Open Access

Soluble microbial products (SMPs) release in activated sludge systems: a review

  • Hamed Azami1,
  • Mohammad Hossein Sarrafzadeh1Email author and
  • Mohammad Reza Mehrnia1
Iranian Journal of Environmental Health Science & Engineering20129:30

DOI: 10.1186/1735-2746-9-30

Received: 5 December 2012

Accepted: 5 December 2012

Published: 18 December 2012

Abstract

This review discusses the characterization, production and implications of soluble microbial products (SMPs) in biological wastewater treatment. The precise definition of SMPs is open to talk about, but is currently regarded as “the pool of organic compounds that are released into solution from substrate metabolism and biomass decay”'. Some of the SMPs have been identified as humic acids, polysaccharides, proteins, amino acids, antibiotics, extracellular enzymes and structural components of cells and products of energy metabolism. They adversely affect the kinetic activity, flocculating and settling properties of sludge. This review outlines some important findings with regard to biodegradability and treatability of SMPs and also the effect of process parameters on their production. As SMPs are produced during biological treatment process, their trace amounts normally remain in the effluent that defines the highest COD removal efficiency. Their presence in effluent represents a high potential risk of toxic by-product formation during chlorine disinfection. Studies have indicated that among all wastewater post-treatment processes, the adsorption by granular activated carbon combined with biologically induced degradation is the most effective method for removal of SMPs. However, it may be concludes that the knowledge regarding SMPs is still under progress and more work is required to fully understand their contribution to the treatment process.

Keywords

Soluble microbial products (SMPs) Effluent Biodegradability Wastewater Activated Sludge

Introduction

Effluents from biological wastewater treatment systems contain a variety of colloidal and soluble organic compounds, including residual degradable or hard-biodegradable influent substrate, intermediates and end products, complex organic compounds formed through chain reactions with both intermediate and final degradation products categorizing as soluble microbial products (SMPs). The presence of complex residual microbial products in wastewater effluents was confirmed from the time when Gaffney and Heukelekian conducted a study dealing with comparison of oxidation rates of the lower fatty acids under various conditions [1]. Since then many researchers [25] have shown that the majority of the soluble organic materials in effluents produced through biological treatment processes are actually microbial products (SMPs). Their presence is an issue of great interest not only in terms of achieving current discharge standards, but also because they effectively set the lower boundary for treatment.

Since the application of membrane based technologies in wastewater treatment and its combination with biological processes in a system such as membrane bioreactor (MBR), more special attention was given to the SMPs due to their role in membrane fouling. Nowadays, many researches concentrate on SMP and their effect on performance of biological processes as the increasing amount of published articles during last two decades confirm it (Figure 1).
https://static-content.springer.com/image/art%3A10.1186%2F1735-2746-9-30/MediaObjects/40201_2012_Article_16_Fig1_HTML.jpg
Figure 1

Number of published articles on SMP and related subjects in various years extracted from Engineering-Village databases.

Paying attention to the presence of SMPs, has resulted in development of wastewater treatment systems. Previously, models of wastewater treatment systems had been based on the Monod models which predict the effluent composition of the rate limiting substrate independently of the influent substrate concentration. Monod models did not agree with experimental results and the interaction of SMPs formation paved the way for more accurate modeling of wastewater treatment [6].

Activated sludge models (ASMs) proposed by IWA are fundamentally based on first engineering principles, meaning that the model equations were developed from general balance equations applied to mass and other conserved quantities, resulting in a set of differential equations.

Many researchers tried to improve the activated sludge models by adding SMPs components into ASM1 and ASM3, and also by integrating the extracellular polymeric substances (EPSs) into ASM1 model [710].

Yoon et al. [11] proposed a kinetic model to calculate the sludge production and aeration requirement. Tian et al. [4] extended ASM3 model to ASM3-SMP with taking into account the concept of simultaneous storage and growth of SMPs by considering two components: Utilization associated product (SUAP) and Biomass associated products (SBAP). However, all of them (except [4, 7]) used parameters directly taken from literature derived from activated sludge systems or even biofilm systems.

