathway via caproate
digestion (Wang et al. 2011; Ramakrishnan and Surampalli
2013).
A second pathway, reported for anaerobic phenol degradation,
is via caproate to acetate. Anaerobic phenol degradation path-
way via caproate is still a relatively unknown process as the
accumulation of intermediate products is hindered by fast deg- Anaerobic biodegradation kinetics
radation rates therefore preventing in-depth studies (Hoyos-
Hernandez et al. 2014). This pathway is known to occur under Anaerobic biodegradation of phenol is certainly a promising
thermophilic conditions (55 °C) while the aforementioned process whose investigation is largely justified by the sustain-
pathway generally occurs mostly under mesophilic conditions ability of the approach and by the potential energy recovery,
but in spite of these attractive features, the low anaerobic environment characterised by the absence of oxygen and the
kinetics is still a drawback. Table 1 summarises the kinetic excess of NO3−, so under not strictly anaerobic conditions.
data reported in the specialised literature for anaerobic phenol For the kinetics characterisation data of consortia, there is
biodegradation for pure cultures and consortia. Studies have not a clear evidence of which process, between metabolic and
been conducted on metabolic processes, i.e. with phenol as the co-metabolic, enables a faster removal. The predominant trait
only substrate as the source of carbon and energy, and on co- in both cases is the marked variability of all parameters de-
metabolic processes, i.e. in presence of an additional growth- pending on the operating conditions. μmax and k values for
supporting substrate. acclimated biomass differ by one order of magnitude with
The first observation is that there is a small number of higher values obtained for granular biomass and longer accli-
studies reporting a complete characterisation of the biomass mation periods. KI exhibits a similar variability with values
kinetics (especially for pure cultures), which may be attribut- ranging from strongly inhibitory (12–36 mg L−1) to practically
able to the long acclimation periods required to reach appre- no-inhibitory (16000–18000 mg L−1) conditions.
pffiffiffiffiffiffiffiffiffiffiffiffi
ciable removal rates. The generally applied kinetic model for C*, defined by K S ∙K I , i.e. the concentration correspond-
biomass characterisation is the Haldane equation (Haldane ing to the maximum removal rate (rC*), is an interesting pa-
1965) derived by the Monod equation including a substrate- rameter to evaluate the process applicability as function of the
inhibition term (S2/KI). pollutant load. Low C* values in the order of 3–30 mg L−1
The substrate consumption rate is given by: demonstrate the limited applicability to most industrial waste-
water whose concentrations are consistently higher.
dS kSX
¼− Promising C* values, in the order of 5000–6600 mg L−1 for
dt S2
S þ KS þ co-metabolic and metabolic processes respectively, are report-
KI ed in a recent article (Mosca Angelucci et al. 2020) where they
where S and X are the substrate and the biomass concentra- were obtained with a biomass acclimated for 2–4 months in a
tions, respectively, k is the maximum specific substrate bio- sequencing batch reactor (SBR). The reduced inhibition effect
degradation rate, and Ks and KI are the half-saturation and in this case could be explained by the dynamic conditions of
inhibition constants, respectively. The corresponding equation the acclimatisation period, which have been demonstrated ef-
for the biomass specific growth rate (μ) is: fective in the biodegradation of biorefractory and toxic com-
pounds (Tomei and Annesini 2005; Mosca Angelucci and
dX S kS Tomei 2015). Removal rates corresponding to C*, rC*, are
μ¼ ¼ μmax −b ¼ Y −b
Xdt S2
S2 in the range of 0.012–0.034 (mgPh mgVSS−1 h−1) and 0.02-
S þ KS þ S þ KS þ
KI KI 0.11 (mgPh mgDW−1 h−1) for co-metabolic and metabolic pro-
cesses, respectively. As observed for other kinetic parameters,
where Y is the growth yield coefficient, b the endogenous the wide interval of values of rC* for metabolic processes is
decay rate, and μmax the maximum specific growth rate. mainly determined by the length of the acclimatisation phase.
Haldane characteristic parameters are reported in Table 1 A general overview of the dependence of the anaerobic
with the range of investigated concentrations and relevant in- removal rate on phenol concentration is shown in Fig. 3 a
formation on the origin of the inoculum and on the acclima- and b for co-metabolic and metabolic processes respectively.
tion procedure. A first observation is that all the studies are Phenol-specific biodegradation rates plotted in Fig. 3 have
conducted under mesophilic and neutral pH conditions. been evaluated from the data of k or μmax and Y (biomass yield
Biomass is expressed in different units as dry weight (DW), coefficient) reported in the studies of Table 1. In order to
volatile suspended solids (VSS), and total suspended solids compare homogeneous data, mgPh mgVSS−1 h−1 units have
(TSS). Comparative data analysis is difficult because of the been converted to mgPh mgDW−1 h−1 by assuming a VSS/
different operating conditions and inoculum properties, lead- TSS ratio of 0.8 for suspended biomass systems (Ekama and
ing to a wide range of values observed for all the kinetic Wentzel 2004) and 0.84 for granular systems (Jahn et al.
parameters. 2019). In Fig. 3a, we observe two inhibited kinetic curves
Characteristic parameters of pure cultures show higher following the Haldane model with low C* values (28–
μmax values than consortia, but KI values (quantifying the 201 mg L−1) and a not inhibited kinetics following the
inhibitory effects) for pure cultures highlighted the presence Monod model. In Fig. 3b, rate vs. concentration curves, in
of inhibition even at relatively low concentrations with C* strictly anaerobic conditions, show, in most cases, the typical
values in the range of 40–170 mg L−1. Moreover, it is worth trend of substrate-inhibited kinetics with the only exception of
noting that the high removal rates (k = 0.505 (mgPh mgDW−1 Mosca Angelucci et al. (2020). The performance of the con-
h−1) reported in Thomas et al. (2002) for Enterobacter and sortia in metabolic biodegradation is strongly affected by sub-
Alcaligenes faecalis have been determined in a reaction strate concentration. In the low range of concentrations (≤
Table 1 Comparison of kinetics parameters and operating conditions tested for anaerobic phenol biodegradation for microbial consortia and pure species
Phenol Co-substrate T pH k μmax Ks Ki C* rC* μC* Origin of inoculum and acclimation References
concentration range (concentration (°C) (mgPh mgDW−1 h−1) (h-1) (mg L−1) (mg L−1) (mg L−1) (mgPh mgDW−1 h−1) (h−1)
(mg L−1) value/range)
(mg L−1)
Co-metabolism—consortia
50–1000 Glucose (0–1500), 26 ± 1 7 – 0.065 20.24 200 63.6 – 0.040 Pulp and paper WWTP Firozjaee et al. (2011)
yeast (800) Acclimation 2 months
Batch tests
25–1000 Glucose (1800), 23 ± 2 7 – 0.01 27.04 127.55 58.7 – 0.005 Coke oven effluent Pishgar et al. (2012)
yeast (1450) No acclimation with phenol
(only glucose)
Batch tests
400–1000 Glucose (1880) 37 7.5 0.029 – 1599.5 16500 5137.3 0.018 – DS from a digester treating Mosca Angelucci
food waste and domestic WW et al. (2020)
Acclimation 2 months in SBR
Appl Microbiol Biotechnol (2021) 105:2195–2224
Batch tests in SBR

0–950 Sucrose (0–2000), 37 8.1 0.240a – 352.1 115 201.2 0.025a – Methanogenic sludge (WWTP) + Chen et al. (2016)b;
m-cresol (0–350) partially GS from UASB treating Zhou and Fang
sucrose WW; (1997)
Acclimation 4 months in UASB;
Batch tests in UASB
600 m-Cresol (200–800) 37 8.1 0.264a – 68.75 11.67 28.3 0.012a– – Methanogenic sludge (WWTP) + Chen et al. (2016)b;
0.034a partially GS from UASB treating Zhou and Fang
sucrose WW (1997)
Acclimation 4 months in UASB
Batch tests in UASB
0–300c Lactate (1500), 30 7 – 0.04 58.22 36.25 45.9 – 0.011 AS from municipal WWTP Mohanty et al. (2018)
sulphate (1000) No acclimation
Batch tests
Metabolism—consortia
25–1500 – 35 7 0.022a 0.004 0.03 363 3.3 0.022a 0.004 Anaerobic sludge already adapted Suidan et al. (1988)
to phenolics from AFBR treating
coal gasification WW
Acclimation 1 year in CSTR
Batch tests
400–1000 – 37 7.5 0.036 – 2384.2 18209 6588.9 0.021 – DS from a digester treating food Mosca Angelucci
waste and domestic WW et al. (2020)
Acclimation 4 months in SBR
Batch tests in SBR
200 – 35 ± 1 7.1 0.165 0.012 3.8 – – – – DS from a digester treating fructose Lin et al. (2009)d
processing WW
Acclimation (not specified period)
Batch tests
20–2000 – 37 – 0.035e – 90 900 285 0.026e – DS from a municipal WWTP Dwyer et al. (1986)
Acclimation 2 years
Batch tests with free cells
20–2000 – 37 – 0.021e – 46 1720 282 0.017e – DS from a municipal WWTP Dwyer et al. (1986)
Acclimation 2 years
Batch tests with immobilised cells
198 – 35 – 0.0167a – 19.9 336 81.8 0.011a – Anaerobic sludge already adapted to Chou and Huang
phenol (2005)
Acclimation 3 months in UASB
Batch tests with biomass after granules
break up
60–450 – 35 – 0.017a – 25 318 89.2 0.011a – Sludge from piggery WWTP Chou et al. (2008)
Acclimation and operation (4 years)
in EGSB
2201
Table 1 (continued)
2202
Phenol Co-substrate T pH k μmax Ks Ki C* rC* μC* Origin of inoculum and acclimation References
concentration range (concentration (°C) (mgPh mgDW−1 h−1) (h-1) (mg L−1) (mg L−1) (mg L−1) (mgPh mgDW−1 h−1) (h−1)
(mg L−1) value/range)
(mg L−1)
Batch tests with biomass after break up

granules
f
188 – 25 7 0.159 0.091 4.91 101 22.3 0.111 0.063 Denitrifying bacteria from a Khouri et al. (1992)
domestic WWTP
Acclimation firstly under aerobic
then anoxic conditions for 2 years
Batch tests
440–1920g – – – 0.333 0.04 560 – – – – DS from a municipal WWTP Logan et al. (1998)d
No acclimation
Batch tests
200–5500c – 35 – 0.279a 0.019 3.85 – – – – DS from a municipal WWTP Lin and Lee (2001)d
Acclimation under sulphate-reducing
conditions in fixed biofilm column
reactor
Batch tests
Metabolism—pure species
300–1000 – 27 7 – 0.031 63.9 450 169.6 – 0.018 Pseudomonas putida (PTCC 1694); Bakhshi et al. (2011)
No acclimation;
Batch tests
0–1800 – 35 7 – 0.315 19.54 208.57 63.8 – 0.195 Candida albicans (PDY-07) isolated Wang et al. (2008)
from AS produced in a refinery plant
No acclimation
Batch tests
18–230f – 35 7.4 0.505 0.206 15 113 41.2 0.292 0.119 Enterobacter + Alcaligenes faecalis Thomas et al. (2002)
isolated from nitrogen-sparged coke
oven waste slurry
Acclimation 1 year (before isolating
pure species)
Batch tests
a
(mgPh mgVSS−1 h−1 )
b
Modified Haldane equation [dS/dt = k X S/(S + KS + S2 /Ki +IS)] by Chen et al. (2016) including an interactive parameter (I) quantifying the inhibitory degradation between phenol and m-cresol
c
In presence of sulphates
d
Monod equation
e
(mgPh mgprotein−1 h−1 )
f
In presence of nitrates
g
In presence of chlorates
Abbreviations: AFBR anaerobic fluidised bed reactor, AS activated sludge, CSTR continuously stirred tank reactor, DS digested sludge, DW dry weight, EGSB expanded granular sludge bed, GS granular
sludge, Ph phenol, SBR sequencing batch reactor, T temperature, UASB up-flow anaerobic sludge blanket, WW wastewater, WWTP wastewater treatment plant
Fig. 3 Anaerobic specific

biodegradation rates of phenol in
co-metabolic (a) and metabolic
(b) processes in mesophilic
conditions as a function of phenol
concentration. In plot (a), 1:
Mosca Angelucci et al. (2020), 2:
Chen et al. (2016) with sucrose
and m-cresol as co-substrates, 3:
Chen et al. (2016) with m-cresol
as co-substrate. In plot (b), 1:
Mosca Angelucci et al. (2020), 4:
Suidan et al. (1988), 5: Chou and
Huang (2005), 6: Chou et al.
(2008), 7: Khouri et al. (1992), 8:
Logan et al. (1998), 9: Lin and
Lee (2001), 10: Enterobacter and
Alcaligenes faecalis, Thomas
et al. (2002). In plot (b),
continuous lines are referred to as
left y-axis while dashed lines are
referred to as right y-axis
200 mg L−1), some of the inhibited kinetics (Suidan et al. mesophilic temperatures and to a more extended time period
1988; Chou and Huang 2005) are still suitable for application for the thermophilic ones. Aerobic biodegradation of phenol
with rate values even higher than the Monod kinetics. At has been extensively investigated and its feasibility via meta-
higher concentrations, inhibition phenomena reduce the pro- bolic pathways has been demonstrated by many authors. The
cess rate at such low values that the process applicability is good performance of aerobic metabolic processes justifies the
seriously limited. Moreover, it is worth noting that higher rate few studies on co-metabolic systems, which can however be
values are observed in presence of weak oxidizing agents such interesting when the additional “primary” substrate is present
as nitrate (Khouri et al. 1992; Thomas et al. 2002), sulphate together with phenol in the wastewater. As for anaerobic data,
(Lin and Lee 2001), and chlorate (Logan et al. 1998). These most of the aerobic studies are related to mesophilic tempera-
conditions are of special interest when these compounds are ture regime, even if several authors tested more extended tem-
present in phenolic wastewaters that require treatment as they perature range of values, comprised in the interval 2.5–50 °C
could significantly increase the process kinetics at values two, (Banerjee and Ghoshal 2010; Li et al. 2010; Wang et al. 2010;
three times higher than the ones detected under fully anaerobic Duan 2011; Zhai et al. 2012; Mao et al. 2015; Lin and Cheng
conditions. 2020; Panigrahy et al. 2020). Nevertheless, in all the men-
tioned studies, kinetic characterisation has been conducted
only at the optimal temperature reported in Table 2. Similar
Comparison between anaerobic and aerobic kinetics for aerobic co-metabolic and metabolic processes are
processes highlighted in Fig. 4 a and b (plotted by applying the same
criterion of unit conversion described for Fig. 3) showing the
Table 2 shows a summary of the kinetic parameters for phenol curves rate-concentration in the temperature range of 15–37
biodegradation under aerobic conditions: given the high num- °C. In both co-metabolic and metabolic processes, we observe
ber of published articles on this topic, the studies reported in a maximum rate of ~ 0.3 (0.276–0.295) (mgPh mgDW−1 h−1)
the table (and employed for the comparison with the anaerobic and C* in the range of 112–162 mg L−1 (Sharma et al. 2012;
process) refer to the last ten years for psychrophilic and Wang et al. 2010). Higher rates are reported only for pure
Table 2 Comparison of kinetics parameters and operating conditions tested for aerobic phenol biodegradation for microbial consortia and pure species
2204
Phenol concentration T pH k μmax Ks Ki C* rC* μC* Origin of inoculum and acclimation References
range (and co-substrate) (°C) (mgPh mgDW−1 h−1) (h−1) (mg L−1) (mg L−1) (mg L−1) (mgPh mgDW−1 h−1) (h−1)
(mg L−1)
Co-metabolism—consortia and pure species

