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A review on mechanism and future perspectives of cadmium-resistant


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Article  in  International journal of Environmental Science and Technology · July 2017


DOI: 10.1007/s13762-017-1400-5

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Int. J. Environ. Sci. Technol.
DOI 10.1007/s13762-017-1400-5

REVIEW

A review on mechanism and future perspectives of cadmium-


resistant bacteria
S. Z. Abbas1 • M. Rafatullah1 • K. Hossain1 • N. Ismail1 • H. A. Tajarudin1 •

H. P. S. Abdul Khalil1

Received: 18 December 2016 / Revised: 12 February 2017 / Accepted: 11 July 2017


Ó Islamic Azad University (IAU) 2017

Abstract Since the last few decades, cadmium anthro- Introduction


pocentric sources have been increased drastically. Various
chemical and physical approaches for cadmium remedia- The global population has increased from 5.3 to 7.3 billion.
tion have been proposed, but these techniques are quite With this reference, rapid industrialization has been revo-
expensive, not healthy for the environment and not efficient lutionized to provide a so-called better quality of living.
at the low concentration of cadmium. Thus, in the last few Sadly, this raised both water and air pollution. As the water
years, the cadmium removal by biological approaches has is fundamental need of daily life, so many measures have
received a great interest. Many bacteria can resist against taken to remediate the toxic waste from water sources.
high concentration of cadmium through different mecha- Although the numbers have reduced over the years, 159
nisms. The cadmium-resistant bacteria can be grouped into million people still use surface water and 663 million
three levels. The main group consists of bacteria which people worldwide still lack in improved drinking water
efflux the cadmium from the cells. The bacteria of the other resources (WHO/UNICEF 2015). Conventional methods
two groups are capable of detoxifying or binding cadmium. like reverse osmosis, ion exchange, bio-slurries, bio-piles,
The cadA and cadB gene systems are involved in efflux chemical precipitation, electrochemical treatment, and
mechanism, and these encode different efflux pump pro- land-filling, oxidation, reduction and phytoremediation are
teins, while the functional groups such as amine, carboxyl, used for the cadmium remediation from soil and water.
phosphate and hydroxyl facilitate cadmium binding to There are many drawbacks of conventional methods, e.g.,
bacterial surface such as chemisorption. Many enzymes are (1) high maintenance, (2) they are not eco-friendly, (3)
involved in the detoxifying the cadmium and make the pollutants production during secondary treatment and (4)
membrane impermeable against cadmium. This paper also they are unable to remove dissolve gaseous contaminants
reviews the industrial application of cadmium-resistant as in reverse osmosis. So there is a need for innovative,
bacteria and the future perspectives of genetic engineering, low-cost and eco-friendly methods (Vinod and Sashidhar
bioelectrochemical system, microbial aggregates and 2011; Singh and Gadi 2012; Abbas et al. 2014c). Biore-
biosorption of cadmium by algae. mediation is one of the sustainable and eco-friendly pro-
cesses that can prove to be much more efficient and
Keywords Binding sites  Bioreactors  Cadmium  Efflux effective in disposing of heavy metals existed in different
pumps  Enzymatic detoxification  Plasmid genes spheres of the environment. The main aim of this strategy
is to maintain the natural biota with cleaning the environ-
ment (Kumar et al. 2015). According to Glazer and
Editorial responsibility: M. Abbaspour. Nikaido (1995), bioremediation is defined as a process that
uses microorganisms, green plants or enzymes to treat the
& M. Rafatullah polluted sites for regaining their healthy condition. This
mrafatullah@usm.my
technique is more favorable than conventional techniques
1
School of Industrial Technology, Universiti Sains Malaysia, due to low cost and economic inputs. Bioremediation can
11800 Gelugor, Penang, Malaysia be pronounced solution for removal of transition metals

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Int. J. Environ. Sci. Technol.

due to its high cost-effective and eco-friendly properties cells, plastics, jewelry, metal plating, nickel–cadmium
(Gaur et al. 2014). batteries, paints, pigments, dyes, photovoltaic devices and
Cadmium usually forms complex oxides with lead, zinc, many other industrial processes. The renal tubules are the
copper ore, zinc, sulfides and carbonates because it nor- target organ in the chronic poisoning but in acute expo-
mally not exists in pure form in the environment. sure only respiratory tract irritation (Nancharaiah et al.
(Monachese et al. 2012). Cadmium oxide is most insoluble 2015). Workers exposed to high cadmium concentration
in water than cadmium sulfate and cadmium chloride may develop glomerular damage, respiratory damage like
(Darwish et al. 2016). The cadmium release by different emphysema and pneumonitis, renal disease, non-hyper-
sources into environment grouped as natural sources trophic, chronic rhinitis, insomnia, eosinophilia, anemia,
includes earth’s crust and mantles, such as weathering of renal proximal tubular dysfunction and acute respiratory
rocks and volcanic activity (Kesler and Simon 2015). The distress syndrome. The US National Toxicology Program
raw materials such as fossil fuels extracts, phosphate and International Agency for Research on Cancer have
minerals, electroplating, leather tanning, cement produc- been classified the cadmium a human carcinogen. Cad-
tion, pesticides, fertilizers, anticorrosive agents treated and mium causes the genomic instability in the humans,
recycled materials, particularly zinc and copper, are listed which induces the carcinogenesis. The target organs of
under anthropogenic sources (Adriano 2013). According to cadmium for carcinogenesis are pancreas, pituitary, liver,
numerical data in Table 1, the total anthropogenic global adrenal, prostate and haematopoietic system. The car-
air emission is approximately 3000 tonnes in 1995. cinogenesis mechanism includes the clastogenic nature of
Richardson et al. (2001) were estimated that the cadmium cadmium. The cadmium interferes with major DNA repair
release by anthropogenic sources exceeds than by natural pathways like cadmium interaction with the DNA
sources. However, natural releases are less significant for nucleotide excision base pair, double-strand break repair,
the long-range transport of cadmium due to differences in DNA mismatch repair, DNA base excision repair and cell
particle size. Cadmium intake is reduced in the countries cycle checkpoints (Filipič 2012). In this reference, envi-
where cadmium emission in the air has been decreased. ronmental remediation through microbes has been an
Most cadmium enters into food through agriculture prod- encouraging aspect. Many mechanisms are used by
ucts because plants absorb cadmium from the air that microorganisms to adjust with cadmium stress like cad-
comes from air deposition or in certain fertilizer through mium accumulation, enzymatic detoxification, active
bioaccumulation and biomagnification. The re-suspension efflux of cadmium and cadmium ions sequestration. The
of dust in heavily contaminated areas causes contamination remediation of cadmium from water and wastewater by
of crops and exposure to human through ingestion and using different microbes has raised high hopes for eco-
inhalation (Martin et al. 2014). The cadmium exposure friendly and cost-effective approaches. This review aims
starts early in life as children expose to foodstuffs as shown to provide current advances of cadmium-resistant mech-
in Table 2 which explains the amount of cadmium in the anisms in bacteria, their industrial applications and future
daily food diet in different countries. prospects. This extensive study has been carried out
Workers may be exposed to cadmium in the steel, during 2015–2016 in Universiti Sains Malaysia, Penang,
copper and zinc industries, in the production of solar Malaysia.

Table 1 Two examples of Source category Cadmium emission in tonnes/year


estimated global emission of
cadmium to the atmosphere Richardson et al. (2001) Nriagu (1989)
from natural sources
Mean 5–95th percentile Mean Range

Release of soil particles during dust storms, etc. 24,000 3000–69,000 210 10–400
Sea salt spray 2000 103–6700 60 0–110
Volcanic emissions 1600 380–3800 820 140–1500
Natural fires 13,000 4400–30,000 110 0–220
Vegetation, pollen and spores – – 190 0–1530
Meteoritic dust 0.0002 0.00004–0.0004 50 0–100
Total 41,000 15,000–88,000a 1300 150–2600b
a
Statistical figures for total emissions are derived by statistical calculations and not by simple addition of
source-specific figures (Richardson et al. 2001)
b
Sum as reported by Nriagu (1989)

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Int. J. Environ. Sci. Technol.

Table 2 Daily intake of cadmium via food: country examples


Country Type of consumption data/intake Average dietary intake Population group Information source
study lg of cadmium per kg
body weight per day

Submission to this assessment


Australia Total diet study by Food 0.08–0.24 Males 25–34 years Australia’s submission
Standards Australia (2005)
New Zealand 2002
0.07–0.22 Females 25–34 years
0.11–0.29 Boys 12 years
0.09–0.22 Girls 12 years
0.18–0.57 Toddler 2 years
0.13–0.68 Infant 9 months
Burkina Faso Total diet study calculated from 0.28 – Burkina Faso’s submission
average total daily intake assuming (2005)
an average weight of 60 kg
Finland 0.17 – NFA (2002) submitted by
Finland
Japan Total diet studies in 10 locations 0.43 – Japan’s submission (2005)
Mexico Calculated from average total daily 4.88 Population of Mezquital Mexico’s submission (2005)
intake assuming an average weight Valley in Hidalgo
of 60 kg
Reported previously (based on WHO 2004)
Austria Disappearance 0.15 – WHO (2004)
Canada Total diet study 0.22 – WHO (2004)
China Total diet studies 0.21–0.51 Adult males WHO (2004)
0.13 Adult females
Czech Republic Total diet study 0.26 – WHO (2004)
Denmark National consumption survey 0.28 – WHO (2004)
France Household consumption survey 0.22 – WHO (2004)
Germany Total diet study 0.18 WHO (2004)
National consumption survey 0.19 Males
0.16 Females
Greece Total diet study 0.74 – WHO (2004)
Not specified 0.94
Italy National consumption survey 0.33 – WHO (2004)
Japan Duplicate diet study 0.36 – WHO (2004)
0.31
Netherlands National consumption survey 0.33–0.40 Males aged 16–70 years WHO (2004)
0.31–0.38 Females aged 16–70 years
New Zealand Total diet study 0.40/0.24 Young males Vanoort et al. (2000)
0.33/0.19 Adult males
0.33/0.16 Females
0.24 Female vegetarians

Mechanisms of cadmium remediation through mechanisms have been also developed by the bacterium to
bacteria resist against the heavy metals as shown in Fig. 1. These
strategies play important role in such situations where high
The binding with polythiols is the main mechanism in the concentrations of heavy metals do not have any toxic effect
eukaryotic microorganisms for the detoxification of cad- on cell division of resistant microbes (Mota et al. 2015).
mium as well as other heavy metals. Sidewise, many The heavy metals-resistant genes are mostly located on

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Int. J. Environ. Sci. Technol.