These advances in modeling, resulted in a better understanding of how mixed bacterial populations work. Chemical structure of SMP compounds has also been clarified due to advances in chemical identification and analytical methods. Most of the works have focused on SMPs in aerobic systems, but some of researches have also investigated SMPs in anaerobic systems [1214].

As mentioned above, SMPs are the main portion of contaminants in effluent of activated sludge not only increasing the BOD content of effluent, but also deteriorating settling properties of activated sludge. In addition, researches indicated that SMPs act as glue and bind the suspended flocs causing increase in activated sludge viscosity [15, 16]. Furthermore, SMPs as a kind of biopolymers have detrimental impact on activated sludge process [17]. The main obstacle to evaluate the impact of SMPs in wastewater treatment process is the difficulty in SMPs measuring especially in complex effluents [18].

Many works have been conducted on pure cultures and have defined feeds for better understanding and evaluation the effects of SMPs on treatment process. However, in industrial systems the phenomenon is more complicated and can be considered as an uncompleted task that needs to be studied more.

Despite the obvious importance of SMPs in wastewater treatment processes, a few publications have attempted to summarize all the information in a comprehensive review. Kimura et al. [19], performed a precise study of microbial product formation in biological systems which concentrated on: the measured characteristics of SMPs in biological processes; effect of sludge age; and the literatures on product formation and effect of product on membrane fouling in MBR. The objective of present paper is to review the currently available literature on SMPs, focusing on: their definition and their origin; biodegradability properties; the factors affecting the production of SMPs; and the treatment (i.e. removal) of SMPs. The current state of the art will be summarized and, finally, a closing section will address the future research needs with regard to SMPs.

What are SMPs?

It is well known that microorganisms produce organic substances during substrate degradation, growth and endogenous decay. The term SMPs as biological produced organic material, still, has been used by many authors without precise definition. This is rather due to the difficulty in identifying SMPs formation procedures and also to the complexities of effluent composition and especially tracing the origin of the mixture of compounds in a biological treatment system [20]. Boero et al. [21] stated that SMPs result “from intermediates or end products of substrate degradation and endogenous cell decomposition”, while most of the studies define SMPs as “the pool of organic compounds that result from substrate metabolism and biomass decay during the complete mineralization of simple substrates” [3, 13, 2224]. The inclusion of “during the complete mineralization of simple substrates” in the definition is open to some debate.

SMPs are sometimes the hard-biodegradable end-products of the incomplete microbial degradation of more complex compounds that can act as the substrates for another group of microorganisms in the aerobic or anaerobic chains. Chudoba [25] classified the SMPs produced by activated sludge microorganisms into three categories:
  1. 1.

    Compounds excreted by microorganisms owing to their interaction with the environment.

     
  2. 2.

    Compounds produced as a result of substrate metabolism and bacterial growth.

     
  3. 3.

    Compounds released during the lysis and degradation of microorganisms.

     

This classification system is used in wastewater process design, particularly from a process engineering point of view, but it does not address the biodegradability of non intermediate soluble microbial products. Engineers prefer Chudoba’s classification whereas microbiologists tend to classify SMPs formation into three categories: growth-synonymous; growth-associated and growth-independent [26, 27]. If we apply this classification to organic compounds produced by activated sludge, then growth-independent products are located in categories 1 and 3 of Chudoba’s classification while growth-synonymous and growth-associated products are placed in second category of Chudoba’s classification.

However recent researches classified the SMPs into two different categories based on the bacterial phase from which they were derived [28, 29]:
  1. 1.

    Utilization associated product (UAP), i.e. SMPs that are associated with substrate metabolism and biomass growth and are produced at a rate proportional to the rate of substrate utilization.

     
  2. 2.

    Biomass associated products (BAP), i.e. SMPs that are associated with biomass decay and are produced at a rate proportional to the concentration of biomass.

     

Using these categories they were able to successfully model substrate utilization, SMP formation and the removal of total soluble organic matter in biological treatment processes [4, 30].

The origin of SMPs

The complete list of the origin of SMPs is provided by Kuo [31]. He mentions the following factors as causes of SMPs release:
  1. 1.

