Review
Soluble microbial products and their
implications in mixed culture
biotechnology
Bing-Jie Ni1, Bruce E. Rittmann2 and Han-Qing Yu3
1
School of Earth and Space Sciences, University of Science and Technology of China, Hefei, 230026 China
2
Swette Center for Environmental Biotechnology, Arizona State University, Tempe, AZ 85287-5701, USA
3
Department of Chemistry, University of Science and Technology of China, Hefei, 230026 China
Soluble microbial products (SMP) are soluble organic
compounds released during normal biomass metabo-
lism in mixed culture biotechnology. In this review, we
give the up-to-date status on several essential SMP
issues: mechanisms of SMP formation, differentiation
between utilization-associated products (UAP) and bio-
mass-associated products (BAP), biodegradability of the
SMP components, how formation of SMP by autotrophs
controls effluent quality and supports a substantial pop-
ulation of heterotrophs, mathematical modeling that
includes SMP, and improving effluent quality by control-
ling SMP. We also present two timely examples that
highlight our current understanding and give an indica-
tion of how SMP affects the performance of modern
mixed culture biotechnology: membrane fouling of
membrane bioreactors (MBRs) and the dynamics of
SMP in anaerobic systems.
Introduction
Soluble microbial products (SMP) are soluble organic com-
pounds that are released during normal biomass metabo-
lism and decay in mixed culture biotechnology (see
Glossary), such as activated sludge processes, anaerobic
digestion, and membrane bioreactor (MBR) technologies
[1]. Resulting from processes common to most bacteria,
SMP comprise a wide range of compounds with low to high
molecular weights (MWs) (0.5 to 50 kDa) [2]. SMP are
important because they are ubiquitously present and often
form the majority of the effluent chemical oxygen demand
(COD) and biochemical oxygen demand (BOD) from bio-
logical treatment systems [2–11]; therefore, they control
the performance of the process, as effluent COD and BOD
are regulated. Also of special contemporary importance is
the role of SMP in membrane fouling of MBRs, which are
becoming more prevalent worldwide [7,9,12–14].
Although clearly significant in mixed culture biotech-
nology, SMP have proven a challenge to measure and
characterize because they are a mixture of unknown com-
pounds that do not correspond to any well-defined com-
pound that is a substrate or product (e.g., glucose is a well-
defined substrate, and a well-defined product would be
Corresponding authors: Rittmann, B.E. (Rittmann@asu.edu);
Yu, H.-Q. (hqyu@ustc.edu.cn).
454 0167-7799/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tibtech.2011.04.006 Trends in Biotechnology, September 2011, Vol. 29, No. 9
Glossary
Activated sludge process: an aerobic biological wastewater treatment process
based on a suspended-growth mixed culture that is selectively retained so that
the SRT of the biomass is substantially larger than the system’s HRT.
Anaerobic baffled reactor: an anaerobic bioreactor consisting of alternating
hanging and standing baffles, which compartmentalize the reactor so that the
liquid flows up and down from one compartment to the next.
Anaerobic digestion: an anaerobic mixed culture process in which organic
solids are hydrolyzed, fermented, and then converted to methane gas (CH4).
AOB: ammonia-oxidizing bacteria, or aerobic bacteria that oxidize NH3 as their
electron-donor substrate.
Biochemical oxygen demand (BOD): the electron equivalents in biodegradable
organic compounds expressed as O2: 8 g O2 per e– equivalent. BOD is
measured by a bioassay and is a gauge of the amount of biodegradable
organic pollution in water.
Biomass-associated products (BAP): the type of SMP that is produced from the
hydrolysis of biomass, in particular from EPS.
BOD5: the result of the most common bioassay of the BOD, a 5-day incubation.
Chemical oxygen demand (COD): the electron-donating equivalents in the C of
organic compounds expressed as O2: 8 g O2 per e– equivalent. COD is a gauge
of the amount of organic pollution in water.
Extracellular polymeric substances (EPS): complex polymeric organic materi-
als produced and secreted by microorganisms for the purpose of adhesion.
Feast-and-famine conditions: alternating conditions of electron-donor avail-
ability caused by cyclic feeding and variations in the presence electron
acceptors; often occurs in an SBR.
Floc: a natural aggregation of biomass, as in activated sludge.
Hydraulic retention time (HRT): the average residence time of water in a
continuous-flow process.
Internal storage polymers: organic polymers, such as polyhydroxybutryate
and glycogen, that some heterotrophic microorganisms produce rapidly and
store during periods of high electron-donor availability (i.e., feast). They can
then be used to support metabolism during periods of electron-donor famine.
Maximum specific utilization rate: the maximum utilization rate of substrate by
microorganisms per unit concentration of biomass.
Membrane bioreactor (MBR): a mixed culture technology that retains biomass
using a membrane separator.
Mixed culture biotechnology: a biotechnology that utilizes a microbial
community comprised of multiple types of microorganisms, not a pure culture.
MW: molecular weight, expressed in g/mol.
NOB: nitrite-oxidizing bacteria, or aerobic bacteria that oxidize NO2– as their
electron-donor substrate.
Sequencing batch reactor (SBR): a mixed culture process in which the input is
fed in cycles that also contain periods of treatment and effluent withdrawal.
Sludge cake: a static deposition of solids on the membrane surface that cannot
be removed by normal shear forces.
Solids retention time (SRT): the average time that biomass spends in the
process; it also is the reciprocal of the specific growth rate.
Specific cake resistance: the resistance of the permeate flux by sludge cake
divided by deposited mass per unit membrane area.