plasmids in bacteria. Due to this plasmid, bacteria can binding cassette (ABC) superfamily, the multidrug and
competitively resist against heavy metals. According to toxin extrusion (MATE) family, the small multidrug
some data, multiple antibiotic resistance is associated with resistance (SMR) family and the major facilitator super-
cadmium resistance on R plasmid. Normally R plasmid family (MFS).
exists in the clinically human isolates pathogens like Most RND transporters, like AcrAB–TolC complex in
Pseudomonas aeruginosa, Klebsiella pneumoniae, Sta- Escherichia coli and the MexBA–OrpM complex in P.
phylococcus aureus and others (Chen et al. 2014). The loci aeruginosa, have been found in Gram-negative bacteria
of genes are involved in cadmium resistance either on with unique tripartite complex containing the periplasmic
plasmid or on chromosome as shown in Table 3; the fol- adaptor protein, transmembrane pump and the outer
lowing mechanisms are involved in bacterial cadmium membrane channel. In the Gram-negative bacteria, the
resistance. resistance against multidrug is due to RND transporters.
Recently, a homolog of the E. coli protein AcrB is found in
Efflux mechanisms the S. aureus as FarE also component of a RND tripartite
efflux system. So, in S. aureus the resistance against drugs
Many efflux mechanisms have been studied. Efflux pumps due to the presence of FarE even antimicrobial fatty acids
consist of integrated membrane proteins for the extrusion are its only identified substrates (Alnaseri et al. 2015). The
of biocides, antibiotics, toxic metals and toxic agents from ABC transporter contains of four conserved domains: two
within the bacteria into the environment. The S. aureus is transmembrane domains and two nucleotide-binding
well studied for efflux mechanism (Andersen et al. 2015) as domains. For example, chromosomally encoded Sav1866
shown in Fig. 2. Until now due to advancement in genome and AbcA are staphylococcal ABC transporters. Based on
analysis and bioinformatics, more than 20 putative efflux in vitro data, ABC efflux pumps MsrA functions with other
pumps proteins either encoded by plasmids or chromosome transmembrane proteins because it only consists of a
have been characterized in S. aureus (Schindler et al. nucleotide-binding domain. ATP hydrolysis facilitates
2015). The drug-resistant efflux pumps are also resistance ABC transporters. The energy-dependent conformational
to heavy metals. The efflux pumps found in S. aureus are changes and overall translocation cycles of substrate are
classified into five membrane protein families: the resis- driven by hydrolysis and binding of ATP. Plasmid-medi-
tance-nodulation-division (RND) superfamily, the ATP- ated Vga proteins are MsrA-like ABC transporters in S.

Fig. 1 General cadmium resistance mechanisms operating in bacteria

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Int. J. Environ. Sci. Technol.

Table 3 Examples of different resistant pathways adapted by cadmium-resistant bacteria


Microorganisms Location of resistance Suggested mechanisms Other metals References

Staphlococcus aureus R plasmid Efflux (cadA) Zn Jang (2016)


Chromosome Efflux Hg
R plasmid Binding (cadB)
Bacillus subtilis Chromosome Permeability Sarin and Sarin (2010)
Pseudomonas aeroginosa R plasmid Efflux Hg Kermani et al. (2010)
Pseudomonas putida Plasmid Binding Shamim and Rehman (2015)
Pseudomonas crucivae Sabdono (2011)
Klebsiella pneumoniae R plasmid Efflux Hg
Klebsiella aerogenes Chromosome Binding (capsule) Coelho et al. (2015)
Alcaligenes autrophus Plasmid Efflux Zn, Co Xia et al. (2010)
Citrobacter Chromosome Precipitation as CdHPO4 Shim et al. (2015)
Proteus mirabilis Chromosome Binding (envelop) Islam et al. (2014)
Arthobacter viscosus Chromosome Binding (exopolysaccharide) Moberly et al. (2010)
Rhodococcus fascians Plasmid – As Sachdev and Cameotra (2013)
Acidithiobacillus ferrooxidans Chromosome Efflux Zn Chen et al. (2015)
Acidiphilium symbioticum – Binding (envelop) – Chakravarty and Banerjee (2012)
Bacillus cereus RC-1 – Binding (envelop) – Huang et al. (2014)
Lactobacillus rhamnosus LC-707 – Binding (envelop) Monachese et al. (2012)
Propionibacterium freundenreichii – Binding (envelop)
Lactobacillus rhamnosus GG – Binding (exopolysaccharide)
Bifidobacterium longum – Binding (exopolysaccharide)
Lactobacillus kefir – Precipitation as CdS
Escherichia coli P4 Chromosome Efflux – Khan et al. (2015)

aureus that consist of ATP-binding domains without cadA gene is located on plasmid pI258 from which a DNA
transmembrane partners (Lewis et al. 2012). MATE efflux fragment was isolated. Other resistance mechanisms like
proteins possess 12 transmembrane helices and contain change in the binding sites are due to the another gene
400–700 amino acids. In S. aureus, MepA is the only cadB also located on the plasmid. The gene cadB confers
classified MATE protein (Jang 2016). The Staphylococcal the resistance to cadmium and also other heavy metals, but
SMR transporters identified so far include Smr (QacC, the location of cadA and cadB genes is same on plasmid
QacD or Ebr), QacG, QacH and QacJ. These proteins are (Wheaton et al. 2015).
carried on plasmids and smaller than other efflux pump The cadmium resistance in Alcaligenes eutrophus and
proteins, which proliferate among the bacteria (Costa et al. Ralstonia sp. CH34 is also conferred by plasmid-encoded
2013). The MFS has been the most extensively studied efflux pumps identified in the Czc and Cad systems,
among staphylococcal efflux pumps and includes NorA, respectively. The cadAB operon encodes Cad system, with
NorB, NorC, LmrS, QacA, QacB MdeA and SdrM, efflux cadA gene for cadmium resistance, while in the absence of
pumps. MFS transporters of Staphylococcal typically the cadA gene cadB gene is only expressed. In A. eutro-
arrange into 12- or 14 membrane-spanning helices and phus, Czc system effluxes zinc and cobalt in addition to
consist of 380–520 amino acids that have a big cytoplasmic cadmium and is encoded by two plasmids, pMOL28 and
loop between helices 6 and 7 forming the typical MFS pMOL30. It contains several genes: czcA, czcB, czcC,
folds (Yan 2013). In S. aureus, except for QacA and QacB, czcD, czcI and czcN (Xia et al. 2010).
the MFS transporters are chromosomally encoded. SMR The efflux mechanism is also well studied in the
transporters consist of about 110 amino acids and four Acidithiobacillus ferrooxidans. The cadmium enters into
transmembrane helices (Wassenaar et al. 2015). cells during the initial concentration and increases the
In S. aureus, the resistance against cadmium is due to intracellular concentration, by its excretion from the cells
many systems. The cadA system is involved in resistance during subsequent growth and adaptation. After analyses
against cadmium and zinc because it codes for an energy- by sequence homology, it was predicted that ten possible
dependent efflux mechanism (Herzberg et al. 2016). The identified genes participate in homeostasis of cadmium,

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Int. J. Environ. Sci. Technol.

Fig. 2 Graphical overview of cadmium and bacterial synergism. of Smt metallothionein on bacterial chromosome to protect against
a Environmental Cd(II) ions; b sorption of Cd(II) on the protein and the adverse effect of these Cd ions; g cadCA operon on S. aureus
carbohydrate of bacterial wall; c MIT-metal transporter inside the plasmid: h export of chelating compounds, which combine with
cell; d cadCA protein (efflux transporter); e CDF (cation diffusion Cd(II) ions directly outside to form complexes, which cannot invade
facilitator); f intracellular sequestration: transcription and translation into cell

and the cells were also cultured in the presence of Enzymes that make the bacterial cell wall
increasing concentrations of toxic divalent cadmium to impermeable to the cadmium
check the expression of these genes. A putative cadmium/
lead responsive transcriptional regulator is encoded by one In the Gram-negative and Gram-positive bacteria, the
gene (cmtRA.f); the cadmium efflux proteins are encoded cadmium enters the cell as the toxic alternative substrate of
by four genes (czcA1A.f, czcA2A.f, czcB1A.f and zinc and manganese transport system, respectively. These
czcC1A.f); a putative cation channel protein related to the both systems are chromosomally coded (Filice et al. 2016).
transport of cadmium is encoded by two genes (cadA1A.f This impermeable strategy is best reported in the Bacillus
and cadB1A.f). At low cadmium concentration, no signif- subtilis where it is associated with the chromosomal
icant enhancement of gene expression has happened. mutation so after this mutation the entrance of cadmium is
Except cmtRA.f, most of the putative cadmium resistance blocked by membrane of manganese transport system
genes are up-regulated, cadB3A.f and czcB1A.f at higher (Zheng et al. 2016).
concentrations (Chen et al. 2015). The cadmium-induced
efflux mechanism is also present in the E. coli P4 strain. Enzymes which catalyze transformation of cadmium
The expression of genes mutS, ftsZ, clpB, ef-tu and dnaK to non-toxic forms
also changes in the presence of cadmium. A remarkable
difference in the banding pattern of E. coli P4 strain was For the detoxification of heavy metals, biological conver-
observed by sodium dodecyl sulfate polyacrylamide gel sion is an important strategy that is adopted by many
electrophoresis (SDS-PAGE). The chromosomal-borne organisms like bacteria and fungi. The organometallic
cadmium resistance in E. coli P4 was due to czcB gene, a metals or compounds undergo changes in valency through
component of czcCBA operon. Furthermore, it consists of biological action (Dixit et al. 2015). This bioconversion
smtAB gene, which plays an important role in cadmium result in metal undergoes valency change, and less volatile
resistance (Khan et al. 2015). and toxic compounds have been produced in many cases,

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Int. J. Environ. Sci. Technol.