    Concentration equilibrium: organisms excrete soluble organic materials to maintain concentration equilibrium across the cell membrane [32, 33]. Concentration equilibrium state chemical potential equilibrium which is the main cause of conditional stress around the cells that cause to excretion of soluble organic materials [34, 35]. Nossal et al. [36] indicated that microorganisms secrete SMPs in highconcentrations of salt to protect against osmotic pressure.

     
  2. 2.

    Starvation: bacteria SMPs during starvation as they must obtain energy for maintenance by metabolism of intracellular components or endogenous respiration when the substrate is essentially absent [37, 38]. Scientists considered all content of SMPs producing in starvation condition as biomass-associated products (BAP) and tried to investigate the impact of them on biological treatment system performance [4, 39].

     
  3. 3.

    Presence of energy source: the presence of an increased concentration of exogenous energy source can stimulate the excretion of SMPs [40].

     
  4. 4.

    Substrate-accelerated death: sudden discharge of a carbon and energy source to bacteria starved for carbon and energy may accelerate the death of some bacteria which results in production of SMPs [41].

     
  5. 5.

    Nutrients deficiency: if essential nutrients are present in very low concentrations, SMPs may be produced to scavenge the required nutrient [42].

     
  6. 6.

    Environmental stress: SMPs are produced in response to environmental stress, such as extreme temperature changes [43], pH variation [26], osmotic shocks [44],and salinity [45, 46]. Other researchers also speculate that SMPs are produced in response to toxic substances such as heavy metals [31, 47].

     
  7. 7.

    Normal bacterial growth and metabolism: SMPs, such as extracellular enzymes, are not only produced during stressed conditions but also during normal growth and metabolism, especially degradation of biodegradable hydrocarbons [48]. Amani et al. [49], furthermore, produced SMPs as a surfactant through the biological degradation of synthetic feed containing whey, crude oil and sucrose.

     
  8. 8.

    Endogenous decay: as mentioned SMPs have been classified into two groups based on the bacterial phase in which they are derived: the utilization associated products (UAP) derived during the original substrate in microbial growth and the biomass-associated products the BAPs generated in the endogenous phase [50].

     

The characteristics of SMPs

Bulk parameters that state overall performance of a treatment system in regard to SMPs have been studied well. The most of researches have focused on the global characteristics of SMPs such as distribution of molecular weights (MW), biodegradability and toxicity [51]. SMPs have a wide range of MW; determination of MW distribution of SMPs sometimes could be very informative and even help evaluating the efficiency of treatment process [52]. There is no standard method for determining the MW distribution of soluble organic compounds. This creates complexities in comparing results from different studies and only their relative MW measurements and trends could be evaluated. Materials size distributions of soluble organic compounds are determined either as a continuous distribution using gel permeation chromatography [53] or as a discrete distribution using ultrafiltration UF membranes in stirred cells [54]. The sizes of these soluble organics are referred to as apparent molecular weight in comparison with standard compounds of known MW [55].

Biodegradability of SMPs is important because it can present the effluent environmental risks and BOD level. Residues of SMPs in effluent could induce the formation of several toxic materials during some post-treatment steps such as chlorine disinfection.

SMPs are also characterized with considering the proportion of protein base SMP (SMPp) and carbohydrate base SMP (SMPc). While SMPp has generally a hydrophobic tendency, SMPc is more hydrophilic. Total organic carbon (TOC) level and more rarely specific ultraviolet absorbance (SUVA) are among the other measurements that can help SMP characterization. Aromaticity and hydrophobicity of SMPs can be determined by the measurement of the SUVA.

Zeta (ζ) potential and hydrophobicity can state electrostatic interaction of SMPs with membrane surface in MBRs and flocculation potential in activated sludge treatment process [56].