Substrate: the compounds that microorganisms oxidize and reduce in order to
generate energy to fuel their growth. The electron-donor substrate is oxidized,
and the electrons are used to reduce the electron-acceptor substrate.
SUVA: specific ultraviolet absorbance.
Utilization-associated products (UAP): the type of SMP that is produced
directly as part of electron-donor oxidation.
Review
Box 1. The characterization methods for SMP
Although most previous studies have focused on global measure-
ment of SMP [2], SMP is complex, consisting of proteins,
polysaccharides, and some humic-like materials [21]. SMP have
been found to have a very wide MW distribution and different
structures and functional groups [2,7,8,11,22]. How can SMP be
characterized better in terms of its molecular size, structure and
functionality?
Gel-permeation chromatography (GPC) has been widely used to
determine the MW distribution of SMP from different origins [2,8,21].
The MW distribution of SMP has been extensively examined because
it is useful in assessing the efficiency and suitability of the subsequent
treatment facilities [2]. A minority of SMP had a MW between 1 and 10
kDa; most SMP were either smaller than 1 kDa or greater than 10 kDa
[21]. Barker and Stuckey [2] also reported a bimodal distribution, with
30% of MW <1 kDa and 25% of MW >100 kDa. This type of bimodal
distribution of SMP supports the division between UAP (low MW) and
BAP (high MW) [20].
Fourier transform infrared spectroscopy (FTIR) and dissolved
organic carbon (DOC) have been utilized to analyze the functional
group characteristics and total content of SMP, respectively [20,21].
Jarusutthirak and Amy [21] found that FTIR spectra of fouling
materials on membranes consisted of SMP-like mixtures of poly-
saccharides, proteins, and/or amino-sugar-like compounds. This
finding was related to the role of SMP in membrane fouling and flux
decline [21].
Chemical analysis has also been performed to determine poly-
saccharides and proteins present in SMP [2,7]. Rosenberger et al. [7]
found that, for two parallel membrane bioreactors, macromolecules,
such as polysaccharides and proteins, and organic colloids with a
molecular weight of over 120 kDa contributed significantly to
membrane fouling. Higher concentrations of these substances
correlated to higher fouling rates. Liang et al. [36] observed that
carbohydrates and proteins appeared to be the SMP components
more prone to accumulate in the MBR, compared with aromatic
compounds. The proportions of SMP with large molecular weight in
supernatants and in filtered effluents were almost identical, implying
that membrane sieving did not work for most SMP. Instead,
hydrophilic neutrals (e.g., carbohydrates) were most likely, respon-
sible for high fouling potentials of SMP observed at short SRTs.
acetate). Box 1 briefly summarizes chemical characteriza-
tion methods that have been applied to SMP.
Despite methodological challenges, the importance of
SMP is now being recognized, and increased scrutiny of
SMP over the last decade has yielded significant progress
regarding fundamental mechanisms controlling the fate of
SMP and their importance in biological wastewater treat-
ment systems. One important realization is that SMP are
related to another type of microbial product, extracellular
polymeric substances (EPS), which are sticky solid materi-
als excreted by cells [1]. Understanding the mechanisms
affecting SMP requires a clear view of its relationship to
EPS [1]. Whereas SMP are soluble, EPS are part of the
solid biomass.
We give an up-to-date synthesis of these essential SMP
issues: mechanisms of SMP formation, differentiation be-
tween utilization-associated products (UAP) and biomass-
associated products (BAP), biodegradability of the SMP
components, how formation of SMP by autotrophs controls
effluent quality and supports a substantial population of
heterotrophs, mathematical modeling that includes SMP,
and improvement of effluent quality by controlling SMP.
We also discuss two timely and forward-looking examples
that highlight our current understanding and give an
indication of how SMP affects the performance of modern
Trends in Biotechnology September 2011, Vol. 29, No. 9
mixed culture biotechnology: membrane fouling of MBRs
and the dynamics of SMP in anaerobic systems.
Mechanisms of SMP formation
Laspidou and Rittmann [1,15] developed a ‘unified theory’
coupling the production and degradation of SMP with the
formation and degradation of EPS. Box 2 summarizes the
theory and explains the relationships among key concepts
and components discussed in this review. Although the
unified theory was developed originally for aerobic sys-
tems, it has also proven reliable for anaerobic systems.
Noguera et al. [16] found that SMP were produced directly
from substrate metabolism (usually with biomass growth)
and from biomass decay during the complete mineraliza-
tion of simple substrates in a pure-culture anaerobic sys-
tem. SMP formation was stimulated by an increased
concentration of exogenous electron donor due to the in-
creased amount of microbial metabolism [2,16].
Aquino and Stuckey [17] proposed an alternative ap-
proach for some parts of the unified theory. They consid-
ered that BAP could be formed by lysis of active biomass (a
decay process) and also from what they called ‘soluble
EPS’. The former route is a form of direct decay that is
required because the model of Aquino and Stuckey [5] does
not include EPS. The earliest models of BAP formation
(e.g., [18]) used the same approach, because they also did
not include EPS. The second route requires that bound
EPS is stripped off the cells and then hydrolyzed to ‘soluble
EPS’ that can contribute to BAP; the last mechanism
accords with the unified theory in that EPS hydrolysis is
the source of BAP (Box 2).
Differentiation between UAP and BAP
Differentiating UAP from BAP has proven to be a chal-
lenge, since both components are heterogeneous materials,