like reduction of mercury ions to metallic mercury and the Styllisa massa and screened them for cadmium accumula-
oxidation of arsenite to arsenate. But still the conversion of tion or binding genes by the radioisotope. They found the
cadmium to Cd0 biologically is unknown (Guo et al. 2016). open reading frame in the clone 247-11C that represents
The conversion of metals to organometallic compounds the cadmium accumulation. This open reading frame was
leads to another important detoxification mechanism which further analyzed by gel electrophoresis technique and noted
is methylation. Mercury and lead are the only two metals the functional protein named as Cdae-1. The composition
that can undergo methylation. The free metal forms are less of Cdae-1 consists of a single peptide and domain har-
toxic than products after methylation; for example, methyl boring an E (G/A) KCG pentapeptide motif. When this
mercury and dimethyl mercury are more toxic than mer- gene was cloned in E. coli, the cadmium accumulation
cury. However, volatile compounds are formed by chemi- range of E. coli was higher than non-clone E. coli strain.
cal and microbial degradation of methylated products. The mechanism of this Cdae-1 to bind with cadmium is
Many organocadmium compounds have been manufac- totally different from the other cadmium-binding proteins
tured; for example, diorganocadmium is analogous to like metallothioneins and phytochelatins because in the
dimethyl mercury compounds that have showed more Cdae-1 very important amino acid residues are present.
thermolabile and light-sensitive properties. The biological Many bacteria have a charge-mediated attraction in the cell
conversion of cadmium and lead is only proved by one wall or envelop that is capable adsorbing high levels of
report (Pavić et al. 2015). dissolved cadmium ions. Normally, these bacteria bind
with cadmium through exopolysaccharides (EPSs). In
Bindings of cadmium ions particular, uronic acid-rich EPSs has high cadmium-bind-
ing ability. The EPSs are an inducible resistance mecha-
The cadmium-resistant bacteria have also adopted the nism developed in the response to metals (Bramhachari and
strategy to bind the cadmium with intracellular binding Nagaraju 2017).
proteins (bacterial metallothioneins and metallochaper- The different bacterial species had various cadmium-
ones), cell wall components (exopolysaccharides) or at binding abilities at different external conditions; for
surface factors. For example, cadmium binds to the cap- example, Alcaligenes xylosoxidans had an equal capacity
sular surface in some bacteria like Arthobacter viscosus of cadmium binding, but A. eutrophus CH34 had the high
and Klebsiella aerogenesis, while in some bacteria cad- cadmium-binding ability than A. xylosoxidans at the same
mium binds with insoluble cell-bound CdHPO4 and stores temperature but with variable pH. Chakravarty and Ban-
intracellularly like mutant citrobacter (Coelho et al. 2015). erjee (2012) also agreed that cadmium biosorption is also
It is conceivable that whether the primary function of influenced by certain conditions. They isolated a cadmium-
intracellular binding proteins is to sequester and store resistant, Gram-negative, acidophilic and heterotrophic
micronutrients in the cell or increase the resistance against bacterial strain named as Acidiphillium symbioticum. The
cadmium. Although cell wall has ability to bind with results of TEM, SEM and FTIR of A. symbioticum indi-
cadmium, but this is not considered as resistance mecha- cated that the anionic functional group present in the cell
nism. Bacterial metallothioneins have ability to bind with envelope was the main agent of cadmium binding to this
Zn2? and Cd2? and are small cysteine-rich proteins (Naik bacterium (Rajesh et al. 2014).
and Dubey 2017). The main function of metallothioneins is The A. symbioticum at pH 6.0 adsorbed 248.62 mg of
lowering the free ion concentrations within the cytoplasm cadmium per gram of biomass. When this anionic func-
and cytoplasmic metal cation-binding proteins. The tional group was blocked by chemical modifications, the
sequences of amino acids in metallothioneins are not adsorption of cadmium in this bacterium also occurs
homologous so they don’t have any relation with the through complex formation and electrostatic reaction (Du
evolution of animal metallothioneins. The first bacterial et al. 2016). Huang et al. (2014) also studied that how the
metallothionein smtA was characterized in Synechococcus cadmium adsorption by Bacillus cereus is influenced by
PCC 7942 function as sequester and detoxifies Cd2? and environmental conditions. They noted that cell morphol-
Zn2?. The mutant lacking smtA gene binds less cadmium ogy, growth and cadmium adsorption mechanisms totally
than wild-type strain. Later smtA also is found in the An- depend upon the cadmium concentrations. When the cad-
abaena PCC 7120, P. aeruginosa and Pseudomonas putida mium concentration was low, the intracellular cadmium
(Malekzadeh and Shahpiri 2017). Recently, the gene accumulation was high and extracellular adsorption was
involved in cadmium accumulation is identified by Mori high at high cadmium concentration. At the end, it can be
et al. (2016). They isolated a clone 247-11C from total suggested that experimental conditions and bacterial spe-
3301 randomly selected clones from a marine sponge cies are very important for cadmium removal capacity.

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Int. J. Environ. Sci. Technol.

Cadmium-resistant bacteria strains the mostly demonstrated low resistance


(\500 lg mL-1). The Bacillus safensis which was also
Microbial diversity has gained much interest in bioreme- isolated from Mangrove sediments showed only resistance
diation due to its adaptability and the search for identifi- up to 20 mg L-1 against cadmium (Priyalaxmi et al. 2014).
cation of new capable strains continues, as only a small This fact strengthens the hypothesis that bacterial remedi-
portion of the microbial strains in the environment is ation can deal with highly polluted sites as well as complex
explored. Microbial populations are normally present in the streams containing cadmium subjected to judicial scrutiny
metal-contaminated environments and can tolerate toxic of the strains to be employed. The information on the
concentrations of heavy metals (Narayani and Shetty relative growth rate of the isolate in the presence of cad-
2013). Tolerance to heavy metals is often evaluated mium will form another important input for the process.
through the determination of minimum inhibitory concen-
tration (MIC) against the test microorganisms. The MIC of
the metal against the strain can be defined as the lowest
Cadmium uptakes by bacterial strains
concentration of the metal, which inhibits the growth of the
microorganism (Vipra et al. 2013).
Generally, the process of heavy metals removals by
The MIC of some strains against cadmium is very high.
microorganism includes bioaccumulation and biosorption.
The Cupriavidus taiwanensis KKU2500-3 and P. aerugi-
Biosorption process involves metal ions which are adsor-
nosa KKU2550-8, P. aeruginosa KKU2550-9 and P.
bed by microorganisms through the biochemical reactions
aeruginosa KKU2550-20 which were isolated from Thai
including chelate, complex and ions exchange.
Jasmine rice (Kao Hom Mali 105) could resist cadmium up to
The Halomonas BVR1 was isolated from the electronic
500 lmol L-1 cadmium chloride and 200 lmol L-1 cad-
industry effluent, and this bacteria had cadmium absorption
mium chloride, respectively (Siripornadulsil and Siripor-
capacity up to 12.023 mg g-1 (Rajesh et al. 2014). The
nadulsil 2013). Stanbrough et al. (2013) also isolated a
Citrobacter sp. JH 11-2 was also isolated from soil mining
cadmium-resistant bacterium Achromobacter sp. strain
sites near disposed electronic industry and efficiently
AO22 from soil and noted its resistance against cadmium
removed the cadmium about 47.7% (Shim et al. 2015). The
was up to 100 mg L-1. The Halomonas BVR 1 which was
bacterial strains isolated from textile industry dye effluents
purified from electronic industry effluent could also tolerate
Bacillus licheniformis showed cadmium removal ability up
the cadmium up to 250 mg L-1 at pH 8.0 (Rajesh et al.
to 98.34% as compared with other bacterial strains like
2014), the Citrobacter sp. JH 11-2 which was also isolated
Salmonella typhi, Pseudomonas fluorescence and E. coli
from soil mining sites near disposed electronic industry
which showed a maximum cadmium removal about 92.4,
showed the highest MIC against cadmium that was
94.8 and 92.06%, respectively (Basha and Rajaganesh
300 mg L-1 (Shim et al. 2015). The bacterial strains
2014).
Acinetobacter brisouii, Pseudomonas abietaniphila, Ex-
Abbas et al. (2014a, b, 2015) characterized six bacterial
iguobacterium aestuarii and Planococcus rifietoensis which
isolates from industrial effluents of Penang, Malaysia.
were isolated from coastal sediments of Vietnam also
Based on 16S rDNA sequence analysis, strains were
showed high resistance against cadmium 100, 130, 60 and
identified as Salmonella enterica, Pantoea sp. RL32.2,
400 mg L-1, respectively (Bhakta et al. 2014). Abbas et al.
Enterobacter sp. OCPSB1, Pseudomonas sp. M3, Enter-
(2014a, b) isolated four bacterial strains from industrial
obacter mori and Enterobacter sp. WS12. analysis. The
effluents of Penang, Malaysia. The Pantoea sp. RL32.2,
bacterial strains Salmonella enterica, Pantoea sp. RL32.2,
Salmonella enteric and Enterobacter sp. OCPSB1 could
Enterobacter sp. OCPSB1, Pseudomonas sp. M3, Enter-
tolerate the cadmium concentration up to 750, 410 and
obacter mori and Enterobacter sp. WS12. were able to
550 lg mL-1, respectively, while MIC of Pseudomonas sp.
remove 82.10, 89.89, 89.14, 70, 87.75 and 85.11% of
M3 against cadmium was 550 lg mL-1. Mustapha and
cadmium, respectively, at pH 7.0 and 35 °C when the
Halimoon (2015) also isolated the uncultured strains denoted
100 lg mL-1 of cadmium was added to the medium. The
as MH1, MH4, MH6, MH15 and MH21. The MH4, MH6 and
molecular weights of induced proteins were 25 kDa and
MH15 were able to resist up to 50 mg L-1 and MH1, and
35 kDa in the presence of cadmium which indicates a
MH 21 could tolerate 200 mg L-1 of cadmium. The Pseu-
possible role of these proteins in cadmium uptake.
domonas mendocina strain E67 was also resistant to
Kim et al. (2015) isolated Bacillus catenulatus JB-022
100 mg L-1 of cadmium in the aqueous solution of cad-
from polluted ponds and soil and measured its potential
mium chloride (Mathivanan and Rajaram 2014).
biosorption of cadmium about 66%. The bacterial isolates
Some strains showed low cadmium tolerance level as
A. brisouii, P. abietaniphila, E. aestuarii and P. rifietoensis
Varghese (2012) also studied that out of 164 collected
from coastal sediments of Vietnam showed a relatively

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higher cadmium removal efficiencies 95, 79, 86, and 99%, bioreactor for cadmium resistance bacteria such as batch,
respectively (Bhakta et al. 2014). The B. safensis which continuous and advance system. The parameters such as
was also isolated from Mangrove sediments showed 83.5% temperature, aeration, pH, temperature and agitation are
of cadmium removal (Priyalaxmi et al. 2014). important factors for cadmium resistance bacteria to sur-
The cadmium absorption properties of Arthrobacter vive. In addition, bioreactor has the capability to control all
nicotianae was compared with other bacterial species. In the factors and less contamination (Boopathy 2000; Saeed
the aqueous solution, A. nicotianae showed the highest and Iqbal 2003; Malakahmad et al. 2011; De et al. 2006;
cadmium absorption capacity (Tsuruta et al. 2014), the Özdemir et al. 2013).
cadmium biosorption capacities of red sea isolates Al-
teromonas macleodii and Nitratireductor basaltis in Batch operation
aqueous solution were 53 and 50%, respectively (Shaaban
et al. 2015), and biosorption ability of P. mendocina strain The batch system can be defined as a system where
E678 was up to 99% in cadmium chloride (Mathivanan and microorganism and substrate mix homogenously inside the
Rajaram 2014). A novel glyphosate-degrading bacterium reactor and permit the occurrence of reactions such as
Ochrobactrum sp. GDOS isolated from pesticide-contam- removal, absorption, adsorption or precipitation in the
inated agricultural soils could also uptake the same reactor. Easy to operate and less contamination are
83.33 mg g-1 of cadmium (Khadivinia et al. 2014). the key factors that contribute to the selection of this sys-
Another novel bacterium Brevundimonas sp. ZF12 was tem by researchers and industries (Wang and Jin 2009).
isolated from a hot spring in high radiations background However, the productivity, such as cell production and
areas had the ability of cadmium uptake up to 90% (Ma- reaction activity, is quite slow compared to the continuous
soudzadeh et al. 2011). system. Improvement has been done by previous
The cadmium removal capacities of zinc mines isolated researchers with combination or altered batch system to
bacteria also high. Tsukamurella paurometabola A155, P. increase the performance, namely sequencing batch reactor
aeruginosa B237 and C. taiwanensis E 324 which were and immobilized cell (Malakahmad et al. 2011; Saeed and
isolated from the zinc mines of Thailand could bioaccu- Iqbal 2003). As bacterial strains Cicerarientinum (Saeed
mulate the 16.89 mg g-1 of cadmium (Limcharoensuk and Iqbal 2003), sulfate-reducing bacteria and Rhodospir-
et al. 2015). The coal mine isolated bacteria Anabaena ilium sp. (Malakahmad et al. 2011), Alcaligenesfaecalis
doliolum Ind1 could also remove the about 92% of cad- (De et al. 2006), Mutated P. aeruginosa (Kermani et al.
mium (Goswami et al. 2015). Wu et al. (2014) isolated 2010), thermophilic bacteria like Geobacillus ther-
Enterococcus faecalis from petrochemical wastewater. mantarcticus and Anoxybacillus amylolyticus (Özdemir
This bacterium could absorb 0.3 mmol L-1 both intracel- et al. 2013) were showed the performance as follow 90% in
lularly and extracellularly because the cadA, ppx and dsbA 10 mg L-1 Cd2?, 96–98% in 0.1-15.5 mg L-1 Cd2?, 70%
were involved in cadmium absorption. The evidence from in a 100 mg L-1 Cd2?, 94.7% from 60 mg L-1 Cd2? and
the recent study also revealed that the CdS nanoparticles 50–70% from 1.83 to 11.43 mg L-1 Cd2?, respectively.
are synthesized by extracellular polymeric substances of Generally, the basic concept of batch cultures and
bacteria that help in uptake of cadmium ions from aqueous growth of microorganism will pass through a number of
solution. The CdS nanoparticles of P. aeruginosa JP-11 in phases and typically start with the lag phase (acclimatizing
functionalized extracellular polymeric substances removed phase) in which the cells adapt to their new environment
about 88.66% of cadmium (Raj et al. 2016). The different (Malakahmad et al. 2011). The specific growth rate (l)
bacterial strains and their cadmium removal capacity with then slowly accelerates until it reaches the log or expo-
various experimental conditions are also listed in Table 4. nential phase. In this phase, the growth is only limited by
the capacity of biomass to grow [the maximum specific
growth rate (lmax) and the cell concentration (x)]. When
Industrial applicability of cadmium-resistant the microorganisms grow in the exponential phase for
bacteria some time, cadmium removal, nutrient depletion and pos-
sible end-product inhibition will occur causing the growth
Bioreactor rate to slow down and finally stop as the culture enters the
stationary phase (Medircio et al. 2007).
Bioreactor for cadmium resistance bacteria is not new to
the environmental industry. Most of previous researchers Continuous operation
have applied bioreactor into their pilot-scale research par-
ticularly in the liquid or slurry substrate. Recently, based The main concept for continuous operation is that it is an
on previous work, there are three main systems of open system. Therefore, the possibility for contamination