Treatment of SMPs

SMPs concentration in wastewater influent is negligible and they are generally produced during wastewater treatment process. This particularity makes their removal process different from other organic pollutants. Removal of SMPs from biological wastewater treatment systems is in theory possible using advanced techniques such as MBR; however it is inevitable that some SMPs remain in the effluent. SMPs are necessary for flocculation in activated sludge process [57], but they induce some inconvenient consequences in treatment process. The part of remained SMPs in effluent results in organic material discharge to the environment. Post- treatment method should be considered in treatment processes to remove the hard-biodegradable SMPs. These SMPs are also precursors for chlorinated organic compounds such as trihalomethanes (THMs) formation during effluent chlorination [27]. Several researchers have studied the treatability of SMPs with complementary treatment techniques, such as activated carbon adsorption and coagulation [58, 59]. Associated literatures with these mentioned techniques for removing SMPs have been listed in Table 1.
Table 1

Various techniques studied for treatment of SMPs and their corresponding literature

Treatment processes

Reference

Adsorption by activated carbon

[58, 60]

Filtration by membrane

[61, 62]

Adsorption by synthetic resin

[63, 64]

Ozonation

[65, 66]

Coagulation and electro-coagulation

[45, 67]

UV treatment

[68, 69]

Reviewing all of these literatures indicates that adsorption on granular activated carbon (GAC) combined with biologically induced degradation was the most effective method for removal of SMPs [70]. There are several investigations trying to improve conventional activated sludge process to reduce biopolymers content in effluents from biological treatment [71, 72]. Parkin and McCarty [73] applied several methods to remove soluble organic nitrogen from effluents, and found that the most efficient treatment process was granular activated carbon (GAC) adsorption (85% removal) and chemical precipitation using high concentrations of ferric chloride (70% removal). Afterward, Randtke and McCarty [74] carried out the feasibility study on diverse individual and combined wastewater treatment processes for the removal of residual soluble organics from aerobic treatment process effluent and again came to the conclusion that GAC adsorption was generally the most proficient. Schultz and Keinath [75] observed that nearly 50% of SMPs were adsorbed onto powdered activated carbon PAC, but only 4% of the adsorbed SMPs were biodegradable that demonstrates the refractory nature of the SMPs. Guo et al. [76] recently, proposed improved biological activated carbon (BAC) which is the combined O3-BAC and AC/O3-BAC processes to remove refractory organic matter from treated sewage effluent. They found that maximum dissolved organic carbon (DOC) removal efficiency was 40% during steady state ozonation step. In comparison with O3-BAC system, the AC/O3-BAC system degraded the effluent DOC more significantly.

Removal of SMPs produced in anaerobic wastewater treatment systems is more complicated. Post- treatment of anaerobic effluents with activated carbon conducted by Barker et al. [60], showed that low MW materials (i.e. MW<1 kDa) from anaerobic treatments were the most difficult to be adsorbed on GAC.

Conclusion

Despite all of these mentioned studies, the knowledge regarding SMPs is still under progress and more works is required to fully understand their contribution in each biological treatment process. However, based on this review the current state of the art on SMPs can be summarized as the following main points:
  • As a result of the complicated measuring procedures of SMPs, their definitions are somewhat uncertain and depend on what point of view is taken. The most widely accepted definition for SMPs which comes from an engineering perspective is “organic compounds produced during microorganism metabolism and biomass decay”. A basic operational definition is any soluble material that appears in the effluent while it was not present in the influent.

  • SMPs have been classified into two groups: substrate utilization associated products and biomass associated products. UAPs are associated with substrate metabolism and biomass growth and are produced at a rate proportional to the rate of substrate utilization, while BAP are associated with biomass decay and are produced at a rate proportional to the concentration of biomass.

  • SMPs are hardly biodegradable and the kinetic of their degradation is very slow.

  • SMPs can be removed from effluents using a variety of different technologies, but the most effective process is adsorption by granular activated carbon.

  • Discharging the SMPs could have deteriorating consequences on environment which needs developing the treatment processes undertaken for their removal. The solution lies on a collaboration between biologists and engineers. Biologists should generate more information on their production mechanisms, nature and properties, while the process engineers should be able to propose some solutions for their treatment in industrial plant scale.

Declarations

Acknowledgements

Authors would like to acknowledge the financial support of University of Tehran for this work under grant number 8104956/1/02. They, also, express their profound gratitude toward Sara Mafirad for her helps.