0–1050 – 7.5 – 0.092 2.64 2623 83.2 – 0.865 Municipal WWTP Lim et al. (2013)
Co-substrates: Acclimation 5 months in SBR
peptone (32),
sucrose (109),
and sodium acetate (56)
100–400 30 – 0.5841 – 348.5 158.6 235.1 0.121–0.140 – Effluent of a coke oven WWTP Dey and Mukherjee (2013)a
Co-substrate: resorcinol (100–400) Acclimation 6 months
100–1800 37 5 0.772 0.312 130.4 200 161.5 0.295 0.119 Paecilomyces variotii JH6 Wang et al. (2010)
Co-substrate: glucose (100) isolated from AS of coking
WWTP
Acclimation (not specified
period)
Metabolism—consortia
100–1000 37 7 – 0.347 984.32 463.56 675.5 – 0.089 WW of a refinery plant Pradhan et al. (2012)
Acclimation 1 month
50–1000 20 3.5–7b 0.264 0.119 11.13 250.88 52.8 0.186 0.084 AS from a domestic WWTP Ucun et al. (2010)
Acclimation 5 months in CSTR,
then 2 weeks in batch JLB
200–800 30 7.5 ± 0.5 0.419 0.13 29.1 432.2 112.1 0.276 0.086 AS from a municipal WWTP Sharma et al. (2012)
Acclimation 5 months
100–700 – – 0.463 0.306 257.5 162.6 204.6 0.132 0.087 Effluent of a coke oven WWTP Dey and Mukherjee (2010)
40–350 30 8 – 0.66 76.1 205.4 125 – 0.298 AS from hazardous wastewater Hamitouche et al. (2012)
treatment plant
No acclimation
250–1000 15–18 6 0.521c – 692 231 399.8 0.117c – AS from a municipal WWTP Kamali et al. (2019)
Acclimation 2 months in batch
mode, then in SBR
50–1500 30 5–8 0.47c – 603.99 28.486 131.2 0.046c – AS from a municipal WWTP Duan (2011)
Acclimation 6 weeks in SBR
500–3000 – – – 0.355 603.8 40.603 156.6 – 0.041 AS from a municipal WWTP Hussain et al. (2015)
Acclimation 6.5 months in SBR
c c
500–3000 30 7 0.088 – 198 357 265.9 0.035 – AS of WWTP Ho et al. (2010)
No acclimation
Tests with AS
500–5000 30 7 0.404c – 650 1140 860.8 0.161c – AS of a WWTP Ho et al. (2010)
Granulation in 2 months and
acclimation in 3 months;
Tests with GS
Metabolism—pure species
376–1410 30 – 1.222 0.55 483.82 2582.63 1117.8 0.655 0.295 Acinetobacter johnsonii D1 Heilbuth et al. (2015)
isolated from AS produced
in a steel-mill sewage-treatment
plant
0–1200 30 – – 0.078 568.2 838.9 690.4 – 0.029 Advenella sp. B9 isolated from a Li et al. (2020)
coking WWTP
No acclimation
Table 2 (continued)
(mg L−1)
0–1200 30 – – 0.081 188.1 965.3 426.1 – 0.043 Advenella sp. B9 + Stenotrophomonas Li et al. (2020)
sp. N5 isolated from a coking WWTP
No acclimation
200–1500 25 7 0.975 0.58 10 550 74.2 0.768 0.457 Alcaligenes sp. TW1 isolated from Essam et al. (2010)
AS from a coking WWTP
before isolation
376–1410 30 – 0.738 0.48 469.23 188.2 297.1 0.178 0.115 Alcaligenes faecalis B6-2 isolated Heilbuth et al. (2015)
from AS produced in a steel-mill
sewage-treatment plant
100–2000 37 6.5 – 0.44 129.4 637.8 287.3 – 0.231 Bacillus cereus MTCC 9817 AKG1 Banerjee and Ghoshal (2010)
isolated from a petroleum
refinery WW
100–2000 37 6.5 – 0.933 110.5 494.4 233.7 – 0.480 Bacillus cereus MTCC Banerjee and Ghoshal (2010)
9818 AKG2 isolated from oil
exploration site WW
47–470 65 6 6.75 5.4 3 14 6.5 3.73 2.986 Bacillus thermoleovorans sp. A2 Feitkenhauer et al. (2001)d
isolated from a water and mud
sample from a hot spring
50–800 30 6–7.5 15.92 – 42603 1.1 216.5 0.040 – Candida (immobilised strain) Jiang et al. (2018)
isolated from AS produced in
a pharmaceutical WWTP
No acclimation
500–2400 30 6 0.277 0.341 15.81 169 51.7 0.256 0.211 Candida tropicalis PHB5 isolated Basak et al. (2014)
from coke oven WW
50–1250 25 ± 2 7.5 1.145 0.315 450.61 38.74 132.1 0.146 0.040 Chlorella pyrenoidosa NCIM 2738 Das et al. (2019)
Acclimation 2 weeks
0–1117 30 – 1.244 0.574 20.29 268.1 73.8 0.983 0.370 Glutamicibacter nicotianae Duraisamy et al. (2020)
MSSRFPD35 isolated from
Canna indica rhizosphere grown
in distillery effluent contaminated sites
Acclimation 3 days
50–2000 36 7.5 0.876 0.601 70.87 418.2 172.2 0.536 0.330 Gulosibacter sp. YZ4 isolated from Zhai et al. (2012)
AS from a coking WWTP
Acclimation 2 months before isolation
20–1000 30 7 0.610 0.243 25.7 156.3 63.4 0.337 0.134 Microbacterium oxydans LY1 isolated Wang et al. (2016)
in sediment in the industry-effluent
dump sites of an industrial area
Acclimation 2.5 months
20–1800 35 7.5 – 0.092 22.517 1126.73 159.3 – 0.072 Pseudochrobactrum sp. XF1 isolated Mao et al. (2015)
from AS produced in a coking WWTP
20–1800 35 7.5 – 0.11 23.934 1579.13 194.4 – 0.088 Pseudochrobactrum sp. XF1-UV Mao et al. (2015)
isolated from AS produced in a
2205
Table 2 (continued)
2206
(mg L−1)
coking WWTP and subjected to

mutation by UV radiation
50–1600 35 7–7.2 – 2.5 48.7 100.6 70.0 – 1.045 Pseudomonas aeruginosa WUST-C1 Liu et al. (2013)
isolated from AS of a coke plant
Acclimation 2 weeks
50–1500 35 7.4 – 0.246 14.85 890 115.0 – 0.195 Pseudomonas citronellolis NS1 Panigrahy et al. (2020)
isolated from a coke oven WW
Acclimation 2.3 months
400–1200 28 6.5–7 0.2336 0.361 36.69 181.5 81.6 0.123 0.191 Pseudomonas fluorescens MTCC Begun and Radha (2013)
103 (free cells)
Acclimation in batch mode
Tests batch in IFBBR
400–1200 28 6.5–7 0.557 0.618 14.58 – – – – Pseudomonas fluorescens MTCC Begun and Radha (2013)e
103 (biofilm)
Acclimation in batch mode before
developing a biofilm on
low-density polystirene beads
Tests batch in IFBBR
0–1400 30 7.2 0.972 0.275 6.9 530.7 60.5 0.791 0.224 Pseudomonas putida cbp1-3 isolated Liu et al. (2012)
from AS of a coking WWTP
and coking WW
Acclimation 1 month
68–563 30 7 0.524 0.31 26.2 255 81.7 0.319 0.189 Pseudomonas putida BCRC 14365 Lin and Cheng (2020)
1-day adaptation
10–400 – – – 0.109 53.18 148.65 88.9 – 0.050 Pseudomonas putida MTCC 1194 Mathur and Majumder (2010)
Acclimation (not specified period) in
CSTR with benzene and toluene
0–800 25 7.1–7.3 0.539 0.217 24.4 121.7 54.5 0.284 0.114 Pseudomonas putida LY1 isolated Li et al. (2010)
from river sediments
No acclimation
51–745 80 3.2 0.1133 0.094 77.7 319.4 157.5 0.0570 0.047 Sulfolobus solfataricus 98/2 Christen et al. (2012)
a
Modified Haldane equation [dSi/dt = ki X Si/(Si + KS,i + Si2 /Ki,i +Ii,jSj)] by Dey and Mukherjee (2013) including an interactive parameter (Ii,j) quantifying the mutual inhibitory effect on biodegradation of
phenol (Si) and resorcinol (Sj)
b
Not controlled
c
(mgPh mgVSS−1 h−1 )
d
Modified Haldane equation [μ = μmax S (1 + S/K)/(S + KS + S2 /KI)] by Feitkenhauer et al. (2001) including an additional inhibition constant K
e
Monod equation
Abbreviations: AS activated sludge; CSTR continuously stirred tank reactor; DW dry weight; GS granular sludge; IFBBR inverse fluidised bed biofilm reactor; JLB jet loop bioreactor; Ph phenol; SBR
sequencing batch reactor; T temperature; WW wastewater; WWTP wastewater treatment plant
species, e.g. Bacillus thermoleovorans sp. A2 is able to reach activity on the strategies to enhance the anaerobic process
rc* values of 3.73 mgPh mgDW−1 h−1 but at lower C* concen- performance. Possible interventions can be realised both on
tration (6.5 mg L−1) and thermophilic conditions (T = 65 °C), the technologies applied and on the improvement of the per-
as reported in Table 2 (Feitkenhauer et al. 2001). formance of bacterial cultures.
As observed for the anaerobic process, aerobic kinetics are
also characterised by a wide range of values (variations up to
one order of magnitude) for the rate constant k and the max- How to improve the anaerobic process
imum growth rate μmax depending on the operating condi- performance?
tions, the origin of the inoculum, and the acclimatisation pro-
cedure. Unlike the anaerobic process, many aerobic bacterial Advanced technologies
isolates can provide effective aerobic phenol biodegradation at
kinetics on average higher than the consortia ones. This is So far, most of the applications of the anaerobic process to
highlighted by the comparison of the curves of rate vs. con- phenol and phenolic compound removal are at the laboratory
centration reported in Fig. 4 b and c showing maximum re- scale with only a few examples of larger scale plants reported
moval rates for pure cultures which were three times higher in the scientific literature. Chen et al. (2009) investigated a
(0.982 vs 0.276 mgPh mgDW−1 h−1, for Duraisamy et al. (2020) full-scale GAC-AFBR (275-m3 working volume) treating
and Sharma et al. (2012) respectively) than the consortia rates. wastewater from manufacturing of phenolic resins located in
Inhibitory effects are evident also for aerobic processes Taiwan. This reactor treated an influent at a concentration of
both in pure cultures and consortia with values of KI at the 2.5–3 gCOD L−1 (approximately 60% of the content is made of
lower end of the range and equal to 28–41 mg L−1 for consor- phenolic compounds and 5% of formaldehyde) and was
tia and to 1–39 mg L−1 for pure cultures. characterised by a chemical oxygen demand (COD) removal
In order to make easier the comparison between anaerobic efficiency of ~ 85% with an organic loading rate (OLR) of 3–5
and aerobic performance for phenol biodegradation, Fig. 5 gCOD L−1 d−1. Other full-scale anaerobic plants were based on
shows specific biodegradation rates of microbial consortia the treatment of wastewater containing phenol and other sub-
for two different phenol concentrations, 100 and 1000 mg strates with co-metabolic processes. In a review of applica-
L−1. Also, in this case, available data have been converted to tions of anaerobic treatments to chemical and petrochemical
the same units. In Fig. 5a, a better performance is observed for wastewater treatment, Macarie (2000) identified only one full-
the microbial consortium originated from the effluent of a scale UASB (1.28 m 3 working volume) in Rotterdam
coke oven WWTP (Dey and Mukherjee 2013), but the com- (Netherlands) treating phenol wastewater characterised by a
parison is not so meaningful given the low number of co- COD content of 30 gCOD L−1 mostly consisting of volatile
metabolic studies under aerobic conditions. More significant fatty acids (VFAs) and of a minor fraction of phenol. Other
is the comparison for metabolic processes (Fig. 5b). At high full-scale plants were reported for the treatment of coking
concentration (1000 mg L−1) in most of the cases, aerobic wastewater (containing 18–567 mg L−1 of phenol, 89–
removal rates are higher than the anaerobic ones. There are 790 mg L−1 of ammonium, 29–616 mg L−1 of cyanide, and
only two exceptions to this trend: Ho et al. (2010) and Duan a total COD in the range of 940–2900 mg L−1). These reactors
(2011) reported aerobic rate values in the range of 0.01–0.018 were operated with sequential anaerobic-aerobic systems usu-
mgPh mgDW−1 h−1 and comparable with the values reported ally combined with tertiary filtration units (from ultrafiltration
for anaerobic conditions (i.e. 0.01 mgPh mgDW−1 h−1) by to reverse osmosis) (Jin et al. 2013; Ren et al. 2019).
Mosca Angelucci et al. (2020). At low concentration To the best of our knowledge, there are no other
(100 mg L−1), even if the aerobic process still shows a better implementations of full-scale anaerobic plants, in spite of the
performance, improved anaerobic rates are observed in re- promising results achieved with pilot- and bench-scale biore-
spect to the higher concentration, with an increase from 0.04 actors, as reported in Table 3. Different bioreactors have been
to 0.09 mgPh mgDW−1 h−1 (Chou and Huang 2005) and from tested from conventional systems such as CSTR and SBR to
0.06 to 0.017 mgPh mgDW−1 h−1 (Suidan et al. 1988). It is high-rate anaerobic reactors, including AnMBR, anaerobic
worth noting that the presence of nitrates, sulphates and chlo- biological activated carbon reactor (AnBAC), AFBR, anaero-
rates (Khouri et al. 1992; Logan et al. 1998; Lin and Lee 2001) bic immobilised fluidised bed reactor (AIFBR), EGSB, and
can increase the process kinetics at values even higher than the UASB. Table 3 summarises significant data of these technol-
aerobic ones. ogies, i.e. influent concentrations, operating conditions, ap-
The comparison of the two biodegradation alternatives plied OLRs, phenol and COD removal efficiencies (RE), phe-
clearly highlights the higher biodegradation rates of the aero- nol removal rate, and biogas production. Most of these studies
bic process, but the good results achieved with the anaerobic have been conducted on both co-metabolic and metabolic
systems in several cases and the additional advantages of a processes under mesophilic conditions (i.e. 30–37 °C) and
more sustainable process justify the challenging research all of them with adapted microbial consortia. Moreover, the
Fig. 4 Aerobic specific