not specific compounds. It was possible to prove that UAP
were separate from BAP by using 14C tracers in simple
model substrates [19,20], but this approach is not possible
for complex organic substrates, such as in wastewaters.
Because the organic components comprising SMP and
wastewater are similar mixtures of undefined compounds,
they cannot be distinguished by simple chemical analysis
only. If UAP and BAP could be accurately and quantita-
tively differentiated, it would become possible to determine
which type of SMP is responsible for effluent COD or for
fouling membranes, and effective control measures may
become evident.
Significant progress has been made in the past decade,
particularly with regard to confirming that BAP has a
much larger MW than UAP and accounts for the majority
of the effluent soluble organic matter. Jarusutthirak and
Amy [21] found that BAP exhibited characteristics of
hydrophilic organic colloids and macromolecules consist-
ing of polysaccharides, proteins, and/or amino-sugar-like
compounds. Jarusutthirak and Amy [22] also showed that
BAP contained in the effluent of a sequencing batch reactor
consisted mainly of high-MW (>10 kDa) organic matter
that had low specific ultraviolet absorbance (SUVA) and a
hydrophilic character.
Jiang et al. [19,23] conducted experiments in which they
attempted to produce UAP that could be distinguished
455
Review
Box 2. The unified theory of SMP and other biomass components
Figure I summarizes the pathways and mechanisms for SMP
formation for a heterotrophic community, such as in activated sludge
wastewater treatment. In the unified theory [1,15], SMP includes all of
the truly soluble products, EPS includes solid-phase products actively
generated during metabolism, and inert biomass includes solids
generated by biomass decay. The unified theory establishes a
comprehensive mass balance so that none of the components overlap
and nothing is left out.
The unified theory classifies SMP into two groups based on the type
[(Figure_I)TD$G]
of bacterial metabolism from which they are derived: UAP that are
Bulk liquid
Electron
donor
substrate
Cell synthesis
Substrate utilization
for UAP formation
SMP
UAP
EPS hydrolysis
for BAP formation
BAP
Figure I. Schematic of the metabolism of SMP and EPS formation in a heterotrophic microbiological system according to the unified theory of SMP and other biomass
components.
from BAP in order to differentiate their characteristics.
The UAP-production batch experiment was conducted
with acetate as substrate [23]. A batch control experiment
was conducted without acetate addition to estimate the
background BAP. True UAP, estimated by difference, in-
cluded protein-like biopolymers and low-MW humic-like
compounds, which generally increased after acetate addi-
tion. BAP had much higher MW than those of UAP, with
63% having MW >20 kDa [19].
Combining chemical analyses and mathematical model-
ing, Ni et al. [20] characterized and fractionated SMP in
activated sludge effluent. The UAP were carbonaceous
compounds with an MW lower than 1 kDa, whereas the
BAP were mainly macromolecules with an MW higher
than 10 kDa.
What is the biodegradability of the SMP components?
Noguera et al. [16], Rittmann and McCarty [24], deSilva
and Rittmann [4], and Jiang et al. [19] summarized that
UAP and BAP have distinct degradation kinetics, with UAP
more readily biodegraded, perhaps owing to their smaller
MW and simpler structure. The slow kinetics of BAP bio-
degradation is illustrated by the low maximum specific
utilization rate for its aerobic biodegradation of 0.07 g
COD/g volatile suspended solids (VSS-d) and its high affini-
ty concentration of 85 g CODBAP/m3 [3,4,14,15,17,18,24,25].
By contrast, the aerobic biodegradation kinetics of UAP
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Trends in Biotechnology September 2011, Vol. 29, No. 9
produced directly during substrate utilization and BAP that are
produced indirectly via the hydrolysis of a biomass component. The
unified theory explains that: (i) SMP are the same as what sometimes
have been called ‘soluble EPS’ in the past; (ii) all EPS are solid phase,
corresponding to what sometimes has been termed ‘bound EPS’; (iii)
UAP are formed in proportion to substrate utilization; (iv) the
formation of EPS is proportional to the rates of substrate utilization
and biomass synthesis; and (v) BAP are formed solely by the
hydrolysis of EPS. The arrows illustrate all of these mechanisms for
formation of SMP and EPS.
Biomass
Inert biomass
(non-biodegradable)
Decay
Active
biomass
EPS formation
EPS
TRENDS in Biotechnology
has a maximum specific utilization rate of 1.3 g COD/g
VSS-d and an affinity concentration of 100 g CODUAP/m3
[3,4,14,15,17,18,24,25].
Based on the slow biodegradation kinetics of BAP (nor-
mally the dominant component of effluent SMP), Rittmann
and McCarty [24] estimated that the BOD5 of BAP is only
14% of its COD. Jiang et al. [23] found that the BOD5 was
only 2.8% of the COD for BAP. Therefore, SMP, especially
BAP, can form a dominant part of the effluent’s soluble
COD [1,2,26], but may not have a correspondingly large
impact on the BOD5 because of their extremely low biode-
gradability.
SMP from autotrophs supports heterotrophs
Heterotrophs and autotrophs often coexist in nitrifying
systems cultured without any externally added COD
[27–30]. Viewed with SMP in mind and as illustrated in
Figure 1, this situation is logical because autotrophs con-
vert inorganic carbon into organic carbon, including SMP,
to support the growth of heterotrophs. Furthermore, the
heterotrophs return inorganic carbon to the autotrophs
from SMP oxidation.
These relationships were demonstrated experimental-
ly. For example, a culture of nitrite-oxidizing bacteria
(NOB) produced EPS and SMP during nitrite oxidation
[31], and these products were the energy and carbon
sources for the observed heterotrophic growth [32]. Other
(Figure_1)TD$IG][ Review Trends in Biotechnology September 2011, Vol. 29, No. 9