Authors’ Affiliations

(1)
Biotechnology Group, School of Chemical Engineering, College of Engineering, University of Tehran

References

  1. Gaffney PE, Heukelekian H: Biochemical oxidation of the lower fatty acids. Journal Water Pollution Control Federation. 1961, 11: 1169-1184.Google Scholar
  2. Jiang T, Myngheer S, De Pauw DJW, Spanjers H, Nopens ID, Kennedy M, Amy G, Vanrolleghem PA: Modelling the production and degradation of soluble microbial products (SMP) in membrane bioreactors (MBR). Water Res. 2008, 42: 4955-4964. 10.1016/j.watres.2008.09.037.View ArticleGoogle Scholar
  3. Schiener P, Nachaiyasit S, Stuckey DC: Production of soluble microbial products (SMP) in an anaerobic baffled reactor: composition, biodegradability and the effect of process parameters. Environ Technol. 1998, 19: 391-400. 10.1080/09593331908616694.View ArticleGoogle Scholar
  4. Tian Y, Chen L, Jiang T: Characterization and modeling of the soluble microbial products in membrane bioreactor. Sep Purif Technol. 2011, 76: 316-324. 10.1016/j.seppur.2010.10.022.View ArticleGoogle Scholar
  5. Zhou W, Wu B, She Q, Chi L, Zhang Z: Investigation of soluble microbial products in a full-scale UASB reactor running at low organic loading rate. Bioresour Technol. 2009, 100: 3471-3476. 10.1016/j.biortech.2009.03.006.View ArticleGoogle Scholar
  6. Aileen NLN, Albert SK: A mini-review of modeling studies on membrane bioreactor (MBR) treatment for municipal wastewaters. Desalination. 2007, 212: 261-281. 10.1016/j.desal.2006.10.013.View ArticleGoogle Scholar
  7. Ahn YT, Choi YK, Jeong HS, Chae SR, Shin HS: Modeling of extracellular polymeric substances and soluble microbial products production in a submerged membrane bioreactor at various SRTs. Water Sci Technol. 2006, 53: 209-216.View ArticleGoogle Scholar
  8. Lu SG, Imai T, Ukita M, Sekine M, Higuchi T, Fukagawa M: A model for membrane bioreactor process based on the concept of formation and degradation of soluble microbial products. Water Res. 2001, 35: 2038-2048. 10.1016/S0043-1354(00)00461-9.View ArticleGoogle Scholar
  9. Lu SG, Imai T, Ukita M, Sekine M, Higuchi T: Modeling prediction of membrane bioreactor process with the concept of soluble microbial product. Water Sci Technol. 2002, 46: 63-69.Google Scholar
  10. Ng ANL, Kim AS: A mini-review of modeling studies on membrane bioreactor (MBR) treatment for municipal wastewaters. Desalination. 2007, 212: 261-281. 10.1016/j.desal.2006.10.013.View ArticleGoogle Scholar
  11. Yoon SH, Kim HS, Yeom IT: The optimum operational condition of membrane bioreactor (MBR): cost estimation of aeration and sludge treatment. Water Res. 2004, 38: 37-46. 10.1016/j.watres.2003.09.001.View ArticleGoogle Scholar
  12. Kim M, Nakhla G: Comparative studies on membrane fouling between two membrane-based biological nutrient removal systems. J Membr Sci. 2009, 331: 91-99. 10.1016/j.memsci.2009.01.018.View ArticleGoogle Scholar
  13. Noguera DR, Araki N, Rittmann BE: Soluble microbial products (SMP) in anaerobic chemostats. Biotechnol Bioeng. 1994, 44: 1040-1047. 10.1002/bit.260440904.View ArticleGoogle Scholar
  14. Wu B, Zhou W: Investigation of soluble microbial products in anaerobic wastewater treatment effluents. J Chem Technol Biotechnol. 2010, 85: 1597-1603. 10.1002/jctb.2471.View ArticleGoogle Scholar
  15. Azami H, Sarrafzadeh MH, Mehrnia MR: Influence of sludge rheological properties on the membrane fouling in submerged membrane bioreactor. Desalin Water Treat. 2011, 34: 117-122. 10.5004/dwt.2011.2852.View ArticleGoogle Scholar