biodegradation rates of phenol in
co-metabolic (a) and metabolic
processes in psychrophilic and
mesophilic conditions for
microbial consortia (b) and pure
species (c) as a function of phenol
concentration. In plot (a), 1:
Paecilomyces variotii JH6 Wang
et al. (2010), 2: Dey and
Mukherjee (2013). In plot (b), 3:
Ucun et al. (2010), 4: Dey and
Mukherjee (2010), 5: Kamali
et al. (2019), 6: Duan (2011), 7:
AS, Ho et al. (2010), 8: GS, Ho
et al. (2010), 9: Sharma et al.
(2012). In plot (c), 10:
Pseudomonas putida cbp1-3, Liu
et al. (2012), 11: Pseudomonas
putida BCRC 14365, Lin and
Cheng (2020), 12: Pseudomonas
fluorescens MTCC 103 (free
cells), Begun and Radha (2013),
13: Pseudomonas fluorescens
MTCC 103 (biofilm), Begun and
Radha (2013), 14: Candida
(immobilised strain), Jiang et al.
(2018), 15: Candida tropicalis
PHB5, Basak et al. (2014), 16:
Microbacterium oxydans LY1,
Wang et al. (2016), 17: Chlorella
pyrenoidosa NCIM 2738, Das
et al. (2019), 18: Pseudomonas
putida LY1, Li et al. (2010), 19:
Glutamicibacter nicotianae
MSSRFPD35, Duraisamy et al.
(2020), 20: Alcaligenes sp. TW1,
Essam et al. (2010), 21:
Gulosibacter sp. YZ4, Zhai et al.
(2012), 22: Alcaligenes faecalis
B6-2, Heilbuth et al. (2015), 23:
Acinetobacter johnsonii D1,
Heilbuth et al. (2015)
majority of studies listed in Table 3 tested synthetic wastewa- these effluents are typical examples of phenolic wastewater,
ter, with some exceptions including real wastewater from phe- whose major organic constituents (in the range of 45-85%) are
nolic resin production (Goeddertz et al. 1990), refinery spent phenol and its substituted compounds (Pradeep et al. 2015).
caustics mixed with sour waters containing a mixture of phe- The two highest influent concentrations of phenol used
nolics (Almendariz et al. 2005), and wastewater originating were 12000 mg L−1 (Goeddertz et al. 1990) and 2000 mg
from coal conversion processes (Wang et al. 2011; L−1 (Mosca Angelucci et al. 2020) for co-metabolic and met-
Ramakrishnan and Surampalli 2013). It is worth noting that abolic processes, respectively. Phenol removal efficiencies are
Fig. 5 Comparison of aerobic and anaerobic specific biodegradation rates co-substrates, 3: Chen et al. (2016) with m-cresol as co-substrate, 4:
of phenol in co-metabolic (a) and metabolic (b) processes in Mosca Angelucci et al. (2020). In plot (b), 5: Ucun et al. (2010), 6:
psychrophilic and mesophilic conditions for microbial consortia. Filled Sharma et al. (2012), 7: Dey and Mukherjee (2010), 8: Kamali et al.
bars stand for anaerobic studies, dashed bars represent studies in the (2019), 9: Duan (2011), 10: AS, Ho et al. (2010), 11: GS, Ho et al.
presence of chlorate, nitrate, or sulphate (as highlighted by the number (2010), 12: Logan et al. (1998), 13: Lin and Lee (2001), 14: Khouri
signs) while empty bars are referred to the aerobic ones. In plot (a), 1: Dey et al. (1992), 15: Chou and Huang (2005), 16: Suidan et al. (1988), 4:
and Mukherjee (2013), 2: Chen et al. (2016) with sucrose and m-cresol as Mosca Angelucci et al. (2020)
in the range of 70–100% for most of the studies with some AnMBR systems. Given its demonstrated high potentialities
cases of lower values due to high applied OLRs (Razo-Flores in many applications of the anaerobic process, UASB is the
et al. 2003; Gali et al. 2006; Chou et al. 2008; Bajaj et al. 2009; most investigated technology for phenolic wastewater
Firozjaee et al. 2013; Na et al. 2016) or low HRTs (Fang et al. treatment and the published studies are mainly focused on
2006; Pishgar et al. 2014). A reliable comparison among dif- the optimisation of the process performance. In a review
ferent technologies is not straightforward given the different article, Veeresh et al. (2005) analysed the bench-scale appli-
operating conditions and the difficulties in taking into account cations of UASBs operated with granular biomass to anaero-
all the specific factors affecting the reactor performance such bic phenol and cresol removal and identified some drawbacks
as the biomass concentration and activity, the dynamic load- related to the long acclimation period, the slow granulation,
ing applied, and wastewater composition. As expected con- and the sensitivity to temperature and shock loading. They
ventional systems (SBR and CSTR) exhibit in general lower suggested effluent recirculation and/or supplementing a co-
process performance with respect to high-rate bioreactors substrate to overcome these problems. Other authors investi-
even if the SBR shows, in some cases, quite good results in gated the effect of operating parameters such as temperature
terms of phenol RE and biogas production (Rosenkranz et al. (Fang et al. 1996, 2004, 2006; Wang et al. 2011), HRT (Na
2013; Mosca Angelucci et al. 2020). et al. 2016; Wang et al. 2011), and recirculation ratio (Lay and
For high-rate bioreactors, best performance in terms of RE Cheng 1998; Wang et al. 2011). Particular attention has been
and phenol removal rate is observed for UASB, EGSB, and paid to the influence of operating temperature on process
Table 3 Comparison of efficiencies and operating conditions tested with different anaerobic technologies applied to phenol removal. Where not specified the study has been performed on synthetic
2210
wastewater
Technology Volume Start-up Phenol COD influent OLR HRT Phenol Specific Phenol COD Biogas Note Reference
(scale (months) influent concentration (gCOD L−1 (d) removal phenol RE RE production
application) concentration (gCOD L−1) d−1) rate removal rate (%) (%) rate
(L) (mgPh L−1) (mgPh L−1 (mgPh gVSS−1 (L L−1 d−1)
d−1) d−1)
Co-metabolism
SBR 1 (B) 2 200–2000 4.6–11.2 2.3–5.6 2 83–729 11–89 70–86 63–82 1.1–1.4 Co-substrate: Glucose Mosca Angelucci
(1.9 g L−1)
et al. (2020)
T: 37 °C
Phenol removal rates
from batch tests in SBR
AFBR 1.8 (B) 1+7 13–2090 1.7–6.6a 3.9–15.5b 0.43 ~ 180–380 – > 95 > 96c 1.4–4.4 Co-substrate: mixture Carbajo et al.
of VFAs (1.1 g L−1)
(2010)
(acetic:propionic:
butyrric 2:1:1 expressed
as TOC)
Carrier material: Biolite®
T: 32 °C
Phenol removal rate from
batch tests in AFBR
AFxBR 2.4 (B) 2.4 190–4700 4.3–14.2 0.9–5.7 2.5 1485 – 89–99 87–99 ~ 0.25–2.25 Co-substrate: Glucose Bajaj et al.
(4 g L−1)
(2009)
Carrier material: Liapor
clay beads
T: 37 °C
AnBAC 0.9–2.2 (B) 3 275–1650 1–6 ~ 1.4–8 0.3–4.7 – – > 99 50–98 ~ 0.6–2.9 Real phenolic resin Goeddertz et al.
production WW
(1990)
containing phenol,
formaldehyde (2–3 g L−1),
methanol (2–2.5 g L−1)
AC: Calgon-F-300
T: 35 °C
AnBAC 30 (P) 4 10000–12000 32–40 ~ 4.3–5.7 6.9–9.2 – – >99 98 ~ 1.1-1.3 Real phenolic resin Goeddertz et al.
production WW
(1990)
containing phenol,
formaldehyde (2-3 g L−1),
methanol (2-2.5 g L−1)
AC: Calgon-F-300
T: 35 °C
AnMBR 6.5 (B) ~ 2.7 10–500 2.5–40 0.15–6.24 6.5 31–113 2–12 ~ 85–99 92–99 ~ 0.5–5d Saline WW containing Muñoz Sierra et al.
phenol, SA, yeast
(2018)
extract (2 g L−1)
and Na+ (8–10 g L−1)
Reactor equipped with a
side-stream ultrafiltration
Table 3 (continued)
d−1) d−1)
(tubular PVDF membrane)

module
T: 30 °C
AnMBR 7 (B) 5 500–5000 38.5–53.5 5.5–7.6 7 111–1110 7–87 96–99 70–99 2.1–4.9d Saline WW containing
phenol, SA, yeast Muñoz Sierra
extract (2 g L−1) and et al. (2019)
Na+ (16-26 g L−1)
Reactor equipped with
a side-stream
ultrafiltration (tubular
PVDF membrane) module
T: 35 °C
Biogas production rate
from SMA tests
AnMBR 6.5 (B) ~3 50–800 ~ 13–26 2–4 6.5 – 6–21 24–95 31–95 – Saline WW containing Muñoz Sierra et al.
phenol, SA (10–20 g
(2020)
L−1), yeast extract
(2 g L−1) and Na+
(18 g L−1)
Reactor equipped with
a side-stream ultrafiltration
(tubular PVDF
membrane) module
T: 55 °C
from SMA tests
EGSB-AF 3.5 (B) 9.1 500–1000 5 5–10 0.5 151–788e 43–137 83–99 40–97 1–1.4d Co-substrate: mixture Scully et al.
of VFAs (acetate:butyrate:
(2006)
propionate:ethanol 1:1:1:1
in COD ratio, 5 g L−1)
Hybrid bioreactor consisted
of an upper section
(randomly packed
with PE rings) and
a sludge bed section
in the lower part
T: 10–15 °C
batch tests (T: 15 °C)
EGSB-AF 3.5 (B) 8.2 400–1200 5 5 1 311e 89 71–98 50–90 0.4d,e Co–substrate: mixture Collins et al.
of VFAs (acetate:butyrate:
(2005)
propionate:ethanol
2211
Table 3 (continued)
2212
d−1) d−1)
1:1:1:1 in COD ratio, 2.1–5