Autotrophic growth

HCO3- UAP HCO3- UAP

NH4+ AOB NO2- NO2- NOB NO3-

O2 O2
EPS EPS

Hydrolysis Hydrolysis

BAP
Heterotrophic growth
AOB: Ammonium oxidizing bacteria
NOB: Nitrite oxidizing bacteria
UAP HET BAP HET: Heterotrophic bacteria
EPS: Extracellular polymeric substances
O2 O2 UAP: Utilization associated products
BAP: Biomass associated products

TRENDS in Biotechnology

Figure 1. Schematic representation of the bioreactions carried out in the three microbial groups and the exchanges of SMP (UAP and BAP) between autotrophs and
heterotrophs in an autotroph-based system.

studies documented that heterotrophs depend on the au-
totrophic production of SMP when only inorganic electron
donors (e.g., ammonium or hydrogen) are supplied to the
system [27,33,34]. Matsumoto et al. [32] evaluated the
community structure in nitrifying granules (average di-
ameter 1600 mm) produced in an aerobic reactor fed with
ammonium nitrogen (NH4+–N) as the sole electron donor.
The research revealed that ammonia-oxidizing bacteria
(AOB) dominated within the first 200 mm below the gran-
ule surface, NOB occupied a deeper layer between 200 and
300 mm, and heterotrophic bacteria and EPS were present
in the core of the nitrifying granule. Having EPS and
heterotrophs in the core of the granule supported the
theory that SMP from autotrophs were the substrate for
the growth of heterotrophs.
Matsumoto et al. [32] also constructed one- and two-
dimensional numerical models to explain the observed
granule development as a result of the multiple bacteria–
substrate interactions. Modeling results showed that het-
erotrophs that utilized UAP were present at the surface of
the nitrifying granule, where sufficient UAP was produced
by active nitrifying bacteria. Heterotrophs that utilized BAP
were present throughout the granule, because EPS pro-
duced by active bacteria spread broadly in the granule.
Because heterotrophs utilize UAP and BAP with signif-
icantly different kinetics, different phylogenetic groups of
heterotrophs may be responsible for mineralizing UAP and
BAP. Box 3 explores ways in which this difference can
affect the microbial ecology when the heterotrophs live
mainly on SMP produced by nitrifiers.