  16. Kornboonraks T, Lee SH: Factors affecting the performance of membrane bioreactor for piggery wastewater treatment. Bioresour Technol. 2009, 100: 2926-2932. 10.1016/j.biortech.2009.01.048.View ArticleGoogle Scholar
  17. Hosnani E, Nosrati M, Shojasadati SA: Role of extracellular polymeric substances in dewaterability of untreated, sonicated and digested waste activated sludge. Iran J Environ Health and Sci Eng. 2010, 7: 395-400.Google Scholar
  18. Le-Clech P, Chen V, Fane TAG: Fouling in membrane bioreactors used in wastewater treatment. J Membr Sci. 2006, 284: 17-53. 10.1016/j.memsci.2006.08.019.View ArticleGoogle Scholar
  19. Kimura K, Naruse T, Watanabe Y: Changes in characteristics of soluble microbial products in membrane bioreactors associated with different solid retention times: Relation to membrane fouling. Water Res. 2009, 43: 1033-1039. 10.1016/j.watres.2008.11.024.View ArticleGoogle Scholar
  20. Azami H, Mehrnia MR, Sarrafzadeh MH, Kazemzadeh M, Mafirad S, Mostoufi N: Membrane biofouling by soluble microbial products in a membrane bioreactor, 18th International congress of chemical and process engineering. 2008, Czech RepublicGoogle Scholar
  21. Boero VJ, Eckenfelder WW, Bowers AR: Soluble microbial product formation in biological systems. Water Sci Technol. 1991, 23: 1067-1076.Google Scholar
  22. Jiang T, Kennedy MD, De Schepper V, Nam SN, Nopens I, Vanrolleghem PA, Amy G: Characterization of Soluble Microbial Products and Their Fouling Impacts in Membrane Bioreactors. Environ Sci Technol. 2010, 44: 6642-6648. 10.1021/es100442g.View ArticleGoogle Scholar
  23. Park N, Kwon B, Kim IS, Cho J: Biofouling potential of various NF membranes with respect to bacteria and their soluble microbial products (SMP): characterizations, flux decline, and transport parameters. J Membr Sci. 2005, 258: 43-54. 10.1016/j.memsci.2005.02.025.View ArticleGoogle Scholar
  24. Trzcinski AP: PhD Thesis. The use of membrane bioreactors in the anaerobic digestion of the biodegradable fraction of municipal solid waste. 2009, London, UK: Imperial CollegeGoogle Scholar
  25. Chudoba J: Quantitative estimation in COD units of refractory organic compounds produced by activated sludge microorganisms. Water Res. 1985, 19: 37-43. 10.1016/0043-1354(85)90320-3.View ArticleGoogle Scholar
  26. De Aquino SF: PhD Thesis. Formation of soluble microbial products (SMPs) in an anaerobic reactor during stress conditions. 2004, London, UK: Imperial CollegeGoogle Scholar
  27. Namkung E, Rittmann BE: Effects of SMP on biofilm-reactor performance. J Environ Eng. 1988, 114: 199-210. 10.1061/(ASCE)0733-9372(1988)114:1(199).View ArticleGoogle Scholar
  28. Fenu A, Guglielmi G, Jimenez J, Spèrandio M, Saroj D, Lesjean B, Brepols C, Thoeye C, Nopens I: Activated sludge model (ASM) based modeling of membrane bioreactor (MBR) processes: a critical review with special regard to MBR specificities. Water Res. 2010, 44: 4272-4294. 10.1016/j.watres.2010.06.007.View ArticleGoogle Scholar
  29. Xie WM, Ni BJ, Seviour T, Sheng GP, Yu HQ: Characterization of autotrophic and heterotrophic soluble microbial product (SMP) fractions from activated sludge. Water Res. 2012, in pressGoogle Scholar
  30. Chen L, Tian Y, Cao C, Zhang S, Zhang S: Sensitivity and uncertainty analyses of an extended ASM3-SMP model describing membrane bioreactor operation. J Membr Sci. 2012, 389: 99-109.View ArticleGoogle Scholar
  31. Kuo WC: Ph.D. Thesis. Production of soluble microbial chelators and their impact on anaerobic treatment. 1993, Iowa City: University of IowaGoogle Scholar