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Table 4 List of cadmium-resistant bacteria isolated from different sources with their removal capacity at different operating factors
S. no. Bacterial strains Cadmium Optimum Optimum References
removal capacity pH temperature (°C)

1. Pseudomonas sp. 40% 7.0 37 Bruins et al. (2000)


2. Bacillus thuringiensis 79% 6.9 37 El-Helow et al. (2000)
3. Enterococcus faecium 98.1% 5.0 37 Valls and De Lorenzo (2002)
4. Pseudomonas putida 80% 6.0 37 Pardo et al. (2003)
5. Alcaligenes eutrophus CH34 99% 9 37 Mahvi and Diels (2004)
6. Alcaligenes xylosoxidans 60.4% 7.0 37 Chovanová et al. (2004)
7. Pantoea sp. TEM 18 50% 6.0 25 Ozdemir et al. (2004)
8. Baccilus licheniformis 62 mg g-1 – – Zouboulis et al. (2004)
Baccilus laterosporus 72.6 mg g-1 – –
9. Halophilic bacteria 92.74% 7.2 45 Massadeh et al. (2005)
10. Bacillus circulans EB 15.8 mg g-1 7.0 – Yilmaz and Ensari (2005)
11. Enterobacter sp. J1 90% 5.0 37 Lu et al. (2006)
12. Pseudomonas pseudoalkaligenes PTCC 1666 40–90% 7.0 30 Shirdam et al. (2006)
Pseudomonas putida 99.9% 8.1 30
13. Rhodotorula sp. Y11 11.38 mg g-1 – – Li and Yuan (2006)
14. Stenotrophomonas maltophilia 80% 7.0 37 Chien et al. (2007)
E. coliJM109 63.26 mg g-1 4.6 – Deng et al. (2007)
-1
15. Pseudomonas sp. 250 mg g 7.0 – Ziagova et al. (2007)
Staphlococcus xylosus 278 mg g-1 7.0 –
16. Pseudomonas aeruginosa strain KUCd1 75–89% – – Sinha and Mukherjee (2008)
17. Pseudomonas veronii 2E 50% 7.5 32 Vullo et al. (2008)
18. Rhodobacter sphaeroides 30–40 mg g-1 – 35 Bai et al. (2008)
19. Halomonas sp. 50% 3.0 25 Ali et al. (2009)
20. Pseudomonas aeruginosa 43.3% 6.5 36 Zeng et al. (2009)
21. Chryseomonas luteola 0.67 mg g-1 7.0 30 Zeid et al. (2009)
22. Bacillus subtilis TP8 16.7% 6.8 30 Sarin and Sarin (2010)
23. Pseudomonas aeruginosa 94.7% 8.0 42 Kermani et al. (2010)
24. Caulobacter crescentus 99% 7.0 30 Patel et al. (2010)
25. Bacillus jeotgali U3 99.9 mg g-1 – 35 Green-Ruiz et al. (2008)
26. Ochrobactrum sp. CdSP9 0.214 mg g-1 6.0–9.0 10–42 Pandey et al. (2010)
27. Pseudomonas sp. M3 79% 7.0 35 Abbas et al. (2014a)
28. Alcaligenes xylosoxidans 65.65% 7.0 35 Divya and Kumar (2011)
29. Pseudoalteromonas sp. strain CD15 68–90% 7.0 37 Sabdono (2011)
30 Bacillus Sp. EM L14 93.7% – – Luo et al. (2011)
31 Brevundimonas sp. ZF12 90% 4.0 – Masoudzadeh et al. (2011)
32. Rhizobium leguminosarum bv. vicia 167.5 mg g-1 – – Abd-Alla et al. (2012)
33. Enterococcus faecium 0.0377 mg g-1 – – Bhakta et al. (2012)
Bacillus cereus 0.0460 mg g-1
34. Achromobacter denitrificans PQ-1 55.1% Abyar et al. (2012)
35. Acidiphilium symbioticum H8 248.62 mg g-1 6.0 – Chakravarty and Banerjee (2012)
36. Staphylococcus cohnii GC 83.034 mg g-1 4.0 – Kalkan et al. (2013)
37. Pseudoalteromonas sp. SCSE709-6 96% 5.0 30 °C Zhou et al. (2013)
38. Alteromonas macleodii NR 150 mg L-1 6.0 30 Moselhy et al. (2013)
39. Pantoea sp. RL32.2 89.89% 7.0 35 Abbas et al. (2014b)
Salmonella enteric 82.10% 7.0 35
Enterobacter sp. OCPSB1 89.14% 7.0 35
40. Enterobacter mori 87.75% 7.0 35 Abbas et al. (2015)
Enterobacter sp. WS12 85.11% 7.0 35

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Table 4 continued
S. no. Bacterial strains Cadmium Optimum Optimum References
removal capacity pH temperature (°C)

41. Halomonas BVR 1 12.023 mg g-1 – – Rajesh et al. (2014)


42. Acinetobacter brisouii 95% – – Bhakta et al. (2014)
Pseudomonas abietaniphila 79% – –
Exiguobacterium aestuarii 86% – –
Planococcus Rifietoensis 99% – –
-1
43. Arthrobacter nicotianae IAM12342 492 lmol Cd g Tsuruta et al. (2014)
Bacillus licheniformis IAM11054 282 lmol Cd g-1
Bacillus megaterium IAM1166 334 lmol Cd g-1
Bacillus subtilis IAM1026 292 369 lmol Cd g-1
Bacillus subtilis IAM11060 308 lmol Cd g-1
Bacillus subtilis var niger IAM1633 324 lmol Cd g-1
Brevibacterium helovolum IAM1637 322 lmol Cd g-1
Corynebacterium equi IAM1038 331 lmol Cd g-1
Deinococcus proteolyticus IAM12141 166 lmol Cd g-1
Escherichia coli IAM1264 166 299 lmol Cd g-1
Micrococcus luteus IAM1056 347 lmol Cd g-1
Pseudomonas aureofaciens IAM12353 178 lmol Cd g-1
Pseudomonas maltophilia IAM1554 130 lmol Cd g-1
Pseudomonas putida IAM1506 165 lmol Cd g-1
Nocardia erythropolis IAM1399 84 lmol Cd g-1
44. Pseudomonas mendocina strain E678 99% – – Mathivanan and Rajaram (2014)
45. Bacillus safensis 83.5% – – Priyalaxmi et al. (2014)
46. Enterococcus faecalis 0.3 mmol L-1 – – Wu et al. (2014)
47. Ochrobactrum sp. GDOS 83.33 mg g-1 – – Khadivinia et al. (2014)
48. Bacillus licheniformis 98.34% – – Basha and Rajaganesh (2014)
Salmonella typhi 92.4%
Pseudomonas fluorescence 94.8%
Escherichia coli 92.06%
49. Tsukamurella paurometabola A155 16.89 mg g-1 – – Limcharoensuk et al. (2015)
Pseudomonas aeruginosa B237
Cupriavidus taiwanensis E 324
50. Bacillus catenulatus JB-022 66% – – Kim et al. (2015)
51. Anabaena doliolum Ind1 92% 7.0 – Goswami et al. (2015)
52. Pseudomonas sp. PM2 69.84% – – Sangthong et al. (2015)
53. Desulfovibrio alaskensis 6SR 99.9% – – Pérez et al. (2015)
54. Alteromonas macleodii 53% – – Shaaban et al. (2015)
Nitratireductor basaltis 50% – –
55. Citrobacter sp. JH 11-2 47.7% – – Shim et al. (2015)
56. Pseudomonas aeruginosa JP-11 88.66% – – Raj et al. (2016)

to occur is very high. This system is very suitable for large continuous system needs to be considered (Zhu et al.
amount of substrates, for instance, removal of cadmium 2003). Generally, continuous cultivation can be catego-
from wastewater using cadmium resistance bacteria (Zhu rized into four general types according to the ways in
et al. 2003; Cazón et al. 2013). The microorganism in the which parameters are controlled and also modes of
continuous system has the capability to remove cadmium operation.
greater than batch system (Saeed and Iqbal 2003). How- Types of continuous cultivation are listed as follows:
ever, the process of acclimatization before starting the