Box 3. Heterotrophic growth through utilization of SMP released by autotrophs

Kindaichi et al. [27] found that an autotrophic nitrifying biofilm was than that of nitrifying sludge (25%). Heterotrophs that live by
composed of 50% nitrifying bacteria (AOB + NOB) and 50% hetero- scavenging SMP should be inherently slow growers because of the
trophic bacteria. The heterotrophs were members of the alpha subclass slow biodegradation kinetics of SMP [4,15,19,21,23,24]. Therefore,
of the class Proteobacteria: a-Proteobacteria (23%), g-Proteobacteria they can accumulate better in a biofilm or granule, particularly if they
(13%), green nonsulfur bacteria (GNSB, 9%), Cytophaga-Flavobacter- are away from the outer surface, where detachment occurs. This
ium-Bacteroides (CFB) division (2%), and unidentified bacteria (3%). In a advantage to BAP-scavenging heterotrophs is accentuated if en-
follow up study, Okabe et al. [29] cross-fed microbial products derived hanced SMP accumulation occurs within nitrifying biofilm or granules
from 14C-labeled nitrifying bacteria to heterotrophic bacteria coexisting because the average SRT of a nitrifying biofilm can be extremely long
in an autotrophic nitrifying biofilm. The objective was to determine [27,32]. In addition, biofilms and granules should accentuate an
which phylogenetic groups of heterotrophic bacteria could directly efficient food web for carbon exchange in the autotrophic-based
utilize the microbial products derived from nitrifying bacteria. Okabe community.
et al. [29] revealed that the members of the Cytophaga-Flavobacterium
cluster gradually utilized 14C-labeled products from a nitrifying culture
Table I. The active-biomass fractions in autotrophic
in which the nitrifiers were actively growing. This result suggests that
these bacteria preferentially utilized UAP of nitrifying bacteria. By
nitrifying systems
contrast, the members of the a-Proteobacteria and g-Proteobacteria Biomass type Source Active-biomass
preferred to utilize the organic matter produced by hydrolysis of EPS fractions (%)
(i.e., BAP). In particular, the members of the Chloroflexi biodegraded AOB NOB HET
the organic products from a nitrifying culture that was in net decay Nitrifying sludge Vadivelu et al. [30] – 75 25
because it had no NH4+-N addition. This implies that the members of
Nitrifying granules Matsumoto et al. [32] 60 10 30
the Chloroflexi preferentially utilized BAP.
Nitrifying biofilms Kindaichi et al. [27] 20 30 50
Our meta-evaluation of experimental observations reported in the
literature (Table I) indicates that heterotrophic growth in nitrifying Nogueira et al. [73] 20 50 30
biofilm or granules (30–50% active biomass) was significantly higher Okabe et al. [29] 50 20 30

457
Review
Mathematical modeling of SMP
When put into a quantitative modeling framework (rate
expressions, stoichiometry, and mass balances), the uni-
fied theory (Box 2) is an outstanding tool for explaining
how, for example, SMP affects effluent quality and mem-
brane fouling in MBRs. It can also help identify new
knowledge most needed from future research.
de Silva and Rittmann [4] developed a nonsteady-state,
multispecies model that describes activated sludge pro-
cesses that transform COD and nitrogen. Although the
mechanism of BAP formation pre-dated the unified model,
the model [4] included the important phenomenon that
UAP and BAP from nitrifiers can be electron donors for
heterotrophs. Using their model to interpret parallel
experiments, de Silva and Rittmann [3,4] found that the
concentration of effluent soluble COD was determined
mostly by the influent NH4+–N concentration, not the
influent COD concentration, in nitrifying activated sludge.
Ni et al. [25] developed an expanded unified model to
integrate production and consumption of internal storage
polymers with the fate of EPS, SMP, and active and inert
biomass in activated sludge. Internal storage polymers
include polyhydroxybutyrate and glycogen, which certain
bacteria are able to produce during periods of COD ‘feast’
and then use to sustain themselves during periods of COD
‘famine’ [25]. Ni et al. [25,26] carried out parallel experi-
ments and model simulations that followed EPS, SMP, and
internal storage polymers for sequencing batch reactors
(SBRs) and continuous-flow activated sludge. The model
outputs matched all experimental measurements and pro-
vided insights into the dynamics of the soluble and solid
components in activated sludge exposed to dynamic feast-
and-famine conditions in SBRs versus stable famine con-
ditions in the continuous-flow system. One key finding was
that the cycling feast-and-famine conditions of the SBR
altered the net production of EPS and SMP. The combina-
tion of experiments and modeling showed that a small UAP
peak at the time of substrate depletion at the beginning of
an SBR cycle, BAP dominated the effluent COD at the end
of an SBR cycle, and the constant famine conditions of the
continuous system lead to lower UAP accumulation, but
higher BAP accumulation than in an SBR due to the
constantly low availability of external substrate.
How can the effluent quality be improved by controlling
SMP?
The effluent concentration of SMP represents a balance of
their production and biodegradation in the biological pro-
cess. Because SMP (particular BAP) is slowly biodegrad-
able, the balance for SMP tends toward its accumulation.
Because most soluble organics that enter the process are
more readily biodegradable than SMP, the effluent soluble
COD generally is controlled by the SMP concentration.
Therefore, improving effluent soluble COD requires mini-
mizing SMP accumulation.
Although the accumulation of SMP can be affected by a
range of factors [2], the solids retention time (SRT) is
especially important, because it can be controlled by design
and operating decisions. The effluent concentrations of
UAP and BAP respond quite differently to the system’s
SRT [21,26]. The BAP concentration is controlled mainly
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Trends in Biotechnology September 2011, Vol. 29, No. 9
by its production rate from EPS, which is first order in EPS
concentration. BAP biodegradation is usually relatively
minor, because BAP have quite slow biodegradation kinet-
ics [15]. The concentrations of EPS and, hence, BAP in-
crease slowly with larger SRT. For very high SRT,
modeling says that BAP approaches 4–5% of the influent
substrate concentration (as COD) [14,16,21]. In contrast to
BAP, the UAP concentration sharply declines at high SRT,
where its production rate is low and its degradation rate is
relatively high due to the large accumulation of active
biomass. Thus, UAP become a major component in the
effluent soluble COD only when the SRT is relatively small,
whereas BAP are most important when the SRT is moder-
ate to large.
These model-predicted trends have been borne out by
experimental measurements. Mixed culture biotechnolo-
gies with a high SRT have been observed to accumulate
more high MW materials [21,22], and this should corre-
spond mainly to BAP [26]. Dong and Jiang [35] experimen-
tally confirmed that BAP were a higher proportion than
UAP in the effluent, especially at long SRTs. Jiang et al.
[19] also confirmed that SRT is a key parameter controlling
the SMP concentration: a lower SRT increased the UAP
concentration, but decreased the BAP concentration. In
addition, Liang et al. [36] found that accumulation of
hydrophilic SMP became more pronounced at short SRT,
but that the hydrophobic proportion of the SMP gradually
increased for longer SRT.
UAP production increases with the increasing substrate
volumetric loading because the formation of UAP is pro-
portional to the concentration of substrate removed. A
higher substrate volumetric loading also results in a great-
er concentration of EPS, which leads to more BAP accu-
mulation [15].
These growing understandings of what controls the
SMP concentration provide engineers with tools, highlight-
ed in Box 4, to optimize mixed culture biotechnology
operation to avoid a high effluent soluble COD from
SMP. In particular, operating at a relatively low SRT
minimizes effluent SMP. If a low SRT is not possible
due to other process requirements or does not give a low
enough SMP concentration, post-treatment needs to be
used to reduce SMP concentration.
Implications in mixed culture biotechnology
Role of SMP in membrane fouling of MBRs
MBRs are being employed more often for municipal and
industrial wastewater treatment [12], but membrane foul-
ing is one of the main obstacles for their wider application.
Over the past few years, considerable efforts have been
made to explore the membrane-fouling problem, and SMP
appear to play a role [13,21,37–40]. Because strategies for
preventing or reducing SMP-caused fouling are essential,
the impact of SMP on MBR fouling has attracted signifi-
cant attention [7,12,41,42].
As shown in Figure 2, membrane fouling by SMP can be
attributed to clogging of membrane pores, deposition of a
sludge cake, or both. Fouling results in a reduction of
permeate flux or an increase of trans-membrane pressure,
depending on the operating mode [12]. BAP are the most
probable cause of SMP-based fouling [21,43–45] because
 Review Trends in Biotechnology September 2011, Vol. 29, No. 9