gCOD L−1)
Hybrid bioreactor
consisted of an
upper section
(randomly packed
with PE rings) and
a sludge bed section in the
lower part
T: 15–18 °C
Phenol removal rate
from batch tests
(T: 15 °C)
Biogas production
rate from SMA
tests (T: 15 °C)
FxFUAB ~ 0.3 (B) ~4 50–150 – 0.2–2.1f 0.25–0.5 – – 86–99 94 – Co-substrate: proteose Tawfiki Hajji et al.
peptone (0.5 g L−1)
(1999)
or whey (0.5 g L−1)
, p-cresol (35 mg L−1),
o-cresol (35 mg L−1)
T: 29 °C
UASB 2.8 (B) ~1 200 0.8–1.9 2.3–5.4 1 – 103–576 ~ 50–99 – 0.1–0.2 Co-substrate: sucrose Fang and Zhou
(0–1 g L−1) and (1999)
m-cresol (100 mg L−1)
Different concentration of
N-NO3− (250–600 mg L−1)
in WW tested
T: 37 °C
batch tests with sucrose and
m-cresol and in presence
and absence of nitrates
UASB 0.2 (B) 1 280–1260 2000–5000 1.7–9.2 0.5–0.6 – 57–66 ~ 25–99 53–94 0.7–3 Co-substrate: SA (1 g L−1) Razo-Flores et al.
and p-cresol (132 mg L−1)
(2003)
T: 30 °C
Different phenol:p-cresol
ratios tested
batch tests
UASB 2.0 (B) 4 105–1260 1.3–4.1 8 0.5 – – 98 92 ~ 3.5–5 Co-substrate: glucose (1 g L−1) Tay et al. (2001)
T: 37 °C
Table 3 (continued)
d−1) d−1)
UASB 12.5 (P) 7+0.6 252–1345 4 4–8 0.5–1 – – 11–99 16–91 1.5–3 Co-substrate: sugarcane Gali et al. (2006)
molasses (1000–5400
mgCOD L−1)
with different phenol/sugarcane
molasse ratios tested
T: 30 °C
UASB 3.5 (B) – 25–1250 2.97–7.15 1.5–3.6 2 70 22 90–98 95–97 – Saline WW containing SA Wang et al.
(3.85 g L−1), catechol
(2017)
(25–250 mg L−1),
resorcinol (25–250 mg
L−1) and hydroquinone
(25–250 mg L−1)
and Na+ (10–18 g L−1)
T: 37 °C
Phenol removal rate from batch
tests
UASB 7 (B) 5 500–5000 38.5–53.5 5.5–7.6 7 92.6–1064.9 16–103 84–99 47–99 0.6–2.3d Saline WW containing SA, Muñoz Sierra et al.
yeast extract (2 g L−1) and
(2019)
Na+ (16–26 g L−1)
T: 35 °C
from SMA tests
Metabolism
CSTR 17 (P) 1 100–1000 0.2–2.4 0.2–1.9 2–4 – – 0–89 10–56 0.006–0.13 T: 22 °C Firozjaee et al.
Best efficiencies for
(2013)
longest HRT (4 d)
SBR 1 (B) 2.5 2000 4.8 2.4 2 779 121 73 72 0.5 T: 37 °C Mosca Angelucci et al.
Phenol removal rates from
(2020)
batch tests in SBR
SBR 5 (B) 3.4 120–1200 0.29–2.88 0.4–0.8 3–23.5 132–312 11–26 90 – – T: 37 °C Rosenkranz et al.
(2013)
AFxBR 2 (B) ~ 7.6 1316 3.1–3.3 1.3–3.5 2.5 53–91 48–76 ~ 0.25–1.25 Carrier material: Liapor clay Bajaj et al. (2009)
beads
T: 37 °C
AHR 13.5 (P) – 752–1128 2.2–3.5 1.1–8.2 0.5–3 – – 85–92 83–91 ~ 0.2–2d Synthetic and real coal Ramakrishnan and
gasification WW Surampalli (2013)
Hybrid bioreactor a filter
media of PVC rings in
the middle of reactor
height
T: 35 °C
2213
Table 3 (continued)
2214
d−1) d−1)
AHR 13.5 (P) – 752–1128 2.2–3.5 1.1–8.2 0.6–3.1 – – 85–92 87–92 ~ 0.3–2.2d Synthetic and real coal Ramakrishnan and
gasification WW Surampalli (2013)
Hybrid bioreactor a filter
media of PVC rings in the
middle of reactor height
T: 55 °C
AIFBR 3.5 (B) 2.2 720 1.8 0.6–11.3 (18.3) 0.15–3 (0.1) – – 84–98 (30) 79–91 (20) 1.2–7 T: 25 °C Pishgar et al. (2014)
Immobilised microorganisms
entrapped in calcium
alginate gel beads
Data in parentheses are related
to the lowest HRT (0.1 d)
which caused a performance
failure
EGSB 3.4 (B) 1.3 500–1250 2–3 1–1.5 2 – – 20–99 ~ 50–96 ~ 0.3–0.7d Real refinery spent caustics Almendariz et al.
WW and sour waters
(2005)
containing mixture of
phenolics
T: 30 °C
EGSB 3.78 (B) – 630–1930 ~ 1.5–5.1 1.7–4.4 0.4 ~ 1652–4593g 120–160 69–100 – – WW containing yeast extract Chou et al. (2008)
(60–90 mg L−1)
T: 35 °C
HAIBR 2 (B) ~1 50–1200 0.12–2.86 0.2–5.7 0.5 – ~ 25–190 97–99 60–99 – Polyurethane foam matrices
for biomass immobilisation Bolaños et al. (2001)
support
T: 30 °C
UASB 2.8 (B) 4.3 580–900 1.57–2.95 4.4–8.3 1 ~ 60 270 98 – – Co-substrate: m-cresol Zhou and Fang
(200–800 mg L−1) (1997)
T: 37 °C
batch tests
UASB ~ 35 (P) 12 2000 4.8 19 0.25 – – 99 67–99 ~ 11–14 T: 35 °C Lay and Cheng
Different recirculation ratios (1998)
tested (6:1, 5:1, 4:1
and 3:1)
UASB 2.0 (B) 7 105–1260 0.25–3 6 0.5 – – 88 86 ~ 1.5–2.5 T: 37 °C Tay et al. (2001)
UASB 0.5 (B) 1–3 500 2.5 7.5 3 – 63 (27–55)h 100 (84–100) 85 (73–86) 0.03 (0.03)i Co-substrate: whey Tawfiki Hajji
(0.5 g L−1), p-cresol
et al. (2000)
(150 mg L−1), o-cresol
(150 mg L−1)
T: 29 °C
Different strategies of
bioaugmentation by
Table 3 (continued)
d−1) d−1)
adsorption or encapsulation
within calcium alginate
beads tested
Data in parentheses are
related to the encapsulation
method
batch tests
UASB 2.8 (B) 2 420–1250 1–3 3–6 0.3–0.5 – – 20–98 0–2.1 T: 37 °C Fang et al. (1996)
UASB 2.8 (B) 2+11 1290 3.1 6 0.5 – – 99 98 3 T: 37 °C Fang et al. (1996)
UASB 2.8 (B) 3 300–1470 0.7–3.5 0.4–9 (18) 0.3–1.7 (0.2) 72–177 38–93 70–100 (33) – ~ 0.1–0.2d T: 26 °C Fang et al. (2004)
to the lowest HRT (0.2
days) which caused a
performance failure
batch tests
Biogas production rate from
SMA tests
UASB 2.8 (B) – 630 1.5 0.6–1.3 1.2–2.5 ~ 10–35 ~ 5–18 59–99 – 0.04–0.1d T: 55 °C Fang et al.
(2006)
batch tests
Biogas production rate from
SMA tests
UASB 10 (P) 3.6 420 1 2.4–4.2 0.25–0.4 – 67–235 90 30–99 0.1–1.9 T: 30 °C Hussain et al.
Study of the effect of
(2010)
phosphorus limitation by
testing different COD:P
ratios (300:1, 300:0.75,
300:0.5, 300:0.25, 300:0)
UASB 2.5 (B) ~2 105–835 (1045) 0.25–2 (2.5) 0.5–4 (5) 0.5 – – 90 (60) – ~ 0.25–1.5 (1.2) T: 35 °C Na et al.
(2016)
to the highest OLR for which
a performance failure of the
system was detected
UASB 2.5 (B) ~2 835 2 4–8 0.5–0.25 – – 79 – ~ 1.2–2.2 T: 35 °C Na et al. (2016)
Testing of different HRTs: best
efficiencies for longest
HRT (0.5 d)
UASB 4.5 (B) 5(+1.5) 625 2.8 2.9 0.98 – – 90–96 73–84 ~ 0.1–0.5 WW containing a mixture of phenol:o- Liang et al.
cresol:m-cresol:p-cresol 5:1:1:1
(2020)
T: 37 °C
2215
Table 3 (continued)
2216
d−1) d−1)
Calcium sulphate (CaSO4),

CaSO4/guar gum, and
CaSO4/cationic
polyacrylamide used to
enhance granulation
UASB 1 (B) 4 500 2.9 1.5 1 – 31–41 20–30 20–30 – Real coal gasification WW Wang et al.
T: 35 °C
(2011)
Phenol removal rate from batch tests
UASB 1 (B) 4 500 2.9 1.25–2.5 1–2 – 31–81 5–55 13–54 0.1–0.2 Real coal gasification WW Wang et al. (2011)
T: 55 °C
batch tests
Different HRTs and recycling
ratios tested
a
(gTOC L−1 )
b
(gTOC L−1 d−1 )
c
TOC RE
d
Data estimated by assuming an average methane content of 70% in the biogas
e
Data estimated by assuming an average biomass concentration of 3.5 gVSS L−1 of the tested concentrations
f
Only phenol OLR
g
Data estimated by assuming an average biomass concentration calculated from the biomass in the sludge-bed zone normalised to the bioreactor volume
h
(mgPh gprotein−1 d−1 )
i
(L gprotein−1 d−1 )
Scale application: B: bench scale (< 10 L), P: pilot scale (> 10 L). Abbreviations: AF anaerobic filter, AFBR anaerobic fluidised bed reactor, AFxBR anaerobic fixed bed reactor, AHR anaerobic hybrid
reactor, AIFBR anaerobic immobilised fluidised bed reactor, AnBAC anaerobic biological activated carbon reactor, AnMBR anaerobic membrane bioreactor, CSTR continuously stirred tank reactor, COD
chemical oxygen demand, EGSB expanded granular sludge bed, FxFUAB fixed film up-flow anaerobic reactor, HAIBR horizontal-flow anaerobic immobilised biomass reactor, HRT hydraulic retention
time, OLR organic loading rate, PE polyethylene, Ph phenol, PVDF polyvinylidene fluoride, RE removal efficiency, SA sodium acetate, SBR sequencing batch reactor, T temperature, TOC total organic
carbon, UASB up-flow anaerobic sludge blanket, WW wastewater, VFA volatile fatty acid, VSS volatile suspended solid
performance. Mesophilic and thermophilic regimes have been Another promising technology, constantly under investiga-
investigated on coal gasification real wastewater, with tion, is the AnMBR bioreactor characterised by the well-known
contrasting results. Wang et al. (2011) observed far exceeding features of high-quality effluents, good removal efficiencies, and
performance in terms of REs, specific removal rates, and complete retention of biomass, regardless of the settling and/or
biogas production in a thermophilic UASB in comparison granulation properties (Dereli et al. 2012). Moreover, the possi-
with a mesophilic control bioreactor while Ramakrishnan bility of treating wastewater under extreme conditions (of salin-
and Surampalli (2013) detected only a slight improvement in ity, pH, temperature, or other toxic agents) is an added value of
treatment efficiency (1–6%) and biogas yields (6–19%) in this technology. Of particular relevance are recent studies on the
thermophilic conditions. On the contrary, Fang and co- application of AnMBR to treat hypersaline (8–18 gNa+ L−1) phe-
authors observed better performance of phenol degradation at nolic wastewater at increasing salinity concentration (Muñoz
37 °C (Fang et al. 1996) than at 55 °C (Fang et al. 2006) and Sierra et al. 2018) and under thermophilic conditions (Muñoz
Levén et al. (2012), in a review paper on anaerobic digestion of Sierra et al. 2020). The comparison of the performance between
organic solid waste, reported similar findings. This may be AnMBR and UASB, in treating saline wastewater, showed a
explained with the low microbial diversity, particularly of the better methanogenic activity and a greater stability in AnMBRs
phenol-degrading bacteria, and/or the presence of temperature- at increased salinity influent content (Muñoz Sierra et al. 2019).
sensitive enzymes at thermophilic temperature. All these results Membrane fouling is the main drawback of AnMBR
did not clearly point out a performance gain compensating the representing the ongoing challenge of the present research activ-
energy demand surplus required for thermophilic treatment, ity. Many efforts and investments are devoted to solve the fouling
unless effluents to be treated are already at high temperature operational problems with the dual purpose of performance im-
suitable for that condition, such as in the case of coal gasifica- provement and operational cost abatement.
tion wastewater (Wang et al. 2011). Moreover, the use of chem-
ical agents (CaSO4, CaSO4/guar gum, and CaSO4/cationic
polyacrylamide) to enhance anaerobic sludge granulation and Biaugmentation and biostimulation
accelerate the start-up period was another proposed UASB op-
timisation strategy (Liang et al. 2020). The bioaugmentation by Bioaugmentation and biostimulation are considered the main
adsorption or by encapsulation within calcium alginate beads is approaches to achieve an effective bioremediation.
another strategy to improve the start-up and the process perfor- Biostimulation involves the addition of nutrients and other com-
mance, as reported by Tawfiki Hajji et al. (2000) with excellent pounds or the modification of an environmental parameter to
phenol removal efficiencies. Further details on this strategy will stimulate the native microbial community growth or bioremedi-
be discussed in the following section. Finally, the effects of ation activity (Tyagi et al. 2011). Bioaugmentation, on the other
wastewater composition, generally including several co- hand, is a technique aiming at the enhancement of a purposeful
substrates at different phenol/co-substrate ratios (Tay et al. process through the addition of one or multiple targeted micro-
2001; Zhou and Fang 1997; Gali et al. 2006), presence of nitrate organisms, indigenous, non-indigenous, or genetically
(Fang and Zhou 1999), occurrence of saline conditions (Wang engineered, to the original community. These microorganisms
et al. 2017; Muñoz Sierra et al. 2018), and nutrient limitation should be further able to withstand the environmental conditions
(Hussain et al. 2010) have been also investigated. they will be subjected to and the microbial pressure (Herrero and
Anaerobic EGSB bioreactors operated with granular bio- Stuckey 2015; Raper et al. 2018). An inability to create and
mass have been applied to phenol removal with very good maintain a stable community is the main reason of failure of
results reaching removal rates of 1653–4593 mgPh L−1 d−1 bioaugmentation processes within wastewater treatment plants
with biomass concentrations in the range of 11.4–29.3 gVSS (Kurzbaum et al. 2017). Numerous causes of bioagmentation
L−1. Their good performance is attributable to the expanded failure have been identified; however, it is still considered essen-
granular sludge bed that allows an effective mixing and mass tial and a cheaper and more sustainable alternative to physio-
transfer of the organic compounds within sludge granules (Li chemical approaches (Tyagi et al. 2011; Nzila et al. 2016). A
et al. 2014) and the high dilution of the wastewater in the biostimulation method is the hydrogen enrichment to enhance
bioreactor (Chou et al. 2008). Collins et al. (2005) and the hydrogenotrophic methanogenic activity of the original com-
Scully et al. (2006) demonstrated the feasibility of a hybrid munity. The use of this tool within an UASB reactor treating
EGSB-AF, realised with the addition to an EGSB of an upper phenolic wastewater produced an increase in the phenol
fixed-film section (anaerobic filter, AF) randomly packed with utilisation rate and a shift in the bacterial community. The com-
polyethylene rings, for phenol removal at psychrophilic con- monly found Proteobacteria, Chloroflexi, and Firmicutes phyla
ditions (10–18 °C). Removal efficiencies similar to the ones showed an increase of Firmicutes at the expense of
observed in mesophilic conditions, and good biogas produc- Proteobacteria with also an increase in the genera Syntrophus
tions make this technology competitive even at low tempera- (Wu et al. 2019). Furthermore, hydrogen addition could also be
ture with significant energetic and economic savings. used as a method for rapid recovery of anaerobic digesters in
response to toxic events especially when the consortium shows a useful information on the general applicability of the anaero-
poor adaptability (Schauer-Gimenez et al. 2010). bic treatment to industrial wastewater.
Within the phenol degradation world, studies on bioaug- Data collected within this review show that currently, an-
mentation of anaerobic phenol degrading communities are aerobic treatment is not competitive in terms of kinetics
still scarce and mainly restricted to lab-scale experiments. against aerobic treatments; however, several strategies can
Bioaugmentation has however proven itself effective in terms be further investigated to attenuate/fill the gap.
of enhancing flocculation. Stimulating aggregation by com- From the microbiological side, the temperature effect is still
bining two or more bacterial strains with complementary ca- a current research topic because of the strong impact of this
pability (e.g. mixing a phenol-degrading strain with a strain parameter on microbial diversity, enzyme activity, degrada-
with high aggregation ability) lead to cooperation for phenol tion pathway, and then on the process performance. Actions to
degradation and increased removal rates due to a reduced improve bacterial performance, such as bioaugmentation and
exposure to phenol toxicity and washout (Prpich and biostimulation, have been demonstrated to be effective and
Daugulis 2005; Jiang et al. 2006). deserve deeper investigations. Similarly, the improvement of
A methanogenic consortium degrading phenol within simpler strategies as enhanced acclimatisation and start-up
UASBs, bioaugmented with + 2%, + 5%, and + 10% of the procedures can be effective in increasing the feasibility of
indigenous and acclimatised consortium, showed further suc- the anaerobic process. Another important strategy to increase
cessful results. The augmented UASBs showed shorter start- the process kinetics is the “concentration of the biomass” in
up periods and increased rates of phenol degradation (100% the system, which can be achieved by operating with attached
removal in less than 90 days) when confronted with the con- or granular biomass.
trol (100% removal in 171 days). Further increase was ob- From the technological side, high-rate anaerobic bioreac-
served by introducing the additional consortium encapsulated tors, successfully applied for diluted streams (such as domes-
within alginate beads as this prevented washout (Guiot et al. tic wastewater), can be extended to phenolic wastewater treat-
2000; Tawfiki Hajji et al. 2000). However, encapsulation ment as demonstrated by previous studies on UASB and
within alginate or beads of other materials enables lower dif- EGSB reactors operated with granular biomass and on
fusion rates of nutrient and is sensitive to mechanical degra- AnMBR bioreactors. Another interesting topic for further
dation and chemical dissolution (Kurzbaum et al. 2017; investigation is the possibility of profitably exploiting the
Youssef et al. 2019). A small bioreactor platform with a presence in the wastewater of oxidizing agents as nitrates,
microfiltration structural membrane was therefore developed sulphates, and chlorates, which can consistently increase the
for a more efficient bioaugmentation and at the same time to removal rates at values comparable with the aerobic ones.
provide a protected environment for the introduced microor- In conclusion, the anaerobic process applied to wastewater
ganisms (Kurzbaum et al. 2017; Menashe et al. 2020). treatment is a step forward to a more sustainable approach in
In terms of bioaugmentation with non-indigenous microor- wastewater treatment, especially for industrial wastewater
ganisms, two strains of phenol degraders (i.e. Pseudomonas whose toxic load is critical in terms of impact on environmen-
PCT01 and PTS02) led to an enhanced phenol degradation tal quality and human health and safety. Even if there are still
when added to a membrane bioreactor treating coking waste- operational strategies to be improved and optimised, research
water (Zhu et al. 2015). The path of bioaugmentation with efforts should be devoted to this challenging objective consid-
non-indigenous strains, or engineered microorganisms, how- ering that the potential advantages of energy and resource
ever, requires further study and it is often overlooked as it is recovery are of primary relevance in achieving sustainable
more likely to develop acclimation problematics and needs an development goals.
in-depth characterisation of the environmental parameters.
Further unexplored techniques that could lead to improve-
ments in the field of anaerobic biodegradation of phenolic Author contribution MCT and DMA conceived and designed the struc-
ture of the article. MCT, DMA, EC, and LB performed the literature
wastewater include the study and control of quorum sensing,
search and the data analysis. MCT, DMA, and EC wrote the first draft
the use of plasmid-mediated bioaugmentation, and nanotech- of the manuscript. MCT and LB reviewed the manuscript. All authors
nologies (Nzila et al. 2016). read and approved the final version of the manuscript.
Declarations
Conclusions and summary of research needs Ethics approval and consent to participate This article does not contain
any studies with human participants or animals performed by any of the
Phenol is the typical target compound considered representa- authors.
tive of industrial contaminants, so the state of knowledge of
the potentialities of phenol anaerobic biodegradation can give Conflict of interest The authors declare no competing interests.
References Butler JE, He Q, Nevin KP, He Z, Zhou J, Lovley DR (2007) Genomic