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(a) Chemostat: A chemostat is a type of bioreactor in (c) Rotating biological contactor—This type of bioreactor
which to keep the culture volume constant, culture is attached with biofilm disk. This biofilm immobilizes
liquid is continuously removed while fresh medium is with cadmium resistance bacteria. The rotational speed
continuously added. of the disks is maintained as previous researchers
(b) Auxostat: An auxostat is a continuous culture device noticed that speed had not disrupted the biofilm, but
which, while in operation, uses feedback from a encouraged turbulence and it increased the contact of
measurement taken on the growth chamber to control cadmium to the cell (Costley and Wallis 2001).
the media flow rate, maintaining the measurement at a (d) Airlift reactor—The concept of airlift reactor is
constant level. similar to bubble column reactor, but it is equipped
(c) Cells recycle: This is an unsteady state system, in with a draft tube. Airlift reactors are often operated
which the main objective is that the growth equals the with cell immobilized because shear levels are lower
feed rate. than stirred vessels. The resulting fraction of dis-
(d) Multi-stage continuous culture: This system will be tributed cultivation is very low. Cadmium resistance
operated in several vessels and mimic tubular flow bacteria are proved to be cultured using this system as
reactor systems. reported by Filipkowska et al. (2015), but depending
on metal concentration and flow rate.
Advance bioreactors
Cells recycle system
In order to further improve the bioreactor system and avoid
disadvantages in the batch and continuous operation, It is possible for enhancement of reactor performance over
advance bioreactor will be applied. classic continuous culture if cells were retained in the
reactor system. Cells retained in the reactor by sedimen-
Immobilized cell reactor tation give highly cell concentrations that result in high
volumetric catalytic power leading to high productivity.
In this type of reactor, three methods could be applied to This allows high flow rate through the system well above
immobilize the cells such as covalent bond formation, that for cells in the conventional continuous system. This
entrapment and biofilm (Qureshi et al. 2005). All of these type of enhancement exploits common behavior in natural
methods are applied in different reactors. The types of environments to form rapidly settling flocks that are found
immobilized cell reactor include: in fresh and sea water environments. Membrane bioreactor
(MBR) concept for this reactor is to retain cadmium
(a) Fluidized bed reactors—This type of reactor operates
resistance cells in the reactor by filtration. There are two
with an upward flow of liquid. It is simpler than the
types of basic design in these systems depending on posi-
packed bed reactor. Fluidized bed reactors are often
tions of the membrane. The first type uses membranes
used in waste treatment with sand or other suit-
which filter the water by suction through the membrane
able carrier material which supports the mixed
surface removing clarified water while retaining the par-
microbial populations inside the fluidized bed. Other
ticulates. This type of system is commonly used in waste
application for this type of reactor includes the
treatment as a replacement for activated sludge processes
commercial production of vinegar. In this process, a
or flocculation processes where filtration replaces sedi-
flocculating organism is applied. Sulaymon et al.
mentation for retaining biomass within the reactor. The
(2013) selected this type of bioreactor in their study
second type of MBR filters pressurized water to force water
for cadmium removal using cadmium resistance
out of the system. These systems are easier for engineer
microorganism.
especially when sterile environments are required and
(b) Packed back reactors—This type of reactor is
systems run under positive pressure. They are often used in
commercially used with immobilized cells. Normally,
reactors with pure cultures. MBR systems have many
the substrate with a high amount of cadmium
advantages over continuous culture or reactors with cell
(continuous liquid flow) will feed through a packed
recycle relying on sedimentation, whereby cell retention is
bed tube either at the bottom or at top of the reactor
controlled by a physical separation and generically applied
tube. Inside, the packed bed is attached with catalyst
to all types of cells to produce high cell concentrations in
particles (cell). The advantage of using this reactor is
the reactor and allow high cadmium removal. The rate of
that the damage to the cells is lower than in a
cadmium uptake by cells in the membrane bioreactor sys-
comparable common bioreactor. Saeed and Iqbal
tem will be increased by supplying high aeration (Mah-
(2003) proved that this bioreactor is suitable for
moudkhani et al. 2014).
cadmium resistance bacteria.

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Specific bacterial bioreporters and bioavailability

The whole-cell microbial biosensors or bacterial biore-


porters are living microbes that produce a precise, signifi-
cant output in response to target chemicals. They give a
biological mean for measuring bioaccessibility or
bioavailability. Comparing chemical analysis methods
which detect whole contaminants in the sample, bacterial
bioreporters only detect the target heavy metals which
influence the cell and easily pass through cell membrane
(Garg and Mehrotra 2017). The bioavailability assays
predict real risk assessment, valuable organisms exposure
to pollutants and selection of suitable remediation choices.
For example, in the case of heavy metals bacterial biore- Fig. 3 A simplest working principle of luminescent bacterial biore-
porter. The metal flux through the cell determines by metal efflux and
porters only detect the metals speciation instead of whole metal uptake mechanisms. The transcription of the reporter element is
heavy metals concentration. This discrepancy is very initiated by binding of metal ions to sensor, and a significant signal is
helpful for detecting those pollutants with poor aqueous produced. The intracellular metal ions concentration correlates with
solubility or low dissociation constants. signal output in a certain concentration
The genetically engineered bacteria are specific biore-
porters where a sensor element that is responsible for contaminated sites. However, to put it into field, many
pollutant detection has been fused with reporter element as economic, environmental, technological and social
shown in Fig. 3. The sensor element normally contains a boundaries are yet to be conquered.
gene with transcription factor and its cognate promoter,
whereas the reporter element consists of a gene or group of Genetically engineered bacteria
gene that code for an easily measurable signal. Such sys-
tems are highly regulated by the presence of certain com- The application of the cadmium is increasing day by day in
pound like heavy metal resistance operons. In this system, industries, and this creates the awareness about its eco-
the presence of the protein is measured by fluorescence and logical effects, accumulation and cadmium toxicity. The
enzymatic activity quantified by substrate-degrading pro- metal binding proteins like metallothioneins and phy-
teins (Bereza-Malcolm et al. 2016). tochelatins have been characterized in metal-resistant
Conventionally, whole-cell bioreporters are only appli- bacteria, and these proteins show high capabilities of
cable on soil and water samples. But recently bacterial binding with heavy metals, especially cadmium (Singh
bioreporters proved that it can be useful for detecting the et al. 2011). Recently, the genes that code metallothioneins
As in drinking water in the developing countries and also and phytochelatins have cloned from fungi and plants,
availability of Fe for cyanobacteria in lake and sea water inserted functionally into E. coli. The E. coli showed both
samples. More novel application of bacterial bioreporters is high affinity and bioaccumulation of target metal ions,
to detect the Hg in urine and As contents in rice. Biore- especially cadmium from multi-component pollutants
porters do not yet participate to find contaminated site (Khan et al. 2015).
management because these bioreporters are still between So the investigation of removal of environmental toxi-
real environmental application and proof-of-principle cants by using genetically engineered bacteria gives a new
phase. era of remediation. The introduction of cadmium resistance
genes inside the aquatic plants also is increasing day by day
because natural hyperaccumulators are not competent
because they are low biomass production and slow grow-
ing. So by using this cell engineering technology (somatic
Future perspectives hybridization and cell fusion) cadmium-resistant genes
from bacteria can be inserted into polyploid aquatic plants
With the many confront advantages and the recent inter- because they are active more in transpiration and bigger in
esting progresses, bioremediation is showing itself as a size. Another future direction is the insertion of cadmium-
promising technique to raise cadmium removal from resistant symbiotic bacteria into the nodules of aquatic

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Int. J. Environ. Sci. Technol.

plants. However, the majority of studies of metals removal the reduction of cadmium(II). The researchers have suc-
by genetically engineered bacteria have been experimented cessfully explained cadmium(II) reduction in a microbial
under laboratory parameters. It is very tough to determine fuel cell chromium(VI) microbial electrolysis cells cad-
the metals removal from contaminated sites by genetically mium(II) system without any extra energy input.
engineered bacteria due to many factors. For example, the There are many factors which limit the practical appli-
genetically engineered bacteria have very less survival in cation of the bioelectrical system. So there is a need to
natural environments due to the introduction of foreign minimize these factors to make the efficient functioning of
genes and environmental stress conditions. Another the bioelectrical system. For example, in the domestic
important factor is that for getting the nutrients and other wastewater the concentration of metals was normally in the
resources there is the competition between naturally lg mL-1 range. The concentration of metals should be
occurring bacteria with genetically engineered bacteria. high especially when bioelectrical systems are used for the
Therefore, future research would be more targeted on treatment of industrial wastewater, process streams and
minimizing these factors and other factors which improve meta-metallurgical wastes. For the recovery and removal of
the in situ bioremediation by genetically engineered bac- metal ions, the both cathode and anode chambers should be
teria. Regardless of the advantages and disadvantages of separately fed with aqueous solution containing metals and
bioremediation technology, for the bioremediation of organics. This approach may help to avoid bioanode
contaminated sites the application of native genetically microbial community from the toxic effects of metal ions.
engineered bacteria may be given a ray of hope for the There is also need to run the bioelectrical system for a long
fruitful application of bioremediation technology. The slow time to understand how the metal ions enter into anode
progress in field application of genetically engineered chamber? And what is their effect on bioanode perfor-
bacteria is due to the mostly low public acceptability and mance? Besides, there is also need of understanding how
possible risks. In the future, the application of native metals ions and electrodes materials have influence on the
genetically engineered bacteria may be helpful in public functions and structure of microbial community? So more
appreciation. research is required to understand the strategies for the
recovery of selective metal. Finally, there is much need to
Bioelectrochemical systems direct the research toward leaching, recovery of selective
metal from real industrial wastewater and combination of
For the removal of metals by microorganisms, the mech- the bioelectrical system with hydrometallurgy.
anisms are not limited to bioreduction, bioabsorption,
biomineralization and bioaccumulation. The conversion of Microbial aggregates
certain metalloids and radionuclides by microorganisms is
also a useful bioremediation way for metals removal from With the advancement of human’s lives, the composition of
contaminated wastewater and waters (Francis and Nan- water and wastewater becomes more complex due to its
charaiah 2015). However, in the literature, the bioelectro- mixing with downstream surface waters and nonpoint-
chemical systems show both microbial fuel cells and source wastewater (Wu et al. 2011). Many methods have
microbial electrolysis cells. These methods have appeared been used to treat surface waters and nonpoint-source
as promising tools for bioremediation because these wastewater, but there are not too much effective due to
methods not only deal with organic wastewater treatment, many limitations. (1) The heterogeneous nature of surface
but also offer possible metals recovery. The microbial waters and nonpoint-source wastewater than domestic and
electrolysis cells and microbial fuel cells are extensively industrial waste water. (2) The method based on activated
used in both basic and applied research for harnessing the sludge needs the maturation phase, i.e., active sludge to be
energy and remediation of contaminated sites (Elmekawy established. (3) For the removal of particular metal,
et al. 2015). The external electrodes (cathode, anode) acclimation of microorganisms is required because
linked the microbial metabolism by acting as electrons microorganisms inoculated in the different environment
donor and acceptor, which cause the development of need some time to acclimatize with new conditions, and
potential difference leading to bioelectrogenic activity maybe during this time animals and humans expose to
(Abbas et al. 2017). Nancharaiah et al. (2015) find out these toxins. (4) Using photosynthetic microorganisms
standard redox potential of cadmium(II)/cadmium (0) needs energy investment for the efficient illumination (Wu
couple is -0.40 V. The external voltage was supplied for et al. 2012). So the removal of multiple pollutants

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Int. J. Environ. Sci. Technol.

simultaneously microbial aggregates may be possible bioremediation, one should also consider the risk assess-
future suggested study. ment by these transgenic forms into the environment.
Microbial aggregates composed of complex microbial A complete biochemical characterization of microbial
consortia of bacteria, algae and other micro- and macro- substrate and its environmental advantages will be com-
organisms that formed on the solid substrate in aquatic pulsory to credibly point out the benefits of algal
environments (Wu et al. 2010). The microbial aggregates biosorption over conventional routine chemical treatment
remove the multiple pollutants through many mechanisms and ion-exchange resins. Further research at both labora-
and at the same time include biodegradation, ion exchange, tory and industrial scales will help to optimize the final
complexation, assimilation, adsorption, precipitation, pre- cadmium biosorption to improve economic sustainability
dation and flocculation. According to the above-mentioned practicalities of large-scale applications of algal cadmium
literature review, we can highlight that the microbial bioremediation. In order to apply the algal biosorption
treatment method is easily accessible, flexible, rapid, sen- technology on large scale require the better understandings
sitive, easily applicable and inexpensive than conventional of influential factors like physicochemical conditions, the
treatment methods. However, microbial aggregates treat- initial concentration and contact times. The successful
ment method is limited because microbial aggregates can algal biosorption may require the inexpensive biomaterials
remove only certain type of pollutants. So for the removal show high cadmium uptake as well as posses suitable me-
of contaminants from real-world aqueous solution, there is chanical properties for applied remediation approaches.
need to develop the complex microbial aggregates that will The algal biosorption technique may be an attractive
be a focal point in future research. Another future study because it produces the high biomass of wastewater grown
area is to understand the nature of complex microbial algae coupled with hybrid production system. The techno-
strains (microbial aggregates). economic analysis, lifecycle assessment and energy cost
could be precisely determined prior to large-scale
Biosorption of cadmium by algae implementation.