Box 4. Techniques to improve effluent quality by controlling SMP

Engineers might be able to optimize bioreactor operation in order to
avoid a high effluent soluble COD and organic N from SMP. To do so
requires understanding of the ways that UAP and BAP differ in
chemical characteristics that affect effluent quality. The main text
describes that BAP are larger and more aromatic than UAP. In
addition, UAP are mainly carbonaceous compounds derived from the
original substrate, whereas BAP are cellular macromolecules contain-
ing carbon and nitrogen [4,21,26]. Therefore, UAP and BAP ought to
affect the N balance in the system differently because BAP contain
organic N in roughly the same proportion as in biomass (0.09 gN/
gCOD or 0.12 gN/g VSS).
According to modeling analysis by Ni et al. [26], the lowest
effluent soluble COD can be obtained for an SRT in the range of 2–
10 days (illustrated in Figure I). In this case, BAP dominates the
effluent COD, and it can be driven down to about 2% of the influent
COD. The effluent organic N associated with the BAP is then
approximately 0.17% of the influent COD. For much higher SRT,
the effluent COD is closer to 4–5% of influent COD [26], with
[(Figure_I)TD$G]
70
60
SCOD (mg/L)
effluent organic N from BAP proportionally higher at 0.35–0.44% of
the influent COD.
If the lowest concentrations achievable are still too high, engineers
might be able to preferentially remove BAP by post-treatment
processes [14,74–76], e.g., coagulation and bed filtration, granular
activated carbon adsorption, ozonation plus more biological treat-
ment, and membrane filtration. For example, Zhu et al. [74] used a
commercialized PVDF flat membrane to treat SMP of secondary
effluent by microfiltration. Their results showed that mainly SMP with
higher molecular weight (BAP) were retained by the membrane.
Based on pilot testing of an MBR system and modeling analysis, de
Silva et al. [75] interpreted that 70% of the BAP was retained by the
membrane separator. Kiser et al. [14] adopted a similar strategy by
assuming 50% removal of BAP with an MBR membrane. Zhu et al.
[74] also demonstrated that pre-ozonation could enhance the
membrane performance in filtration of the BAP, probably by
biodegradation by a biofilm on the membrane, as was observed by
others [55,77] for low MW SMP.
70
SMP BAP UAP
60

50 50

40 SMP (mg/L) 40

30 30

20 20

10 10

0 0
0 10 20 30 40 50 0 10 20 30 40 50
SRT (d) SRT (d)
TRENDS in Biotechnology

Figure I. Effects of SRT on production of SMP, UAP, and BAP and their contributions to the effluent soluble COD (based on Ni et al. [26]).