and microarray analysis of aromatics degradation in Geobacter
metallireducens and comparison to a Geobacter isolate from a con-
Al-Khalid T, El-Naas MH (2012) Aerobic Biodegradation of Phenols: A
taminated field site. BMC Genomics 8:180. https://doi.org/10.1186/
Comprehensive Review. Crit Rev Environ Sci Technol 42(16):
1471-2164-8-180
1631–1690. https://doi.org/10.1080/10643389.2011.569872
Cabrol L, Malhautier L (2011) Integrating microbial ecology in
Almendariz FJ, Meraz M, Olmos AD, Monroy O (2005) Phenolic refin-
bioprocess understanding: the case of gas biofiltration. Appl
ery wastewater biodegradation by an expanded granular sludge bed
Microbiol Biotechnol 90(3):837–849. https://doi.org/10.1007/
reactor. Water Sci Technol 52(1-2):391–396. https://doi.org/10.
s00253-011-3191-9
2166/wst.2005.0544
Carbajo JB, Boltes K, Leton P (2010) Treatment of phenol in an anaer-
Bajaj M, Gallert C, Winter J (2009) Treatment of phenolic wastewater in
obic fluidized bed reactor (AFBR): continuous and batch regime.
an anaerobic fixed bed reactor (AFBR)-Recovery after shock load-
Biodegradation 21:603–613. https://doi.org/10.1007/s10532-010-
ing. J Hazard Mater 162:1330–1339. https://doi.org/10.1016/j.
9328-1
jhazmat.2008.06.027
Carmona M, Zamarro MT, Blázquez B, Durante-Rodríguez G, Juárez JF,
Bak F, Widdel F (1986) Anaerobic degradation of phenol and phenol Valderrama JA, Barragán MJL, García JL, Díaz E (2009) Anaerobic
derivatives by Desulfobacterium phenolicum sp. nov. Arch catabolism of aromatic compounds: a genetic and genomic view.
Microbiol 146:177–180. https://doi.org/10.1007/BF00402347 Microbiol Mol Biol Rev 73:71–133. https://doi.org/10.1128/
Bakhshi Z, Najafpour G, Kariminezhad E, Pishgar R, Mousavi N, MMBR.00021-08
Taghizade T (2011) Growth kinetic models for phenol biodegrada- Chapleur O, Madigou C, Civade R, Rodolphe Y, Mazeas L, Bouchez T
tion in a batch culture of Pseudomonas putida. Environ Technol (2016) Increasing concentrations of phenol progressively affect an-
32(16):1835–1841. https://doi.org/10.1080/09593330.2011.562925 aerobic digestion of cellulose and associated microbial communi-
Bakker G (1977) Anaerobic degradation of aromatic-compounds in pres- ties. Biodegradation 27(1):15–27. https://doi.org/10.1007/s10532-
ence of nitrate. FEMS Lett 1:103–108. https://doi.org/10.1111/j. 015-9751-4
1574-6968.1977.tb00591.x Chen C-L, Wu J-H, Liu W-T (2008) Identification of important microbial
Banerjee A, Ghoshal AK (2010) Isolation and characterization of hyper populations in the mesophilic and thermophilic phenol-degrading
phenol tolerant Bacillus sp. from oil refinery and exploration sites. J methanogenic consortia. Water Res 42:1963–1976. https://doi.org/
Hazard Mater 176:85–91. https://doi.org/10.1016/j.jhazmat.2009. 10.1016/j.watres.2007.11.037
11.002 Chen C-L, Wu J-H, Tseng I-C, Liang T-M, Liu W-T (2009)
Basak B, Bhunia B, Dutta S, Chakraborty S, Dey A (2014) Kinetics of Characterization of active microbes in a full-scale anaerobic fluid-
phenol biodegradation at high concentration by a metabolically ver- ized bed reactor treating phenolic wastewater. Microbes Environ
satile isolated yeast Candida tropicalis PHB5. Environ Sci Pollut 24(2):144–153. https://doi.org/10.1264/jsme2.ME09109
Res 21:1444–1454. https://doi.org/10.1007/s11356-013-2040-z Chen Y, He J, Wang YQ, Kotsopoulos TA, Kaparaju P, Zeng RJ (2016)
Begun SS, Radha KV (2013) Biodegradation Kinetic Studies on Phenol Development of an anaerobic co-metabolic model for degradation of
in Internal Draft Tube (Inverse Fluidized Bed) Biofilm Reactor phenol, m-cresol and easily degradable substrate. Biochem Eng J
Using Pseudomonas fluorescens: Performance Evaluation of 106:19–25. https://doi.org/10.1016/j.bej.2015.11.003
Biofilm and Biomass Characteristics. Biorem J 17(4):264–277. Chou HH, Huang JS (2005) Comparative granule characteristics and
https://doi.org/10.1080/10889868.2013.827622 biokinetics of sucrose-fed and phenol-fed UASB reactors.
Bolaños RML, Varesche MBA, Zaiat M, Foresti E (2001) Phenol degra- Chemosphere 59:107–116. https://doi.org/10.1016/j.chemosphere.
dation in horizontal-flow anaerobic immobilized biomass (HAIB) 2004.09.097
reactor under mesophilic conditions. Water Sci Technol 44(4):167– Chou H-H, Huang J-S, Jheng J-H, Ohara R (2008) Influencing effect of
174. https://doi.org/10.2166/wst.2001.0212 intra-granule mass transfer in expanded granular sludge-bed reactors
Boll M, Fuchs G (1995) Benzoyl-coenzyme A reductase (dearomatizing), treating an inhibitory substrate. Bioresour Technol 99:3403–3410.
a key enzyme of anaerobic aromatic metabolism. ATP dependence https://doi.org/10.1016/j.biortech.2007.08.011
of the reaction, purification and some properties of the enzyme from Christen P, Vega A, Casalot L, Simon G, Auria R (2012) Kinetics of
Thauera aromatica strain K172. Eur J Biochem 234:921–933. aerobic phenol biodegradation by the acidophilic and hyperthermo-
https://doi.org/10.1111/j.1432-1033.1995.921_a.x philic archaeon Sulfolobus solfataricus 98/2. Biochem Eng J 62:56–
Boll M, Laempe D, Eisenreich W, Bacher A, Mittel-Berger T, Heinze J, 61. https://doi.org/10.1016/j.bej.2011.12.012
Fuchs G (2000) Nonaromatic products from anoxic conversion of Collins G, Fou C, McHugh S, Mahony T, O’Flaherty V (2005) Anaerobic
benzoyl-CoA with benzoyl-CoA reductase and cyclohexa-1,5-di- biological treatment of phenolic wastewater at 15–18 °C. Water Res
ene-1- carbonyl-CoA hydratase. J Biol Chem 275:21889–21895. 39:1614–1620. https://doi.org/10.1016/j.watres.2005.01.017
https://doi.org/10.1074/jbc.M001833200 Das B, Selvaraj G, Patra S (2019) An environmentally sustainable pro-
Boll M, Löffler C, Morris BE, Kung JW (2014) Anaerobic degradation of cess for remediation of phenol polluted wastewater and simulta-
homocyclic aromatic compounds via arylcarboxyl-coenzyme A es- neous clean energy generation as by-product. Int J Environ Sci
ters: organisms, strategies and key enzymes. Environ Microbiol Technol 16:147–170. https://doi.org/10.1007/s13762-017-1599-1
16(3):612–627. https://doi.org/10.1111/1462-2920.12328 Dereli RK, Ersahin ME, Ozgun H, Ozturk I, Jeison D, van der Zee F, van
Breese K, Fuchs G (1998) 4-Hydroxybenzoyl-CoA reductase Lier JB (2012) Potentials of anaerobic membrane bioreactors to
(dehydroxylating) from the denitrifying bacterium Thauera overcome treatment limitations induced by industrial wastewaters.
aromatica - Prosthetic groups, electron donor, and genes of a mem- Bioresour Technol 122:160–170. https://doi.org/10.1016/j.biortech.
ber of the molybdenum-flavin-iron-sulfur proteins. Eur J Biochem 2012.05.139
251(3):916–923. https://doi.org/10.1046/j.1432-1327.1998. Dey S, Mukherjee S (2010) Performance and kinetic evaluation of phenol
2510916.x biodegradation by mixed microbial culture in a bioreactor. Int J Wat
Breinig S, Schiltz E, Fuchs G (2000) Genes involved in anaerobic me- Resour Environ Eng 2(3):40–49. https://doi.org/10.5897/IJWREE.
tabolism of phenol in the bacterium Thauera aromatica. J Bacteriol 9000043
182(20):5849–5863. https://doi.org/10.1128/jb.182.20.5849-5863. Dey S, Mukherjee S (2013) Biodegradation Kinetics of Bi-substrate
2000 Solution of Phenol and Resorcinol in an Aerobic Batch Reactor.
KSCE J Civ Eng 17(7):1587–1595. https://doi.org/10.1007/s12205- Environ Eng 132(11):1539–1542. https://doi.org/10.1061/(ASCE)