High cadmium ion uptake, low-cost cultivation, selectivity


of cadmium and special mechanical properties of algae Conclusion
make it possibly suitable for cadmium remediation. For
detoxification and recovery of cadmium, using metabolic There is no proper balance between natural and human
active immobilized microalgae may be attractive future exploitation of cadmium, so alternative ways of cadmium
option. There is more need to investigate the pros and cons removal from wastewater came into existence. Cadmium
of using immobilized microalgae. In future to enhance the bioremediation has got much attraction because they are
cadmium specificity and binding of microalgae, transgenic economical, safe and eco-friendly. In order to apply at
technique may be developed with an objective to use industrial scale, it needs to get a basic knowledge of
microalgae for cadmium treatment especially in sediments bioremediation and develop the most efficient and copious
and wastewater. These approaches will encompass the research in the laboratory, bench scale, pilot studies and
overexpression of enzymes whose metabolic products may in situ studies. The addition of genetic engineering, bio-
alleviate the effects of cadmium-binding protein on the electrochemical system, microbial aggregates and
surface, cadmium-induced stress and in cytoplasm of biosorption of cadmium by algae in the bioremediation will
transgenic microalgae cells (Zeraatkar et al. 2016). How- lead this technology in more modern ways. In these tech-
ever, in order to avert the good cadmium remediation niques, the bacteria are central machinery so many pre-
capacities with these transgenic algae, it is necessary to cautions should be taken for cadmium-resistant bacteria
have clear biological and engineering considerations. The because these cadmium-resistant bacteria are also resistant
transportation of these live transgenic microalgae into the to antibiotics. The antibiotic resistance of bacteria has got
environment could accumulate in the food chains through serious issues at international level. Soon cadmium-resis-
biogeochemical cycling of cadmium, which could be tant genes should be transferred from mutated bacteria into
potentially toxic (Kumar et al. 2015); thus, the non-viable normal bacterial flora in the laboratory and these bacteria
transgenic microalgae with significant binding and selec- can be used for wastewater treatment in a closed system,
tivity would be alternative strategy. Thus, even though and after that this water should be released into rivers and
there is high market of these transgenic cells for lakes so the evolution of non-antibiotic-resistant bacteria

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will be in progress in the environment and antibiotic-re- Australia’s submission (2005) Information about cadmium in
sistant bacteria slowly eradicate. Every technology has its Australia. Prepared by the Australian Government for the
United Nations Environment Programme. Australia Govern-
own advantages and disadvantages which depend upon ment, 12
how we use this technology for benefits. Characterizing Bai H-J, Zhang Z-M, Yang G-E, Li B-Z (2008) Bioremediation of
cadmium removal pathways, marking the enzymes and cadmium by growing Rhodobacter sphaeroides: kinetic charac-
genes involved in cadmium resistance exhibit fields for teristic and mechanism studies. Bioresour Technol
99:7716–7722
further research. Basha SA, Rajaganesh K (2014) Microbial bioremediation of heavy
metals from textile industry dye effluents using isolated bacterial
Acknowledgements The authors would like to express their appre- strains. Int J Curr Microbiol Appl Sci 3:785–794
ciation to Universiti Sains Malaysia Global Fellowship (USMGF/FC/ Bereza-Malcolm L, Aracic S, Franks AE (2016) Development and
04/2015) for the support and research facilities for this project. application of a synthetically-derived lead biosensor construct
for use in gram-negative bacteria. Sensors 16:2174. doi:10.3390/
Compliance with ethical standards s16122174
Bhakta J, Munekage Y, Ohnishi K, Jana B (2012) Isolation and
Conflict of interest The authors declare that they do not have any identification of cadmium-and lead-resistant lactic acid bacteria
conflict of interest. for application as metal removing probiotic. Int J Environ Sci
Technol 9:433–440
Bhakta JN, Munekage Y, Ohnishi K, Jana B, Balcazar J (2014)
Isolation and characterization of cadmium-and arsenic-absorbing
References bacteria for bioremediation. Water Air Soil Pollut 225:1–10
Boopathy R (2000) Factors limiting bioremediation technologies.
Abbas SZ, Rafatullah M, Ismail N, Lalung J (2014a) Isolation, Bioresour Technol 74:63–67
identification, and characterization of cadmium resistant Pseu- Bramhachari P, Nagaraju GP (2017) Extracellular polysaccharide
domonas sp. M3 from industrial wastewater. J Waste Manag production by bacteria as a mechanism of toxic heavy metal
2014:1–6 biosorption and biosequestration in the marine environment. In:
Abbas SZ, Rafatullah M, Ismail N, Lalung J (2014b) Isolation, Marine pollution and microbial remediation. Springer, Berlin,
identification, characterization, and evaluation of cadmium pp 67–85
removal capacity of Enterobacter species. J Basic Microbiol Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to
54:1279–1287 metals in the environment. Ecotoxicol Environ Saf 45:198–207
Abbas SZ, Riaz M, Ramzan N, Zahid MT, Shakoori FR, Rafatullah M Burkina Faso’s submission (2005) Contribution of Burkina Faso to
(2014c) Isolation and characterization of arsenic resistant the study on lead and cadmium. Semče Idrissa, Ministry of
bacteria from wastewater. Braz J Microbiol 45:1309–1315 Environment and Life Quality
Abbas SZ, Rafatullah M, Ismail N, Lalung J (2015) Isolation and Cazón JP, Viera M, Donati E, Guibal E (2013) Zinc and cadmium
characterization of Cd-resistant bacteria from industrial wastew- removal by biosorption on Undaria pinnatifida in batch and
ater. Desalin Water Treat 56:1037–1046 continuous processes. J Environ Manag 129:423–434
Abbas SZ, Rafatullah M, Ismail N, Syakir MI (2017) A review on Chakravarty R, Banerjee PC (2012) Mechanism of cadmium binding
sediment microbial fuel cells as a new source of sustainable on the cell wall of an acidophilic bacterium. Bioresour Technol
energy and heavy metal remediation: mechanisms and future 108:176–183
prospective. Int J Energy Res. doi:10.1002/er.3706 Chen L, Mathema B, Chavda KD, DeLeo FR, Bonomo RA,
Abd-Alla MH, Morsy FM, El-Enany A-WE, Ohyama T (2012) Kreiswirth BN (2014) Carbapenemase-producing Klebsiella
Isolation and characterization of a heavy-metal-resistant isolate pneumoniae: molecular and genetic decoding. Trends Microbiol
of Rhizobium leguminosarum bv. viciae potentially applicable 22:686–696
for biosorption of Cd2? and Co2?. Int Biodeterior Biodegrad Chen M, Li Y, Zhang L, Wang J, Zheng C, Zhang X (2015) Analysis
67:48–55 of gene expression provides insights into the mechanism of
Abyar H, Safahieh A, Zolgharnein H, Zamani I (2012) Isolation and cadmium tolerance in Acidithiobacillus ferrooxidans. Curr
identification of Achromobacter denitrificans and evaluation of Microbiol 70:290–297
its capacity in cadmium removal. Pol J Environ Stud Chien CC, Hung CW, Han CT (2007) Removal of cadmium ions
21:1523–1527 during stationary growth phase by an extremely cadmium-
Adriano DC (2013) Trace elements in the terrestrial environment. resistant strain of Stenotrophomonas sp. Environ Toxicol Chem
Springer, Berlin 26:664–668
Ali N, Hameed A, Ahmed S (2009) Physicochemical characterization Chovanová K et al (2004) Identification and characterization of eight
and bioremediation perspective of textile effluent, dyes and cadmium resistant bacterial isolates from a cadmium-contami-
metals by indigenous bacteria. J Hazard Mater 164:322–328 nated sewage sludge. Biologia 59:817–827
Alnaseri H, Arsic B, Schneider JE, Kaiser JC, Scinocca ZC, Heinrichs Coelho LM, Rezende HC, Coelho LM, de Sousa PA, Melo DF,
DE, McGavin MJ (2015) Inducible expression of a resistance- Coelho NM (2015) Bioremediation of polluted waters using
nodulation-division-type efflux pump in Staphylococcus aureus microorganisms. In: N Shiomi (ed) Agricultural and biological
provides resistance to linoleic and arachidonic acids. J Bacteriol sciences. Advances in bioremediation of wastewater and
197:1893–1905 polluted soil
Andersen JL et al (2015) Multidrug efflux pumps from Enterobac- Costa SS, Mourato C, Viveiros M, Melo-Cristino J, Amaral L, Couto
teriaceae, Vibrio cholerae and Staphylococcus aureus bacterial I (2013) Description of plasmid pSM52, harbouring the gene for
food pathogens. Int J Environ Res Public Health 12:1487–1547 the Smr efflux pump, and its involvement in resistance to