they accumulate more in MBRs due to the normally long cause more EPS increases the amount of the biomass
SRT in an MBR [12,13], the relatively refractory charac- solids, as well as the amount of BAP [1,15].
teristic of BAP [20], and their larger size [20,21,23], which Geng and Hall [49] observed that the floc-size distribu-
leads to membrane rejection. EPS could also play an tion and the amount of SMP in the mixed liquor were the
important role in membrane fouling by SMP [46–48] be- most important properties influencing the propensity for
[(Figure_2)TD$IG]
(a) (b)

Key:
(c) Components Legend
Sludge
flocs Particulate biomass

EPS Particulate biomass

Biomass associated
products (BAP)
Total Large BAP
SMP
Utilization associated
products (UAP)
TRENDS in Biotechnology

Figure 2. Schematic representation of membrane fouling in MBRs by SMP (UAP and BAP) and EPS attributed to (a) clogging of the membrane pores, (b) deposition of
sludge solids on membranes, and (c) both of them.

459
Review
membrane fouling. Furthermore, experimental results have
shown that polysaccharide-like substances in SMP contrib-
ute to fouling more than protein-like substances [21,50].
Fonseca et al. [37] observed that microbial products, in the
absence of microbiological activity, have intrinsic mem-
brane-fouling properties at levels that are operationally
significant to commercial-scale membrane treatment prac-
tices. Meng et al. [13] summarized that the impacts of SMP
on membrane fouling depend on SMP concentration, mem-
brane materials and operation modes.
SMP also play an important role in membrane fouling in
anaerobic MBRs. Aquino and Stuckey [51] showed that
SMP could cause membrane fouling in an anaerobic MBR.
Berube et al. [52] summarized that the size and concentra-
tion of SMP in the mixed liquor affected permeate flux for
anaerobic MBRs: high concentrations of SMP contributed
greatly to membrane fouling. Aquino et al. [53] found high-
MW protein and carbohydrate material in SMP to be the
main contributor to pore fouling of the membrane. Lin et al.
[54] further indicated that floc size, SMP, EPS and sludge-
cake layer structure were the major factors governing
membrane fouling in anaerobic MBR systems.
However, SMP are not always linked directly to mem-
brane fouling [55–60], and the impacts of SMP can be
highly variable [23,41,55,61]. For example, Drews et al.
[41,61] indicated that temperature, SRT, and pore size
Box 5. Modeling the performance and membrane fouling of MBRs
Jang et al. [78] published an MBR model that captures some of the
features of the unified model. In particular, it determines EPS, UAP, and
fractions of BAP that will and will not permeate the membrane. In
addition, the model calculates a modified fouling index used to predict
biofouling potentials. However, it does not include the effects of mixed
liquor suspended solids (MLSS) on trans-membrane flux and the
oxygen transfer efficiency. Instead, the molecular weight characteristics
of soluble materials are the focus in their model, in which a low
concentration of SMP with a high MW could cause a higher membrane-
fouling rate than a high concentration of low MW materials. Therefore,
the notion of a critical MW for membrane rejection was introduced in
their model. The critical MW is the largest MW able to pass through the
membrane pores. SMP larger than the critical MW are retained in the
bioreactor, and the membrane biofouling potential by SMP increases
with increasing fractions of rejected SMP.
Kiser et al. [14] adapted for the MBR the complete unified theory for
heterotrophic activated sludge. Specifically, they divided the BAP into
a large fraction retained by the membrane separator and a small
fraction passing through the membrane. Based on a meta-analysis of
[(Figure_I)TD$G]
Schwarz et al. [79], Kiser et al. [14] included relationships for how high
Soluble components
UAP BAP S Bioreactor
BAP L
UAPe BAPe Se
Figure I. Schematic diagram for membrane retention of SMP components.
460
Trends in Biotechnology September 2011, Vol. 29, No. 9
affected SMP’s propensity to foul. Jiang et al. [23] showed
that membrane-retained SMP did not always yield fouling
effects. Ironically, UAP had the highest specific cake resis-
tance and pore blocking resistance, although their reten-
tion percentage was lower than BAP [23]. Pan et al. [55]
also found that only the hydrophilic fraction of SMP was a
major cause for membrane fouling. Therefore, ‘blaming’
SMP for MBR fouling is too simplistic, particularly since
the dynamics and characteristics of SMP are still emerg-
ing.
Despite uncertainties, many investigations suggest that
SMP (mainly BAP) have a significant impact on membrane
fouling. Thus, the control of the SMP concentration in
MBRs may be crucial to long-term good performance of
the membrane. As indicated above, SMP control can be
achieved to a limited degree by adjusting the SRT. High
SRT leads to the greatest BAP concentration, and this is
exacerbated by a high volumetric loading of COD and a
high rejection of BAP by the membrane [14].
Comprehensive mechanistic models of the microbiolog-
ical phenomena that affect effluent water quality and
trans-membrane flux in MBRs have been proposed recent-
ly to describe the performance and membrane fouling of
MBRs. These models, highlighted in Box 5, identify param-
eters and mechanisms that need to be better defined to
understand the role of SMP in MBR fouling.
MLSS concentration lowers the oxygen-transfer rate and the trans-
membrane flux. In particular, a high concentration of MLSS, which is