013-0196-1 0733-9372(2006)132:11(1539)
Duan Z (2011) Microbial Degradation of Phenol by Activated Sludge in a Ghosh SK, Doctor PB (1992) Toxicity screening of phenol using
Batch Reactor. Environ Prot Eng 37:53 Microtox®. Environ Toxicol Water Qual 7(2):157–163. https://
Duraisamy P, Sekar J, Arunkumar AD, Ramalingam PV (2020) Kinetics doi.org/10.1002/tox.2530070206
of Phenol Biodegradation by Heavy Metal Tolerant Rhizobacteria Gibson J, Harwood CS (2002) Metabolic diversity in aromatic compound
Glutamicibacter nicotianae MSSRFPD35 From Distillery Effluent utilization by anaerobic microbes. Annu Rev Microbiol 56:345–
Contaminated Soils. Front Microbiol 11:1573. https://doi.org/10. 369. https://doi.org/10.1146/annurev.micro.56.012302.160749
3389/fmicb.2020.01573 Gibson J, Dispensa M, Harwood CS (1997) 4-Hydroxybenzoyl
Dwyer DF, Krumme ML, Boyd SA, Tiedje JM (1986) Kinetics of phenol Coenzyme A Reductase (Dehydroxylating) Is Required for
biodegradation by an immobilized methanogenic consortium. Appl Anaerobic Degradation of 4-Hydroxybenzoate by
Environ Microbiol 52:345-351. https://aem.asm.org/content/aem/ Rhodopseudomonas palustris and Shares Features with
52/2/345.full.pdf. (Accessed Nov 2020) Molybdenum-Containing Hydroxylases. J Bacteriol 197(3):634–
Egland PG, Pelletier DA, Dispensa M, Gibson J, Harwood CS (1997) A 642. https://doi.org/10.1128/jb.179.3.634-642.1997
cluster of bacterial genes for anaerobic benzene ring biodegradation. Glöckler R, Tschech A, Fuchs G (1989) Reductive dehydroxylation of 4-
Proc Natl Acad Sci USA 94:6484–6489. https://doi.org/10.1073/ hydroxybenzoyl-CoA to benzoyl-CoA in a denitrifying, phenol
pnas.94.12.6484 degrading Pseudomonas species. FEBS Lett 251:237–240. https://
Ekama GA, Wentzel MC (2004) Modelling inorganic material in activat- doi.org/10.1016/0014-5793(89)81461-9
ed sludge systems. Water SA 30(2):153–174. https://doi.org/10. Goeddertz JG, Weber AS, Ying WC (1990) Startup and operation of an
4314/wsa.v30i2.5060 anaerobic biological activated carbon (AnBAC) process for treat-
Essam T, Amin MA, El Tayeb O, Mattiasson B, Guieysse B (2010) ment of a high strength multicomponent inhibitory wastewater.
Kinetics and metabolic versatility of highly tolerant phenol Environ Prog 9(2):110–117. https://doi.org/10.1002/ep.670090219
degrading Alcaligenes strain TW1. J Hazard Mater 173:783–788. Guiot SR, Tawfiki-Hajj K, Lépine F (2000) Immobilization strategies for
https://doi.org/10.1016/j.jhazmat.2009.09.006 bioaugmentation of anaerobic reactors treating phenolic com-
EU (2013) Directive 2013/39/EU of the European Parliament and of the pounds. Water Sci Technol 42(5-6):245–250. https://doi.org/10.
Council of 12 August 2013 amending Directives 2000/60/EC and 2166/wst.2000.0520
2008/105/EC as regards priority substances in the field of water Haldane JBS (1965) Enzymes. MIT Press, Cambridge
policy. https://eur-lex.europa.eu/legal-content/EN/ALL/?uri= Hamitouche A-E, Bendjama Z, Amrane A, Kaouah F, Hamane D (2012)
CELEX:32013L0039 (Accessed Nov 2020) Relevance of the Luong model to describe the biodegradation of
phenol by mixed culture in a batch reactor. Ann Microbiol 62(2):
Fang HHP, Zhou GM (1999) Interactions of methanogens and denitrifiers
581–586. https://doi.org/10.1007/s13213-011-0294-6
in degradation of phenols. J Environ Eng ASCE 125:57–63. https://
He Z, Wiegel J (1995) Purification and Characterization of an Oxygen-
doi.org/10.1061/(ASCE)0733-9372(1999)125:1(57)
Sensitive Reversible 4-Hydroxy-benzoate Decarboxylase from
Fang HHP, Chen T, Li YY, Chui HK (1996) Degradation of phenol in
Clostridium hydroxybenzoicum. Eur J Biochem 229:77–82. https://
wastewater in an upflow anaerobic sludge blanket reactor. Water
doi.org/10.1111/j.1432-1033.1995.0077l.x
Res 30(6):1353–1360. https://doi.org/10.1016/0043-1354(95)
Heilbuth NM, Linardi VR, Monteiro AS, da Rocha RA, Mimim LA,
00309-6
Santos VL (2015) Estimation of kinetic parameters of phenol deg-
Fang HHP, Liu Y, Ke SZ, Zhang T (2004) Anaerobic degradation of radation by bacteria isolated from activated sludge using a genetic
phenol in wastewater at ambient temperature. Water Sci Technol algorithm. J Chem Technol Biotechnol 90:2066–2075. https://doi.
49(1):95–102. https://doi.org/10.2166/wst.2004.0028 org/10.1002/jctb.4518
Fang HHP, Liang DW, Zhang T, Liu Y (2006) Anaerobic treatment of Hernandez JE, Edyvean RGJ (2008) Inhibition of biogas production and
phenol in wastewater under thermophilic condition. Water Res 40: biodegradability by substituted phenolic compounds in anaerobic
427–434. https://doi.org/10.1016/j.watres.2005.11.025 sludge. J Hazard Mater 160:20–28. https://doi.org/10.1016/j.
Feitkenhauer H, Schnicke S, Müller R, Märkl H (2001) Determination of jhazmat.2008.02.075
the kinetic parameters of the phenol-degrading thermophile Bacillus Herrero M, Stuckey DC (2015) Bioaugmentation and its application in
themoleovorans sp. A2. Appl Microbiol Biotechnol 57:744–750. wastewater treatment: A review. Chemosphere 140:119–128.
https://doi.org/10.1007/s002530100823 https://doi.org/10.1016/j.chemosphere.2014.10.033
Firozjaee TT, Najafpour GD, Asgari A, Bakhshi Z, Pishgar R, Mousavi N Ho K-L, Chen Y-Y, Lin B, Lee D-J (2010) Degrading high-strength
(2011) Phenol biodegradation kinetics in an anaerobic batch reactor, phenol using aerobic granular sludge. Appl Microbiol Biotechnol
world environmental and water resources congress 2011: bearing 85:2009–2015. https://doi.org/10.1007/s00253-009-2321-0
knowledge for sustainability, 2011, pp. 4313–4321 Holmes DE, Risso C, Smith JA, Lovley DR (2012) Genome-scale anal-
Firozjaee TT, Najafpour GD, Asgari A, Khavarpour M (2013) Biological ysis of anaerobic benzoate and phenol metabolism in the hyperther-
treatment of phenolic wastewater in an anaerobic continuous stirred mophilic archaeon Ferroglobus placidus. ISME J 6:146–157.
tank reactor. Chem Ind Chem Eng Q 19(2):173–179. https://doi.org/ https://doi.org/10.1038/ismej.2011.88
10.2298/CICEQ120216052F Hosoda A, Kasai Y, Hamamura N, Takahata Y, Watanabe K (2005)
Franchi O, Rosenkranz F, Chamy R (2018) Key microbial populations Development of a PCR method for the detection and quantification
involved in anaerobic degradation of phenol and p-cresol using dif- of benzoyl-CoA reductase genes and its application to monitored
ferent inocula. Electron J Biotechnol 3:33–38. https://doi.org/10. natural attenuation. Biodegrad 16:591–601. https://doi.org/10.
1016/j.ejbt.2018.08.002 1007/s10532-005-0826-5
Franchi O, Cabrol L, Chamy R, Rosenkranz F (2020) Correlations be- Hoyos-Hernandez C, Hoffmann M, Guenne A, Mazeas L (2014)
tween microbial population dynamics, bamA gene abundance and Elucidation of the thermophilic phenol biodegradation pathway via
performance of anaerobic sequencing batch reactor (ASBR) treating benzoate during the anaerobic digestion of municipal solid waste.
increasing concentrations of phenol. J Biotechnol 310:40–48. Chemosphere 97:115–119. https://doi.org/10.1016/j.chemosphere.
https://doi.org/10.1016/j.jbiotec.2020.01.010 2013.10.045
Gali VS, Kumar P, Mehrotra I (2006) Biodegradation of phenol with Huang J, He Z, Wiegel J (1999) Cloning, characterization, and expression
wastewater as a cosubstrate in upflow anaerobic sludge blanket. J of a novel gene encoding a reversible 4-hydroxybenzoate
decarboxylase from Clostridium hydroxybenzoicum. J Bacteriol compound-degrading anaerobes. Appl Environ Microbiol 77(14):
181:5119–5122. https://doi.org/10.1128/JB.181.16.5119-5122. 5056–5061. https://doi.org/10.1128/AEM.00335-11
1999 Kurzbaum E, Raizner Y, Cohen O, Suckeveriene RY, Kulikov A, Hakimi
Hussain A, Kumar P, Mehrootra I (2010) Anaerobic treatment of pheno- B, Kruh LI, Armon R, Farber Y, Menashe O (2017) Encapsulated
lic wastewater: Effect of phosphorous limitation. Desalin Water Pseudomonas putida for phenol biodegradation : use of a structural
Treat 20:189–196. https://doi.org/10.5004/dwt.2010.1151 membrane for construction of a well-organized confined particle.
Hussain A, Dubey SK, Kumar V (2015) Kinetic study for aerobic treat- Water Res 121:37–45. https://doi.org/10.1016/j.watres.2017.04.079
ment of phenolic wastewater. Water Resour Ind 11:81–90. https:// Laempe D, Eisenreich W, Bacher A, Fuchs G (1998) Cyclohexa-1,5-
doi.org/10.1016/j.wri.2015.05.002 diene-1-carbonyl-CoA hydratase [corrected], an enzyme involved
Jahn L, Saracevic E, Svardal K, Krampe J (2019) Anaerobic biodegrada- in anaerobic metabolism of benzoyl-CoA in the denitrifying bacte-
tion and dewaterability of aerobic granular sludge. J Chem Technol rium Thauera aromatica. Eur J Biochem 255:618–627. https://doi.
Biotechnol 94(9):2908–2916. https://doi.org/10.1002/jctb.6094 org/10.1046/j.1432-1327.1998.2550618.x
Jiang H-L, Tay J-H, Maszenan AM, Tay ST-L (2006) Enhanced Phenol Laempe D, Jahn M, Fuchs G (1999) 6-Hydroxycyclohex-1-ene-1-car-
Biodegradation and Aerobic Granulation by Two Coaggregating bonyl-CoA dehydrogenase and 6-oxocyclohex-1-ene-1-carbonyl-
Bacterial Strains. Environ Sci Technol 40:6137–6142. https://doi. CoA hydrolase, enzymes of the benzoyl-CoA pathway of anaerobic
org/10.1021/es0609295 aromatic metabolism in the denitrifying bacterium Thauera
Jiang Y, Yang K, Deng T, Ji B, Shang Y, Wang H (2018) Immobilization aromatica. Eur J Biochem 263:420–429. https://doi.org/10.1046/j.
of halophilic yeast for effective removal of phenol in hypersaline 1432-1327.1999.00504.x
conditions. Water Sci Technol 77:706–713. https://doi.org/10.2166/ Lay J-J, Cheng S-S (1998) Influence of hydraulic loading rate on UASB
wst.2017.576 reactor treating phenolic wastewater. J Environ Eng 124(9):829–
Jin X, Li E, Lu S, Qiu Z, Sui Q (2013) Coking wastewater treatment for 837. https://doi.org/10.1061/(ASCE)0733-9372(1998)124:9(829)
industrial reuse purpose: Combining biological processes with ultra- Levén L, Schnürer A (2005) Effects of temperature on biological degra-
filtration, nanofiltration and reverse osmosis. J Environ Sci 25(8): dation of phenols, benzoates and phthalates under methanogenic
1565–1574. https://doi.org/10.1016/S1001-0742(12)60212-5 conditions. Int Biodeterior Biodegrad 55:153–160. https://doi.org/
10.1016/j.ibiod.2004.09.004
Joshi DR, Zhang Y, Tian Z, Gao Y, Yang M (2016) Performance and
Levén L, Nyberg K, Korkea-aho L, Schnürer A (2006) Phenols in anaer-
microbial community composition in a long-term sequential
obic digestion processes and inhibition of ammonia oxidising bac-
anaerobic-aerobic bioreactor operation treating coking wastewater.
teria (AOB) in soil. Sci Total Environ 364(1-3):229–238. https://doi.
Appl Microbiol Biotechnol 100:8191–8202. https://doi.org/10.
org/10.1016/j.scitotenv.2005.06.003
1007/s00253-016-7591-8
Levén L, Nyberg K, Schnürer A (2012) Conversion of phenols during
Ju F, Wang Y, Zhang T (2018) Bioreactor microbial ecosystems with
anaerobic digestion of organic solid waste - A review of important
differentiated methanogenic phenol biodegradation and competitive
microorganisms and impact of temperature. J Environ Manag 95:
metabolic pathways unraveled with genome-resolved
S99–S103. https://doi.org/10.1016/j.jenvman.2010.10.021
metagenomics. Biotechnol Biofuels 11:135. https://doi.org/10.
Li Y, Li J, Wang C, Wang P (2010) Growth kinetics and phenol biodeg-
1186/s13068-018-1136-6
radation of psychrotrophic Pseudomonas putida LY1. Bioresour
Kamali M, Gameiro T, Costa ME, Capela I, Aminabhavi TM (2019)
Technol 101:6740–6744. https://doi.org/10.1016/j.biortech.2010.
Enhanced biodegradation of phenolic wastewaters with acclima-
03.083
tized activated sludge - a kinetic study. Chem Eng J 378:122186.
Li C, Tabassum S, Zhang Z (2014) An advanced anaerobic expanded
https://doi.org/10.1016/j.cej.2019.122186
granular sludge bed (AnaEG) for the treatment of coal gasification
Karlsson A, Ejlertsson J, Nezirevic D, Svensson BH (1999) Degradation wastewater. RSC Adv 4:57580. https://doi.org/10.1039/c4ra08042d