  32. Payne JW: Peptides and microorganisms. Adv Microb Physiol. 1976, 13: 55-113.View ArticleGoogle Scholar
  33. Song B: Characterization of soluble microbial products produced by Cyanobacteria and wastewater bacteria, Ms Thesis. 2006, USA: Arizona State UniversityGoogle Scholar
  34. Azami H, Sarrafzadeh MH, Mehrnia MR: Fouling in membrane bioreactors with various concentrations of dead cells. Desalination. 2011, 278: 373-380. 10.1016/j.desal.2011.05.052.View ArticleGoogle Scholar
  35. Ni BJ, Yu HQ: Microbial products of activated sludge in biological wastewater treatment systems: a critical review. Crit Rev Environ Sci Technol. 2012, 42: 187-223. 10.1080/10643389.2010.507696.View ArticleGoogle Scholar
  36. Nossal NG, Heppel LA: The release of enzymes by osmotic shock from E. coli in exponential phase. J Biol Chem. 1966, 241: 3055-3062.Google Scholar
  37. Boylen CW, Ensign JC: Intracellular substrates for endogenous metabolism during long-term starvation of rod and spherical cells of arthrobacter crustallopoietes. J Bacteriol. 1970, 103: 578-587.Google Scholar
  38. Li ZH, Kuba T, Kusuda T: The influence of starvation phase on the properties and the development of aerobic granules. Enzym Microb Technol. 2006, 38: 670-674. 10.1016/j.enzmictec.2005.07.020.View ArticleGoogle Scholar
  39. Jiang T: Characterization and modeling of soluble microbial products in membrane bioreactor. 2007, Belgium: PhD thesis, Gent UniversityGoogle Scholar
  40. Thompson J: Characteristics and energy requirements of an A-aminoisobutyric acid transport system in Streptococcus lactis. J Bacteriol. 1976, 127: 719-730.Google Scholar
  41. Pirt SJ: Principles of Microbe and Cell Cultivation. 1975, Oxford: Blackwell ScientificGoogle Scholar
  42. Morel FMM: Principles of Aquatic Chemistry. 1983, New York: John Wiley InterscienceGoogle Scholar
  43. Feng H, Hu L, Shan D, Chengran F, He Y, Shen D: Effects of operational factors on soluble microbial products in a carrier anaerobic baffled reactor treating dilute wastewater. J Environ Sci. 2008, 20: 690-695. 10.1016/S1001-0742(08)62114-2.View ArticleGoogle Scholar
  44. Rogers D: Osmotic pools in Escherichia coli. Science. 1968, 159: 531-532. 10.1126/science.159.3814.531.View ArticleGoogle Scholar
  45. Azami H, Mehrnia MR, Sarrafzadeh MH, Mafirad S, Kazemzadeh M, Madaeni SS: Effect of cations on activated sludge characterization and membrane fouling in membrane bioreactor for waste water treatment. Journal of Chemical and Petroleum Engineering. 2010, 44: 1-8.Google Scholar
  46. Vyrides I, Stuckey DC: Adaptation of anaerobic biomass to saline conditions: Role of compatible solutes and extracellular polysaccharides. Enzym Microb Technol. 2009, 44: 46-51. 10.1016/j.enzmictec.2008.09.008.View ArticleGoogle Scholar
  47. Amiri S, Mehrnia MR, Azami H, Barzegari D, Shavandi M, Sarrafzadeh MH: Effect of heavy metals on fouling behavior in membrane bioreactors. Iran J Environ Health and Sci Eng. 2011, 7: 277-282.Google Scholar
  48. Saier MH, Feucht BU, Mc Caman MT: Regulation of intracellular adenosine cyclic 3′:5′-monophosphate levels in Escherichia coli and Salmonella typhimurium. J Biol Chem. 1975, 250: 7593-7601.Google Scholar
  49. Amani H, Haghighi M, Sarrafzadeh MH, Mehrnia MR, Shahmirzaee F: Optimization of the production of biosurfactant from iranian indigenous bacteria for the reduction of surface tension and enhanced oil recovery. Pet Sci Technol. 2011, 29: 301-311. 10.1080/10916460903393963.View ArticleGoogle Scholar