123
Int. J. Environ. Sci. Technol.

biocides in a meticillin-resistant Staphylococcus aureus strain. Herzberg M, Bauer L, Kirsten A, Nies DH (2016) Interplay between
Int J Antimicrob Agents 41:490–492 seven secondary metal uptake systems is required for full metal
Costley S, Wallis F (2001) Bioremediation of heavy metals in a resistance of Cupriavidus metallidurans. Metallomics. doi:10.
synthetic wastewater using a rotating biological contactor. Water 1039/C5MT00295H
Res 35:3715–3723 Huang F, Guo C-L, Lu G-N, Yi X-Y, Zhu L-D, Dang Z (2014)
Darwish AM, Eisa WH, Shabaka AA, Talaat MH (2016) Investigation Bioaccumulation characterization of cadmium by growing
of factors affecting the synthesis of nano-cadmium sulfide by Bacillus cereus RC-1 and its mechanism. Chemosphere
pulsed laser ablation in liquid environment. Spectrochim Acta A 109:134–142
Mol Biomol Spectrosc 153:315–320 Islam F, Yasmeen T, Riaz M, Arif MS, Ali S, Raza SH (2014)
De J, Sarkar A, Ramaiah N (2006) Bioremediation of toxic substances Proteus mirabilis alleviates zinc toxicity by preventing
by mercury resistant marine bacteria. Ecotoxicology 15:385–389 oxidative stress in maize (Zea mays) plants. Ecotoxicol
Deng X, Yi X, Liu G (2007) Cadmium removal from aqueous Environ Saf 110:143–152
solution by gene-modified Escherichia coli JM109. J Hazard Jang S (2016) Multidrug efflux pumps in Staphylococcus aureus and
Mater 139:340–344 their clinical implications. J Microbiol 54:1–8
Divya B, Kumar MD (2011) Plant–microbe interaction with enhanced Kalkan E, Nadaroglu H, Dikbas N, Tasgin E, Çelebi N (2013)
bioremediation research. J Biotechnol 6:72–79 Bacteria-modified red mud for adsorption of cadmium ions from
Dixit R et al (2015) Bioremediation of heavy metals from soil and aqueous solutions. Pol J Environ Stud 22:105–117
aquatic environment: an overview of principles and criteria of Kermani AJN, Ghasemi MF, Khosravan A, Farahmand A, Shakibaie
fundamental processes. Sustainability 7:2189–2212 M (2010) Cadmium bioremediation by metal-resistant mutated
Du H, Chen W, Cai P, Rong X, Dai K, Peacock CL, Huang Q (2016) bacteria isolated from active sludge of industrial effluent. Iranian
Cd(II) sorption on montmorillonite-humic acid-bacteria com- J Environ Health Sci Eng 7:279–286
posites. Sci Rep 6:19499 Kesler S, Simon A (2015) Mineral resources, economics and the
El-Helow E, Sabry S, Amer R (2000) Cadmium biosorption by a environment. Cambridge University Press, Cambridge
cadmium resistant strain of Bacillus thuringiensis: regulation and Khadivinia E, Sharafi H, Hadi F, Zahiri HS, Modiri S, Tohidi A
optimization of cell surface affinity for metal cations. Biometals (2014) Cadmium biosorption by a glyphosate-degrading bac-
13:273–280 terium, a novel biosorbent isolated from pesticide-contaminated
ElMekawy A, Srikanth S, Bajracharya S, Hegab HM, Nigam PS, Singh agricultural soils. J Ind Eng Chem 20:4304–4310
A (2015) Food and agricultural wastes as substrates for bioelec- Khan Z, Nisar MA, Hussain SZ, Arshad MN, Rehman A (2015)
trochemical system (BES): the synchronized recovery of sustain- Cadmium resistance mechanism in Escherichia coli P4 and its
able energy and waste treatment. Food Res Int 73:213–225 potential use to bioremediate environmental cadmium. Appl
Filice FP, Li MS, Henderson JD, Ding Z (2016) Mapping Cd2?- Microbiol Biotechnol 99:10745–10757
induced membrane permeability changes of single live cells by Kim SY, Jin MR, Chung CH, Yun Y-S, Jahng KY, Yu K-Y (2015)
means of scanning electrochemical microscopy. Anal Chim Biosorption of cationic basic dye and cadmium by the novel
Acta. doi:10.1016/j.aca.2015.12.027 biosorbent Bacillus catenulatus JB-022 strain. J Biosci Bioeng
Filipič M (2012) Mechanisms of cadmium induced genomic insta- 119:433–439
bility. Mutat Res Fundam Mol Mech 733:69–77 Kumar KS, Dahms H-U, Won E-J, Lee J-S, Shin K-H (2015)
Filipkowska U, Szymczyk P, Kuczajowska-Zadro_zna M, Jóźwiak T Microalgae—a promising tool for heavy metal remediation.
(2015) Effect of conditions of air-lift type reactor work on Ecotoxicol Environ Saf 113:329–352
cadmium adsorption. Korean J Chem Eng 32:2024–2030 Lewis VG, Ween MP, McDevitt CA (2012) The role of ATP-binding
Francis A, Nancharaiah Y (2015) In situ and ex situ bioremediation of cassette transporters in bacterial pathogenicity. Protoplasma
radionuclide-contaminated soils at nuclear and NORM sites. In: 249:919–942
Environmental remediation and restoration of contaminated Li Z, Yuan H (2006) Characterization of cadmium removal by
nuclear and norm sites, p 185 Rhodotorula sp. Y11. Appl Microbiol Biotechnol 73:
Garg M, Mehrotra S (2017) Biosensors. In: Principles and applica- 458–463
tions of environmental biotechnology for a sustainable future. Limcharoensuk T, Sooksawat N, Sumarnrote A, Awutpet T, Krua-
Springer, Berlin, pp 341–363 trachue M, Pokethitiyook P, Auesukaree C (2015) Bioaccumu-
Gaur N, Flora G, Yadav M, Tiwari A (2014) A review with recent lation and biosorption of Cd2? and Zn2? by bacteria isolated
advancements on bioremediation-based abolition of heavy from a zinc mine in Thailand. Ecotoxicol Environ Saf
metals. Environ Sci Process Impacts 16:180–193 122:322–330
Glazer A, Nikaido H (1995) Environmental applications microbial Lu W-B, Shi J-J, Wang C-H, Chang J-S (2006) Biosorption of lead,
biotechnology: fundamentals of applied microbiology. WH copper and cadmium by an indigenous isolate Enterobacter sp.
Freeman and Company, New York, pp 561–614 J1 possessing high heavy-metal resistance. J Hazard Mater
Goswami S, Syiem MB, Pakshirajan K (2015) Cadmium removal by 134:80–86
Anabaena doliolum Ind1 isolated from a coal mining area in Luo S, Xiao X, Xi Q, Wan Y, Chen L, Zeng G, Chen J (2011)
Meghalaya, India: associated structural and physiological alter- Enhancement of cadmium bioremediation by endophytic bac-
ations. Environ Eng Res 20:41–50 terium Bacillus sp. L14 using industrially used metabolic
Green-Ruiz C, Rodriguez-Tirado V, Gomez-Gil B (2008) Cadmium inhibitors (DCC or DNP). J Hazard Mater 190:1079–1082
and zinc removal from aqueous solutions by Bacillus jeotgali: Mahmoudkhani R, Torabian A, Hassani AH, Mahmoudkhani R
pH, salinity and temperature effects. Bioresour Technol (2014) Copper, cadmium and ferrous removal by membrane
99:3864–3870 bioreactor. APCBEE Procedia 10:79–83
Guo S, Yao Y, Zuo L, Shi W, Gao N, Xu H (2016) Enhancement of Mahvi A, Diels L (2004) Biological removal of cadmium by
tolerance of Ganoderma lucidum to cadmium by nitric oxide. Alcaligenes eutrophus CH34. Int J Environ Sci Technol
J Basic Microbiol 56:36–43 1:199–204

123
Int. J. Environ. Sci. Technol.

Malakahmad A, Hasani A, Eisakhani M, Isa MH (2011) Sequencing NFA (2002): Riskiraportti: Elintarvikkeiden ja talousveden kemial-
Batch Reactor (SBR) for the removal of Hg2? and Cd2? from liset vaarat. [Risk Report: chemical hazards of food and drinking
synthetic petrochemical factory wastewater. J Hazard Mater water]. National Food Agency, Valvontaopas-sarja 2/2002,
191:118–125 Helsinki, Finland (in Finnish)
Malekzadeh R, Shahpiri A (2017) Independent metal-thiolate cluster Nriagu JO (1989) A global assessment of natural sources of
formation in C-terminal Cys-rich region of a rice type 1 atmospheric trace metals. Nature 338:47–49
metallothionein isoform. Int J Biol Macromol 96:436–441 Ozdemir G, Ceyhan N, Ozturk T, Akirmak F, Cosar T (2004)
Martin R, Dowling K, Pearce D, Sillitoe J, Florentine S (2014) Health Biosorption of chromium(VI), cadmium(II) and copper(II) by
effects associated with inhalation of airborne arsenic arising Pantoea sp. TEM18. Chem Eng J 102:249–253
from mining operations. Geosciences 4:128–175 Özdemir S, Kilinc E, Nicolaus B, Poli A (2013) Resistance and
Masoudzadeh N, Zakeri F, Bagheri LT, Sharafi H, Masoomi F, Zahiri bioaccumulation of Cd2?, Cu2?, Co2? and Mn2? by ther-
HS et al (2011) Biosorption of cadmium by Brevundimonas sp. mophilic bacteria, Geobacillus thermantarcticus and Anoxy-
ZF12 strain, a novel biosorbent isolated from hot-spring waters bacillus amylolyticus. Ann Microbiol 63:1379–1385
in high background radiation areas. J Hazard Mater 197:190–198 Pandey S, Saha P, Barai PK, Maiti TK (2010) Characterization of a
Massadeh AM, Al-Momani FA, Haddad HI (2005) Removal of lead Cd2?-resistant strain of Ochrobactrum sp. isolated from slag
and cadmium by halophilic bacteria isolated from the Dead Sea disposal site of an iron and steel factory. Curr Microbiol
shore, Jordan. Biol Trace Elem Res 108:259–269 61:106–111
Mathivanan K, Rajaram R (2014) Tolerance and biosorption of Pardo R, Herguedas M, Barrado E, Vega M (2003) Biosorption of
cadmium(II) ions by highly cadmium resistant bacteria isolated cadmium, copper, lead and zinc by inactive biomass of
from industrially polluted estuarine environment. Indian J Pseudomonas putida. Anal Bioanal Chem 376:26–32
Geomarine Sci 43:580–588 Patel J, Zhang Q, McKay RML, Vincent R, Xu Z (2010) Genetic
Medircio SN, Leao VA, Teixeira MC (2007) Specific growth rate of engineering of Caulobacter crescentus for removal of cadmium
sulfate reducing bacteria in the presence of manganese and from water. Appl Biochem Biotechnol 160:232–243
cadmium. J Hazard Mater 143:593–596 Pavić A, Ilić-Tomić T, Pačevski A, Nedeljković T, Vasiljević B,
Mexico’s submission (2005) Information on sources of exposure to Morić I (2015) Diversity and biodeteriorative potential of
lead and cadmium in Mexico. Federal Commission for the bacterial isolates from deteriorated modern combined-technique
Protection against Sanitary Risk. Health protection canvas painting. Int Biodeterior Biodegrad 97:40–50
Moberly JG, Staven A, Sani RK, Peyton BM (2010) Influence of pH Pérez PL, López RA, González MN (2015) Cadmium removal at
and inorganic phosphate on toxicity of zinc to Arthrobacter sp. high concentration in aqueous medium: mediated by Desul-
isolated from heavy-metal-contaminated sediments. Environ fovibrio alaskensis International. J Environ Sci Technol
Science Technol 44:7302–7308 12:1975–1986
Monachese M, Burton JP, Reid G (2012) Bioremediation and Priyalaxmi R, Murugan A, Raja P, Raj KD (2014) Bioremediation of
tolerance of humans to heavy metals through microbial pro- cadmium by Bacillus safensis (JX126862), a marine bacterium
cesses: a potential role for probiotics? Appl Environ Microbiol isolated from mangrove sediments. Int J Curr Microbiol Appl Sci
78:6397–6404 3:326–335
Mori T, Iwamoto K, Wakaoji S, Araie H, Kohara Y, Okamura Y et al Qureshi N, Annous BA, Ezeji TC, Karcher P, Maddox IS (2005)
(2016) Characterization of a novel gene involved in cadmium Biofilm reactors for industrial bioconversion processes: employ-
accumulation screened from sponge-associated bacterial meta- ing potential of enhanced reaction rates. Microb Cell Fact 4:1
genome. Gene 576:618–625 Raj R, Dalei K, Chakraborty J, Das S (2016) Extracellular polymeric
Moselhy K, Shaaban MT, Ibrahim HA, Abdel-Mongy AS (2013) substances of a marine bacterium mediated synthesis of CdS
Biosorption of cadmium by the multiple-metal resistant marine nanoparticles for removal of cadmium from aqueous solution.
bacterium Alteromonas macleodii ASC1 isolated from Hurghada J Colloid Interface Sci 462:166–175
harbour, Red Sea. Arch Sci 66:259–272 Rajesh V, Kumar ASK, Rajesh N (2014) Biosorption of cadmium
Mota R, Pereira SB, Meazzini M, Fernandes R, Santos A, Evans CA using a novel bacterium isolated from an electronic industry
(2015) Effects of heavy metals on Cyanothece sp. CCY 0110 effluent. Chem Eng J 235:176–185
growth, extracellular polymeric substances (EPS) production, Richardson GM, Garrett R, Mitchell I, Mah-Poulson M, Hackbarth T
ultrastructure and protein profiles. J Proteomics 120:75–94 (2001) Critical review on natural global and regional emissions
Mustapha MU, Halimoon N (2015) Screening and isolation of heavy of six trace metals to the atmosphere. Prepared for the
metal tolerant bacteria in industrial effluent. Procedia Environ International Lead Zinc Research Organisation, the International
Sci 30:33–37 Copper Association, and the Nickel Producers Environmental
Naik MM, Dubey S (2017) Lead-and mercury-resistant marine Research Association
bacteria and their application in lead and mercury bioremedia- Sabdono A (2011) Cadmium removal by a bioreducpiun coral
tion. In: Marine pollution and microbial remediation. Springer, bacterium Pseudoalteromonas sp. strain cd15 isolated from the
Berlin, pp 29–40 tissue of coral Goniastrea aspera, Jepara waters. J Coast Dev
Nancharaiah Y, Mohan SV, Lens P (2015) Metals removal and 13:81–91
recovery in bioelectrochemical systems: a review. Bioresour Sachdev DP, Cameotra SS (2013) Biosurfactants in agriculture. Appl
Technol 195:102–114 Microbiol Biotechnol 97:1005–1016
Narayani M, Shetty KV (2013) Chromium-resistant bacteria and their Saeed A, Iqbal M (2003) Bioremoval of cadmium from aqueous
environmental condition for hexavalent chromium removal: a solution by black gram husk (Cicer arientinum). Water Res
review. Crit Rev Environ Sci Technol 43:955–1009 37:3472–3480