controlled in part by its EPS content, lowers the oxygen-transfer rate
and the critical trans-membrane flux. According to the model results
for a heterotrophic system, effluent COD is sensitive to the influent
COD and to the ability of the membrane to retain the large BAP. High
influent COD or a membrane that is relatively permeable to BAP
results in larger effluent COD. Although the ability of an MBR to
achieve high MLSS and volumetric loading has cost benefits, high
MLSS increases the required aeration power and decreases the trans-
membrane flux.
The modeling work to date provides a good framework for guiding
profitable new research. In the area of membrane fouling in MBRs,
research should be focused on quantifying how membranes retain
BAP and how the critical trans-membrane flux is affected by particular
components of the mixed liquor (e.g. EPS or large BAP, illustrated in
Figure I). More generally, research should be focused on determining
the formation and consumptions kinetics for BAP, which requires a
similar focus on EPS and on the generation of SMP by autotrophic
microorganisms.
Biomass
EPS, Xa
and Xi
Membrane
The effluent of MBR
TRENDS in Biotechnology
Review
SMP in anaerobic systems
Most information on SMP production, consumption, and
characterization comes from aerobic systems [62]. To date,
information about the SMP production in anaerobic sys-
tems conditions has been relatively sparse [63–65]. The
dearth of information on anaerobic SMP is partly due to
methodological limitations. In particular, it is necessary to
exclude fermentation products (e.g., volatile fatty acids, or
VFA) from true SMP. Fortunately, the common fermenta-
tion products can be measured separately (e.g., [66]).
SMP formation may differ quantitatively in anaerobic
systems, compared to aerobic systems. For example, SMP
accumulation varied from 2 to 68% of the influent COD in
the aerobic reactor, but from 9 to 27% in the anaerobic
reactor [67]. For both reactors, more SMP accumulated
when the substrate was acetate, compared to glucose. SMP
accumulation was smaller with lower temperature and
hydraulic retention time (HRT) in the aerobic reactor,
but HRT and temperature had little impact on SMP accu-
mulation in the anaerobic reactor. Barker and Stuckey [68]
indicated that SMP accumulation in anaerobic system
depended not only on the strength of the substrate input,
but also on the composition of the feed and the type of
reactor. Kuo et al. [69] showed that longer SRTs resulted in
higher levels of SMP, with SMP ranging from 17 to 59 mg
COD/L when acetate was the sole carbon and energy source
and 50 to 291 mg COD/L when glucose was the sole sub-
strate. Normalized production of SMP (SMP/influent COD)
during anaerobic treatment appeared to be lower when
compared with aerobic production of SMP reported in the
literature [69].
SMP accumulation in anaerobic systems was increased
by stress conditions, such as temperature changes, toxic
substances, and osmotic shocks [2]. Baker et al. [70]
showed that SMP accumulation in an anaerobic baffled
reactor increased with increasing HRT due to enhanced
biomass decay at high HRTs. It also increased with de-
creasing temperature due to increased stress on the bio-
mass and a reduced rate of SMP utilization at low
temperatures. SMP accumulation in anaerobic chemo-
stats also was increased by nutrient deficiency, possibly
due to enhanced cell lysis under stressed conditions [71]
and by a higher chromium (a toxicant) concentration [5].
Hydrolysis of EPS did not seem to contribute to SMP
accumulation in the presence of chromium, but cell lysis
products appeared to become important [2,5]. Kuo and
Parkin [72] showed that SMP complexed nickel (a toxic
heavy metal), playing a role in mitigating heavy metal
toxicity. Thus, cells may produce more SMP when exposed
to stress conditions.
Concluding remarks
We have outlined several essential SMP issues and dis-
cussed their implications in modern mixed culture biotech-
nology. The mechanisms affecting SMP are closely related
to another important type of microbial product, EPS. UAP
and BAP have distinct chemical and degradation kinetics,
with UAP more readily biodegraded and BAP having a
much larger MW. SMP, especially BAP, can form a domi-
nant part of the effluent’s soluble COD, but may not have a
correspondingly large impact on the BOD5. UAP become a
Trends in Biotechnology September 2011, Vol. 29, No. 9
major component in the effluent soluble COD only when
the SRT is relatively small, whereas BAP are most impor-
tant when the SRT is moderate to large. Production of SMP
by autotrophs can control effluent soluble COD in nitrify-
ing systems. Examples of the roles of SMP in MBR fouling
and in anaerobic systems highlight our current under-
standing and how SMP can affect the performance of
modern mixed culture biotechnology.
Future research in SMP will probably focus on quanti-
fying how membranes retain BAP and how the critical
trans-membrane flux is affected by particular components
of the mixed liquor (e.g., EPS or large BAP). More gener-
ally, research should be focused on determining the forma-
tion and consumption kinetics for BAP, which requires a
similar focus on EPS, the generation of SMP by autotrophic
microorganisms and characteristic of SMP in anaerobic
systems.
Acknowledgments
The authors wish to thank the Natural Science Foundation of China
(50738006 and 50828802) for the partial support of this work.
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