of phenol under meso- and thermophilic, anaerobic conditions. Li Y, Tabassum S, Yu Z, Wu X, Zhang X, Song Y, Chu C, Zhang Z
Anaerobe 5:25–35. https://doi.org/10.1006/anae.1998.0187 (2016) Effect of effluent recirculation rate on the performance of
Khan N, Khan MD, Sabir S, Nizami A-S, Anwer AH, Rehan M, Khan anaerobic bio-filter treating coal gasification wastewater under co-
MZ (2020) Deciphering the effects of temperature on bio-methane digestion conditions. RSC Adv 6:87926–87934. https://doi.org/10.
generation through anaerobic digestion. Environ Sci Pollut Res 27: 1039/c6ra18363h
29766–29777. https://doi.org/10.1007/s11356-019-07245-w Li H, Meng F, Duan W, Lin Y, Zheng Y (2019) Biodegradation of phenol
Khouri N, Dott W, Kampfer P (1992) Anaerobic degradation of phenol in in saline or hypersaline environments by bacteria: A review. Ecotox
batch and continuous cultures by a denitrifying bacterial consortium. Environ Safe 184:109658. https://doi.org/10.1016/j.ecoenv.2019.
Appl Microbiol Biotechnol 37:524–528. https://doi.org/10.1007/ 109658
BF00180981 Li C-M, Wu H-Z, Wang Y-X, Zhu S, Wei C-H (2020) Enhancement of
Kobayashi T, Hashinaga T, Mikami E, Suzuki T (1989) Methanogenic phenol biodegradation: Metabolic division of labor in coculture of
degradation of phenol and benzoate in acclimated sludge. Water Sci Stenotrophomonas sp. N5 and Advenella sp. B9. J Hazard Mater
Technol 21:55–65. https://doi.org/10.2166/wst.1989.0210 400:123214. https://doi.org/10.1016/j.jhazmat.2020.123214
Kung JW, Löffler C, Dörner K, Heintz D, Gallien S, Van Dorsselaer A, Liang J, Wang Q, Yoza BA, Li QX, Chen C, Ming J, Yu J (2020) Rapid
Friedrich T, Boll M (2009) Identification and characterization of the granulation using calcium sulfate and polymers for refractory waste-
tungsten-containing class of benzoyl-coenzyme A reductases. Proc water treatment in up-flow anaerobic sludge blanket reactor.
Natl Acad Sci USA 106:17687–17692. https://doi.org/10.1073/ Bioresour Technol 305:123084. https://doi.org/10.1016/j.biortech.
pnas.0905073106 2020.123084
Kuntze K, Shinoda Y, Moutakki H, McInerney MJ, Vogt C, Richnow Lim J-W, Seng C-E, Lim P-E, Ng S-L, Tan K-C, Kew S-L (2013)
HH, Boll M (2008) 6-Oxocyclohex-1-ene-1-carbonyl-coenzyme A Response of low-strength phenol-acclimated activated sludge to
hydrolases fromobligately anaerobic bacteria: Characterization and shock loading of high phenol concentrations. Water SA 39(5):
identification of its gene as a functional marker for aromatic com- 695–699. https://doi.org/10.4314/wsa.v39i5.14
pounds degrading anaerobes. Environ Microbiol 10(6):1547–1556. Limam I, Mezni M, Guenne A, Madigou C, Driss MR, Bouchez T,
https://doi.org/10.1111/j.1462-2920.2008.01570.x Mazéas L (2013) Evaluation of biodegradability of phenol and
Kuntze K, Vogt C, Richnow HH, Boll M (2011) Combined application of bisphenol A during mesophilic and thermophilic municipal solid
PCR-based functional assays for the detection of aromatic- waste anaerobic digestion using 13C-labeled contaminants.
Chemosphere 90:512–520. https://doi.org/10.1016/j.chemosphere. 3D-cellulose acetate membrane. Polym Adv Technol 32:681–689.
2012.08.019 https://doi.org/10.1002/pat.5121
Lin Y-H, Cheng Y-S (2020) Phenol Degradation Kinetics by Free and Mohanty MP, Brahmacharimayum B, Ghosh PK (2018) Effects of phe-
Immobilized Pseudomonas putida BCRC 14365 in Batch and nol on sulfate reduction by mixed microbial culture: kinetics and
Continuous-Flow Bioreactors. Process 8:721. https://doi.org/10. bio-kinetics analysis. Water Sci Technol 77(4):1079–1088. https://
3390/pr8060721 doi.org/10.2166/wst.2017.630
Lin YH, Lee KK (2001) Verification of anaerobic biofilm model for Mosca Angelucci D, Tomei MC (2015) Pentachlorophenol aerobic re-
phenol degradation with sulphate reduction. J Environ Eng 127: moval in a sequential reactor: start-up procedure and kinetic study.
119–125. https://doi.org/10.1061/(ASCE)0733-9372(2001)127: Environ Technol 36:327–335. https://doi.org/10.1080/09593330.
2(119) 2014.946099
Lin Y-H, Wu C-L, Hsu C-H, Li H-L (2009) Biodegradation of phenol Mosca Angelucci D, Clagnan E, Brusetti L, Tomei MC (2020) Anaerobic
with chromium (VI) reduction in an anaerobic fixed-biofilm phenol biodegradation: kinetic study and microbial community
process—Kinetic model and reactor performance. J Hazard Mater shifts under high-concentration dynamic loading. Appl Microbiol
172:1394–1401. https://doi.org/10.1016/j.jhazmat.2009.08.005 Biotechnol 104:6825–6838. https://doi.org/10.1007/s00253-020-
Liu J, Jia X, Wen J, Zhou Z (2012) Substrate interactions and kinetics 10696-8
study of phenolic compounds biodegradation by Pseudomonas sp. Muñoz Sierra JDM, Oosterkamp MJ, Wang W, Spanjers H, van Lier JB
cbp1-3. Biochem Eng J 67:156–166. https://doi.org/10.1016/j.bej. (2018) Impact of long-term salinity exposure in anaerobic mem-
2012.06.008 brane bioreactors treating phenolic wastewater: performance robust-
Liu JZ, Wang Q, Yan JB, Qin XR, Li LL, Xu W, Subramaniam R, Bajpai ness and endured microbial community. Water Res 141:172–184.
RK (2013) Isolation and characterization of a novel phenol https://doi.org/10.1016/j.watres.2018.05.006
degrading bacterial strain WUST-C1. Ind Eng Chem Res 52:258– Muñoz Sierra JDM, Oosterkamp MJ, Wang W, Spanjers H, van Lier JB
265. https://doi.org/10.1021/ie3012903 (2019) Comparative performance of upflow anaerobic sludge blan-
Löffler C, Kuntze K, Ramos Vazquez J, Rugor A, Kung JW, Böttcher A, ket reactor and anaerobic membrane bioreactor treating phenolic
Boll M (2011) Occurrence, genes and expression of the W/Se-con- wastewater: Overcoming high salinity. Chem Eng J 366:480–490.
taining class II benzoyl-coenzyme A reductases in anaerobic bacte- https://doi.org/10.1016/j.cej.2019.02.097
ria. Environ Microbiol 13:696–709. https://doi.org/10.1111/j.1462- Muñoz Sierra JDM, García Rea VS, Cerqueda-García D, Spanjers H, van
2920.2010.02374.x Lier JB (2020) Anaerobic conversion of saline phenol-containing
wastewater under thermophilic conditions in a membrane bioreac-
Logan BE, Bliven AR, Olsen SR, Patnaik R (1998) Growth Kinetics of
tor. Front Bioeng Biotechnol 8:565311. https://doi.org/10.3389/
Mixed Cultures under Chlorate-Reducing Conditions. J Environ
fbioe.2020.565311
Eng 124(10):1008–1011. https://doi.org/10.1061/(ASCE)0733-
Na JG, Lee MK, Yun YM, Moon C, Kim MS, Kim DH (2016) Microbial
9372(1998)124:10(1008)
community analysis of anaerobic granules in phenol-Degrading
Lopez Barragan MJ, Diaz E, Garcia JL, Carmona M (2004) Genetic clues
UASB by next generation sequencing. Biochem Eng J 112:241–
on the evolution of anaerobic catabolism of aromatic compounds.
248. https://doi.org/10.1016/j.bej.2016.04.030
Microbiol (Reading) 150:2018–2021. https://doi.org/10.1099/mic.
Narihiro T, Nobu MK, Kim NK, Kamagata Y, Liu WT (2015) The nexus
0.27186-0
of syntrophy-associated microbiota in anaerobic digestion revealed
Lovley DR, Lonergan DJ (1990) Anaerobic oxidation of toluene, phenol,
by long-term enrichment and community survey. Environ Microbiol
and p-Cresol by the dissimilatory iron-reducing organism, GS-15.
17(5):1707–1720. https://doi.org/10.1111/1462-2920.12616
Appl Environ Microbiol 56:1858–1864
Narmandakh A, Gad’on N, Drepper F, Knapp B, Haehnel W, Fuchs G
Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM, Flanagan (2006) Phosphorylation of phenol by phenylphosphate synthase:
KA, Aklujkar M, Butler JE, Giloteaux L, Rotaru A-E, Holmes DE, role of histidine phosphate in catalysis. J Bacteriol 188:7815–
Franks AE, Orellana R, Risso C, Nevin KP (2011) Geobacter: the 7822. https://doi.org/10.1128/JB.00785-06
microbe electric’s physiology, ecology, and practical applications. Nobu MK, Narihiro T, Tamaki H, Qiu YL, Sekiguchi Y, Woyke T,
Adv Microb Physiol 59:1–100. https://doi.org/10.1016/B978-0-12- Goodwin L, Davenport KW, Kamagata Y, Liu WT (2014) Draft
387661-4.00004-5 genome sequence of Syntrophorhabdus aromaticivorans strain UI:
Macarie H (2000) Overview of the application of anaerobic treatment to a mesophilic aromatic compound-degrading syntroph. Genome
chemical and petrochemical wastewaters. Water Sci Technol 42(5- Announc 2(1):e01064–e01013. https://doi.org/10.1128/genomeA.
6):201–213. https://doi.org/10.2166/wst.2000.0515 01064-13
Madigou C, Poirier S, Bureau C, Chapleur O (2016) Acclimation strategy Nzila A, Razzak SA, Zhu J (2016) Bioaugmentation: An Emerging
to increase phenol tolerance of an anaerobic microbiota. Bioresour Strategy of Industrial Wastewater Treatment for Reuse and
Technol 216:77–86. https://doi.org/10.1016/j.biortech.2016.05.045 Discharge. Int J Environ Res Public Health 13:846. https://doi.org/
Mao Z, Yu C, Xin L (2015) Enhancement of Phenol Biodegradation by 10.3390/ijerph13090846
Pseudochrobactrum sp. through Ultraviolet-Induced Mutation. Int J Panigrahy N, Barik M, Sahoo NK (2020) Kinetics of phenol biodegrada-
Mol Sci 16:7320–7333. https://doi.org/10.3390/ijms16047320 tion by an indigenous Pseudomonas citronellolis NS1 isolated from
Martinez-Sosa D, Helmreich B, Netter T, Paris S, Bischof F, Horn H coke oven wastewater. J Hazard Toxic Radioact Waste 24:
(2011) Anaerobic submerged membrane bioreactor (AnSMBR) for 04020019-1, 04020019–04020019-1, 04020017. https://doi.org/
municipal wastewater treatment under mesophilic and psychrophilic 10.1061/(asce)hz.2153-5515.0000502
temperature conditions. Bioresour Technol 102(22):10377–10385. Pishgar R, Najafpour GD, Mousavi N, Bakhshi Z, Khorrami M (2012)
https://doi.org/10.1016/j.biortech.2011.09.012 Phenol biodegradation kinetics in the presence of supplementary
Mathur AK, Majumder CB (2010) Kinetics Modelling of the substrate. IJE Transc B: Appl 25(3):181–191. https://doi.org/10.
Biodegradation of Benzene, Toluene and Phenol as Single 5829/idosi.ije.2012.25.03b.05
Substrate and Mixed Substrate by Using Pseudomonas putida. Pishgar R, Najafpour GD, Neya BN, Mousavi N, Bakhshi Z (2014)
Chem Biochem Eng Q 24(1):101–109. https://hrcak.srce.hr/49491. Effects of organic loading rate and hydraulic retention time on treat-
(Accessed Nov 2020) ment of phenolic wastewater in an anaerobic immobilized fluidized
Menashe O, Rosen-Kligvasser J, Kurzbaum E, Suckeveriene RY (2020) bed reactor. J Environ Eng Landsc Manag 22(1):40–49. https://doi.
Structural properties of a biotechnological capsule confined by a org/10.3846/16486897.2013.800079
Pradeep NV, Anupama S, Navya K, Shalini HN, Idris M, Hampannavar aromatica. J Bacteriol 186:8044–8057. https://doi.org/10.1128/JB.
US (2015) Biological removal of phenol from wastewaters: a mini 186.23.8044-8057.2004
review. Appl Water Sci 5:105–112. https://doi.org/10.1007/s13201- Schühle K, Fuchs G (2004) Phenylphosphate carboxylase: a new C-C
014-0176-8 lyase involved in anaerobic phenol metabolism in Thauera
Pradhan B, Murugavelh S, Mohanty K (2012) Phenol biodegradation by aromatic. J Bacteriol 186:4556–4567. https://doi.org/10.1128/JB.
indigenous mixed microbial consortium: growth kinetics and inhi- 186.14.4556-4567.2004
bition. Environ Eng Sci 29:86–92. https://doi.org/10.1089/ees.2011. Scully C, Collins G, O’Flaherty V (2006) Anaerobic biological treatment
0024 of phenol at 9.5–15 °C in an expanded granular sludge bed (EGSB)-
Prpich GP, Daugulis AJ (2005) Enhanced biodegradation of phenol by a based bioreactor. Water Res 40:3737–3744. https://doi.org/10.1016/
microbial consortium in a solid-liquid two phase partitioning biore- j.watres.2006.08.023
actor. Biodegradation 16:329–339. https://doi.org/10.1007/s10532- Sharma NK, Philip L, Bhallamudi SM (2012) Aerobic degradation of
004-2036-y phenolics and aromatic hydrocarbons in presence of cyanide.
Qiu YL, Hanada S, Ohashi A, Harada H, Kamagata Y, Sekiguchi Y Bioresour Technol 121:263–273. https://doi.org/10.1016/j.