123
Int. J. Environ. Sci. Technol.

Sangthong C, Duangboobpha S, Prapagdee B (2015) Cadmium natural carbohydrate biopolymer. Indian J Biotechnol
removal from water and soil by a cadmium-resistant Rhizobac- 10:113–120
terium and its effect on plant root elongation. Environ Asia Vipra A, Desai SN, Junjappa RP, Roy P, Poonacha N, Ravinder P,
8:94–100 Sriram B, Padmanabhan S (2013) Determining the minimum
Sarin C, Sarin S (2010) Removal of cadmium and zinc from soil using inhibitory concentration of bacteriophages: potential advantages.
immobilized cell of biosurfactant producing bacteria. Environ Adv Microbiol 3:181–190
Asia 3:49–53 Vullo DL, Ceretti HM, Daniel MA, Ramı́rez SA, Zalts A (2008)
Schindler BD, Frempong-Manso E, DeMarco CE, Kosmidis C, Matta Cadmium, zinc and copper biosorption mediated by Pseu-
V, Seo SM, Kaatz GW (2015) Analyses of multidrug efflux domonas veronii 2E. Bioresour Technol 99:5574–5581
pump-like proteins encoded on the Staphylococcus aureus Wang X, Jin B (2009) Process optimization of biological hydrogen
chromosome. Antimicrob Agents Chemother 59:747–748 production from molasses by a newly isolated Clostridium
Shaaban MT, Ibrahim HA, Abouhend AS, El-Moselhy KM (2015) butyricum W5. J Biosci Bioeng 107:138–144
Removal of heavy metals from aqueous solutions using multi- Wassenaar T, Ussery D, Nielsen L, Ingmer H (2015) Review and
metals and antibiotics resistant bacterium isolated from the Red phylogenetic analysis of qac genes that reduce susceptibility to
Sea, Egypt. Am J Microbiol Res 3:93–106 quaternary ammonium compounds in Staphylococcus species.
Shamim S, Rehman A (2015) Antioxidative enzyme profiling and Eur J Microbiol Immunol 5:44–61
biosorption ability of Cupriavidus metallidurans CH34 and Wheaton G, Counts J, Mukherjee A, Kruh J, Kelly R (2015) The
Pseudomonas putida mt2 under cadmium stress. J Basic Micro- confluence of heavy metal biooxidation and heavy metal
biol 55:374–381 resistance: implications for bioleaching by extreme thermoaci-
Shim J, Kim J-W, Shea PJ, Oh B-T (2015) Biosorption of cadmium dophiles. Minerals 5:397–451
by Citrobacter sp. JH 11-2 isolated from mining site soil. Sep WHO (2004) Cadmium (addendum). WHO Food Additives Series:
Sci Technol 50(14):2134–2141 52. First draft. World Health Organisation, Geneva,
Shirdam R, Khanafari A, Tabatabaee A (2006) Cadmium, nickel and Switzerland
vanadium accumulation by three strains of marine bacteria. Iran WHO and UNICEF (2015) Progress on drinking water and
J Biotechnol 4:180–187 sanitation-2014 update. 20 Avenue Appia, 1211 Geneva 27,
Singh N, Gadi R (2012) Bioremediation of Ni(II) and Cu(II) from Switzerland
wastewater by the nonliving biomass of Brevundimonas vesic- Wu Y, He J, Yang L (2010) Evaluating adsorption and biodegradation
ularis. J Environ Chem Ecotoxicol 4:137–142 mechanisms during the removal of microcystin-RR by periphy-
Singh JS, Abhilash P, Singh H, Singh RP, Singh D (2011) Genetically ton. Environ Sci Technol 44:6319–6324
engineered bacteria: an emerging tool for environmental reme- Wu Y, Hu Z, Yang L, Graham B, Kerr PG (2011) The removal of
diation and future research perspectives. Gene 480:1–9 nutrients from non-point source wastewater by a hybrid biore-
Sinha S, Mukherjee SK (2008) Cadmium-induced siderophore actor. Bioresour Technol 102:2419–2426
production by a high Cd-resistant bacterial strain relieved Cd Wu Y, Li T, Yang L (2012) Mechanisms of removing pollutants from
toxicity in plants through root colonization. Curr Microbiol aqueous solutions by microorganisms and their aggregates: a
56:55–60 review. Bioresour Technol 107:10–18
Siripornadulsil S, Siripornadulsil W (2013) Cadmium-tolerant bacte- Wu G, Sun M, Liu P, Zhang X, Yu Z, Zheng Z et al (2014)
ria reduce the uptake of cadmium in rice: potential for microbial Enterococcus faecalis strain LZ-11 isolated from Lanzhou reach
bioremediation. Ecotoxicol Environ Saf 94:94–103 of the Yellow River is able to resist and absorb cadmium. J Appl
Stanbrough R, Chuaboonmee S, Palombo EA, Malherbe F, Bhave M Microbiol 116:1172–1180
(2013) Heavy metal phytoremediation potential of a heavy metal Xia L, Yin C, Cai L, Qiu G, Qin W, Peng B, Liu J (2010) Metabolic
resistant soil bacterial isolate, Achromobacter sp. strain AO22. changes of Acidithiobacillus caldus under Cu2? stress. J Basic
APCBEE Procedia 5:502–507 Microbiol 50:591–598
Sulaymon AH, Mohammed AA, Al-Musawi TJ (2013) Column Yan N (2013) Structural advances for the major facilitator superfam-
biosorption of lead, cadmium, copper, and arsenic ions onto ily (MFS) transporters. Trends Biochem Sci 38:151–159
algae. J Bioprocess Biotech 3:1–7 Yilmaz EI, Ensari N (2005) Cadmium biosorption by Bacillus
Tsuruta T, Umenai D, Hatano T, Hirajima T, Sasaki K (2014) circulans strain EB1. World J Microbiol Biotechnol 21:777–779
Screening micro-organisms for cadmium absorption from aque- Zeid AAA, Hassanein WA, Salama HM, Fahd GA (2009) Biosorption
ous solution and cadmium absorption properties of Arthrobacter of some heavy metal ions using bacterial species isolated from
nicotianae. Biosci Biotechnol Biochem 78:1791–1796 agriculture waste water drains in Egypt. J Appl Sci Res
Valls M, De Lorenzo V (2002) Exploiting the genetic and biochem- 5:372–383
ical capacities of bacteria for the remediation of heavy metal Zeng X-X, Tang J-X, Liu X-D, Jiang P (2009) Isolation, identification
pollution. FEMS Microbiol Rev 26:327–338 and characterization of cadmium-resistant Pseudomonas aerug-
Vanoort R, Cressey P, Silvers K (2000) 1997/98 New Zealand Total inosa strain E1. J Cent South Univ Technol 16:416–421
Diet Survey. Part 2: Elements. Report prepared for the Ministry Zeraatkar AK, Ahmadzadeh H, Talebi AF, Moheimani NR, McHenry
of Health MP (2016) Potential use of algae for heavy metal bioremedia-
Varghese R (2012) Bioaccumulation of cadmium by Pseudomonas sp. tion, a critical review. J Environ Manag 181:817–831
isolated from metal polluted industrial region. Environ Res Eng Zheng L, Abhyankar W, Ouwerling N, Dekker HL, van Veen H, Van
Manag 61:58–64 der Wel NN et al (2016) The Bacillus subtilis spore inner
Vinod V, Sashidhar R (2011) Bioremediation of industrial toxic membrane proteome. J Proteome Res. doi:10.1021/acs.
metals with gum kondagogu (Cochlospermum gossypium): a jproteome.5b00976

123
Int. J. Environ. Sci. Technol.

Zhou W, Ma Y, Zhou J, Zhang Y (2013) Bio-removal of cadmium by Cd(II) and Cr(VI) biosorption on Staphylococcus xylosus and
growing deep-sea bacterium Pseudoalteromonas sp. SCSE709-6. Pseudomonas sp. in single and binary mixtures. Bioresour
Extremophiles 17:723–731 Technol 98:2859–2865
Zhu N, Zhang L, Li C, Cai C (2003) Recycling of spent nickel– Zouboulis A, Loukidou M, Matis K (2004) Biosorption of toxic
cadmium batteries based on bioleaching process. Waste Manag metals from aqueous solutions by bacteria strains isolated from
23:703–708 metal-polluted soils. Process Biochem 39:909–916
Ziagova M, Dimitriadis G, Aslanidou D, Papaioannou X, Tzannetaki
EL, Liakopoulou-Kyriakides M (2007) Comparative study of

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