(2008) Syntrophorhabdus aromaticivoransgen. nov., sp. nov., the biortech.2012.06.039
first cultured anaerobe capable of degrading phenol to acetate in Shin SG, Koo T, Lee J, Han G, Cho K, Kim W, Hwang S (2016)
obligate syntrophic associations with a hydrogenotrophic Correlations between bacterial populations and process parameters
methanogen. Appl Environ Microbiol 74:2051–2058. https://doi. in four full-scale anaerobic digesters treating sewage sludge.
org/10.1128/AEM.02378-07 Bioresour Technol 214:711–721. https://doi.org/10.1016/j.
Rabus R, Widdel F (1995) Anaerobic degradation of ethylbenzene and biortech.2016.05.021
other aromatic hydrocarbons by new denitrifying bacteria. Arch Shinoda Y, Sakai Y, Ué M, Hiraishi A, Kato N (2000) Isolation and
Microbiol 163:96–103. https://doi.org/10.1007/BF00381782 characterization of a new denitrifying Spirillum capable of anaerobic
Ramakrishnan A, Surampalli RY (2013) Performance and energy eco- degradation of phenol. Appl Environ Microbiol 66(4):1286–1291.
nomics of mesophilic and thermophilic digestion in anaerobic hy- https://doi.org/10.1128/aem.66.4.1286-1291.2000
brid reactor treating coal wastewater. Bioresour Technol 127:9–17. Sieber JR, McInerney MJ, Gunsalus RP (2012) Genomic Insights into
https://doi.org/10.1016/j.biortech.2012.09.071 Syntrophy: The Paradigm for Anaerobic Metabolic Cooperation.
Ramos C, Suárez-Ojeda ME, Carrera J (2016) Denitritation in an anoxic Annu Rev Microbiol 66:429–452. https://doi.org/10.1146/annurev-
granular reactor using phenol as sole organic carbon source. Chem micro-090110-102844
Eng J 288:289–297. https://doi.org/10.1016/j.cej.2015.11.099 Smith AL, Stadler LB, Love NG, Skerlos SJ, Raskin L (2012)
Raper E, Stephenson T, Anderson DR, Fisher R, Soares A (2018) Perspectives on anaerobic membrane bioreactor treatment of domes-
Industrial wastewater treatment through bioaugmentation. Process tic wastewater: A critical review. Bioresour Technol 122:149–159.
Saf Environ Prot 118:178–187. https://doi.org/10.1016/j.psep.2018. https://doi.org/10.1016/j.biortech.2012.04.055
06.035 Suidan M, Najm I, Pfeffer J, Wang Y (1988) Anaerobic biodegradation of
Razo-Flores E, Iniestra-Gonzalez M, Field JA, Olguin-Lora P, Puig- phenol: inhibition kinetics and system stability. J Environ Eng
Grajales L (2003) Biodegradation of mixtures of phenolic com- 114(6):1359–1376. https://doi.org/10.1061/(ASCE)0733-
pounds in an upward-flow anaerobic sludge blanket reactor. J 9372(1988)114:6(1359)
Environ Eng ASCE 129:999–1006. https://doi.org/10.1061/ Surkatti R, Al-Zuhair S (2018) Microalgae cultivation for phenolic com-
(ASCE)0733-9372(2003)129:11(999) pounds removal. Environ Sci Pollut Res 25:33936–33956. https://
Ren J, Li J, Li J, Chen Z, Cheng F (2019) Tracking multiple aromatic doi.org/10.1007/s11356-018-3450-8
compounds in a full-scale coking wastewater reclamation plant: Tauseef SM, Abbasi T, Abbasi SA (2013) Energy recovery from waste-
Interaction with biological and advanced treatments. Chemosphere waters with high-rate anaerobic digesters. Renew Sust Energ Rev
222:431–439. https://doi.org/10.1016/j.chemosphere.2019.01.179 19:704–741. https://doi.org/10.1016/j.rser.2012.11.056
Ribo JM, Kaiser KLE (1983) Effects of selected chemicals to Tawfiki Hajji K, Lepine F, Bisaillon J, Beaudet R (1999) Simultaneous
photoluminescent bacteria and their correlations with acute and sub- removal of phenol, o and p-cresol by mixed anaerobic consortia.
lethal effects on other organisms. Chemosphere 12(11-12):1421– Can J Microbiol 45:318–325. https://doi.org/10.1139/w99-003
1442. https://doi.org/10.1016/0045-6535(83)90073-5 Tawfiki Hajji K, Lepine F, Bisaillon J-G, Beaudet R, Hawari J, Guiot SR
Rosenkranz F, Cabrol L, Carballa M, Donoso-Bravo A, Cruz L, Ruiz- (2000) Effects of Bioaugmentation Strategies in UASB Reactors
Filippi G, Chamy R, Lema JM (2013) Relationship between phenol with a Methanogenic Consortium for Removal of Phenolic
degradation efficiency and microbial community structure in an an- Compounds. Biotechnol Bioeng 67(4):417–423. https://doi.org/10.
aerobic SBR. Water Res 47:6739–6749. https://doi.org/10.1016/j. 1002/(sici)1097-0290(20000220)67:4%3C417::aid-bit5%3E3.0.co;
watres.2013.09.004 2-#
Schauer-Gimenez AE, Zitomer DH, Maki JS, Struble CA (2010) Tay J-H, He Y-X, Yan Y-G (2001) Improved anaerobic degradation of
Bioaugmentation for improved recovery of anaerobic digesters after phenol with supplemental glucose. J Environ Eng 127:38–45.
toxicant exposure. Water Res 44:3555–3564. https://doi.org/10. https://doi.org/10.1061/(ASCE)0733-9372(2001)127:1(38)
1016/j.watres.2010.03.037 Tay ST-L, Moy BY-P, Jiang H-L, Tay J-H (2005) Rapid cultivation of
Schink BY, Philipp B, Müller J (2000) Anaerobic Degradation of stable aerobic phenol-degrading granules using acetate-fed granules
Phenolic Compounds. Naturwiss 23:12–23. https://doi.org/10. as microbial seed. J Biotechnol 115(4):387–395. https://doi.org/10.
1007/s001140050002 1016/j.jbiotec.2004.09.008
Schleinitz KM, Schmeling S, Jehmlich N, von Bergen M, Harms H, Thomas S, Sarfaraz S, Mishra LC, Iyengar L (2002) Degradation of
Kleinsteuber S, Vogt C, Fuchs G (2009) Phenol Degradation in phenol and phenolic compounds by a defined denitrifying bacterial
the Strictly Anaerobic Iron-Reducing Bacterium Geobacter culture. World J Microbiol Biotechnol 18:57–63. https://doi.org/10.
metallireducens GS-15. Appl Environ Microbiol 75(12):3912– 1023/A:1013947722911
3919. https://doi.org/10.1128/AEM.01525-08 Tomei MC, Annesini MC (2005) 4-Nitrophenol biodegradation in a se-
Schmeling S, Narmandakh A, Schmitt O, Gad’on N, Schuhle K, Fuchs G quencing batch reactor operating with aerobic-anoxic cycles.
(2004) Phenylphosphate synthase: a new phosphotransferase cata- Environ Sci Technol 39:5059–5065. https://doi.org/10.1021/
lyzing the first step in anaerobic phenol metabolism in Thauera es0483140
Tremblay PL, Zhang T (2017) Functional Genomics of Metal-Reducing Microbacterium oxydans from the sediment of Taihu Lake
Microbes Degrading Hydrocarbons. Springer International (China). Water Sci Technol 73(8):1882–1890. https://doi.org/10.
Publishing AG 2017, M. Boll (ed.), Anaerobic Utilization of 2166/wst.2016.036
Hydrocarbons, Oils, and Lipids, Handbook of Hydrocarbon and Wang W, Wu B, Pan S, Yang K, Hu Z, Yuan S (2017) Performance
Lipid Microbiology, https://doi.org/10.1007/978-3-319-33598-8_ robustness of the UASB reactors treating saline phenolic wastewater
13-1 and analysis of microbial community structure. J Hazard Mater 331:
Tschech A, Fuchs G (1987) Anaerobic degradation of phenol by pure 21–27. https://doi.org/10.1016/j.jhazmat.2017.02.025
cultures of newly isolated denitrifying pseudomonads. Arch Wang J, Wu B, Sierra JM, He C, Hu Z, Wang W (2020) Influence of
Microbiol 148:213–217. https://doi.org/10.1007/BF00414814 particle size distribution on anaerobic degradation of phenol and
Tschech A, Fuchs G (1989) Anaerobic degradation of phenol via carbox- analysis of methanogenic microbial community. Environ Sci
ylation to 4-hydroxybenzoate: in vitro study of isotope exchange Pollut Res 27:10391–10403. https://doi.org/10.1007/s11356-020-
between 14C02 and 4-hydroxybenzoate. Arch Microbiol 152:594– 07665-z
599. https://doi.org/10.1007/BF00425493 Wirth B, Krebs M, Andert J (2015) Anaerobic degradation of increased
Tyagi M, da Fonseca MM, de Carvalho CC (2011) Bioaugmentation and phenol concentrations in batch assays. Environ Sci Pollut Res 22:
biostimulation strategies to improve the effectiveness of bioremedi- 19048–19059. https://doi.org/10.1007/s11356-015-5100-8
ation processes. Biodegradation 22:231–241. https://doi.org/10. Wu B, He C, Yuan S, Hu Z, Wang W (2019) Hydrogen enrichment as a
3390/ijerph13090846 bioaugmentation tool to alleviate ammonia inhibition on anaerobic
Ucun H, Yildiz E, Nuhoglu A (2010) Phenol biodegradation in a batch jet digestion of phenol-containing wastewater. Bioresour Technol 276:
loop bioreactor (JLB): Kinetics study and pH variation. Bioresour 97–102. https://doi.org/10.1016/j.biortech.2018.12.099
Techol 101:2965–2971. https://doi.org/10.1016/j.biortech.2009.12. Youssef M, El-Shatoury EH, Ali SS, El-Taweel GE (2019) Enhancement
005 of phenol degradation by free and immobilized mixed culture of
US-EPA (2013) “Appendix A to 40 CFR, Part423. – 126 Priority pollut- Providencia stuartii PL4 and Pseudomonas aeruginosa PDM iso-
ants” (Washington, DC) Available at http://www.epa.gov/region1/ lated from activated sludge. Biorem J 23(2):53–71. https://doi.org/
npdes/permits/generic/prioritypollutants.pdf (Accessed Nov 2020) 10.1080/10889868.2019.1602106
van Schie PM, Young LY (1998) Isolation and characterization of Zhai Z, Wang H, Yan S, Yao J (2012) Biodegradation of phenol at high
phenol-degrading denitrifying bacteria. Appl Environ Microbiol concentration by a novel bacterium: Gulosibacter sp. YZ4. J Chem
64(7):2432–2438 Technol Biotechnol 87:105–111. https://doi.org/10.1002/jctb.2689
Veeresh G, Kumar P, Mehrotra I (2005) Treatment of phenol and cresols
Zhang X, Wiegel J (1994) Reversible conversion of 4-hydroxybenzoate
in upflow anaerobic sludge blanket (UASB) process: a review.
and phenol by Clostridium hydroxybenzoicum. Appl Environ
Water Res 39(1):154–170. https://doi.org/10.1016/j.watres.2004.
Microbiol 60:4182–4185. https://doi.org/10.1128/AEM.60.11.
07.028
4182-4185.1994
Wang GY, Wen JP, Yu GH, Li HM (2008) Anaerobic biodegradation of
Zhang T, Ke SZ, Liu Y, Fang HP (2005) Microbial characteristics of a
phenol by Candida albicans PDY-07 in the presence of 4-
methanogenic phenol-degrading sludge. Water Sci Technol 52(1–
chlorophenol. World J Microbiol Biotechnol 24:2685–2691.
2):73–78. https://doi.org/10.2166/wst.2005.0500
https://doi.org/10.1007/s11274-008-9797-0
Wang L, Li Y, Yu P, Xie Z, Luo Y, Lin Y (2010) Biodegradation of Zhou G-M, Fang HHP (1997) Co-degradation of phenol and m-cresol in
phenol at high concentration by a novel fungal strain Paecilomyces a UASB reactor. Bioresour Technol 61(1):47–52. https://doi.org/10.
variotii JH6. J Hazard Mater 183(1-3):366–371. https://doi.org/10. 1016/S0960-8524(97)84698-6
1016/j.jhazmat.2010.07.033 Zhu X, Liu R, Liu C, Chen L (2015) Bioaugmentation with isolated
Wang W, Ma W, Han H, Li H, Yuan M (2011) Thermophilic anaerobic strains for the removal of toxic and refractory organics from coking
digestion of Lurgi coal gasification wastewater in a UASB reactor. wastewater in a membrane bioreactor. Biodegradation 26:465–474.
Bioresour Technol 102:2441–2447. https://doi.org/10.1016/j. https://doi.org/10.1007/s10532-015-9748-z
biortech.2010.10.140
Wang L, Li Y, Niu L, Dau Y, Wu Y, Wang Q (2016) Isolation and Publisher’s note Springer Nature remains neutral with regard to jurisdic-
growth kinetics of a novel phenol-degrading bacterium tional claims in published maps and institutional affiliations.

Anaerobic Biodegradation of Phenol in Wastewater Treatment

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Anaerobic Biodegradation of Phenol in Wastewater Treatment

Uploaded by

Copyright:

Available Formats

Applied Microbiology and Biotechnology (2021) 105:2195–2224

Anaerobic biodegradation of phenol in wastewater treatment:

Introduction refinery, pharmaceutical, coal conversion, and chemical

Why anaerobic treatment? Anaerobic phenol degraders

Fig. 1 Anaerobic phenol

Fig. 2 Anaerobic benzoyl-CoA degradation pathways

Batch tests in SBR

Batch tests with biomass after break up

Fig. 3 Anaerobic specific

Co-metabolism—consortia and pure species

coking WWTP and subjected to

Fig. 4 Aerobic specific

(tubular PVDF membrane)

1:1:1:1 in COD ratio, 2.1–5

Calcium sulphate (CaSO4),

References Butler JE, He Q, Nevin KP, He Z, Zhou J, Lovley DR (2007) Genomic

KSCE J Civ Eng 17(7):1587–1595. https://doi.org/10.1007/s12205- Environ Eng 132(11):1539–1542. https://doi.org/10.1061/(ASCE)

You might also like