  50. Jarusutthirak C, Amy G: Role of soluble microbial products (SMP) in membrane fouling and flux decline. Environ Sci Technol. 2006, 40: 969-974. 10.1021/es050987a.View ArticleGoogle Scholar
  51. Dong B, Jiang S: Characteristics and behaviors of soluble microbial products in sequencing batch membrane bioreactors at various sludge retention times. Desalination. 2009, 243: 240-250. 10.1016/j.desal.2008.04.026.View ArticleGoogle Scholar
  52. Huang G, Jin G, Wu J, Liu Y: Effects of glucose and phenol on soluble microbial products (SMP) in sequencing batch reactor systems. Int Biodeterior Biodegrad. 2008, 62: 104-108. 10.1016/j.ibiod.2007.07.015.View ArticleGoogle Scholar
  53. Amy GL, Collins MR, Kuo CJ, King PH: Comparing gel permeation and ultrafilltration for the molecular weight characterization of aquatic organic matter. J Am Water Works Assoc. 1987, 79: 43-49.Google Scholar
  54. Shin HS, Kang ST: Characteristics and fates of soluble microbial products in ceramic membrane bioreactor at various sludge retention times. Water Res. 2003, 37: 121-127. 10.1016/S0043-1354(02)00249-X.View ArticleGoogle Scholar
  55. Logan BE, Jiang Q: Molecular size distributions of dissolved organic matter. J Environ Eng. 1990, 116: 1046-1062. 10.1061/(ASCE)0733-9372(1990)116:6(1046).View ArticleGoogle Scholar
  56. Chen L, Tian Y, Cao CQ, Zhang J, Li ZN: Interaction energy evaluation of soluble microbial products (SMP) on different membrane surfaces: role of the reconstructed membrane topology. Water Res. 2012, 46: 2693-2704. 10.1016/j.watres.2012.02.030.View ArticleGoogle Scholar
  57. Fallah N, Bonakdarpour B, Nasernejad B, Alavimoghaddam MR: The use of a submerged membrane bioreactor for the treatment of a styrene containing synthetic wastewater. Iran J Environ Health and Sci Eng. 2010, 7: 115-122.Google Scholar
  58. Poostchi AA, Mehrnia MR, Sarrafzadeh MH: Removal of dissolved organic carbon by multi-walled carbon nanotubes, powdered activated carbon and granular activated carbon. Research Journal of Chemistry and Environment. 2010, 14: 59-66.Google Scholar
  59. Remy M, Van der Marela P, Zwijnenburg A, Rulkens W, Temmink H: Low dose powdered activated carbon addition at high sludge retention times to reduce fouling in membrane bioreactors. Water:. 2009, 43: 345-350. 10.1016/j.watres.2008.10.033.Google Scholar
  60. Barker DJ, Mannucchi GA, Salvi SML, Stuckey DC: Characterisation of Soluble Residual Chemical Oxygen Demand (COD) in Anaerobic Wastewater Treatment Effluents. Water Res. 1999, 33: 2499-2510. 10.1016/S0043-1354(98)00489-8.View ArticleGoogle Scholar
  61. Mafirad S, Mehrnia MR, Azami H, Sarrafzadeh MH: Effects of biofilm formation on membrane performance in submerged membrane bioreactors. Biofouling. 2011, 27: 477-485. 10.1080/08927014.2011.584619.View ArticleGoogle Scholar
  62. Ng CA, Sun D, Zhang J, Chua HC, Bing W, Tay S, Fane A: Strategies to improve the sustainable operation of membrane bioreactors. Proceedings of the International Desalination Association Conference. 2005, SingaporeGoogle Scholar
  63. Dean RB: Processes for water reclamation. Waste Management and Research. 1991, 9: 425-430.View ArticleGoogle Scholar
  64. Rueffer H, Griesing H: Industrial process water from biologically pretreated effluents purified by polymeric adsorbents. Dechema Monographien. 1980, 86: 321-347.Google Scholar
  65. Eremektar G, Selcuk H, Meric S: Investigation of the relation between COD fractions and the toxicity in a textile finishing industry wastewater: effect of preozonation. Desalination. 2007, 211: 314-320. 10.1016/j.desal.2006.02.096.View ArticleGoogle Scholar
  66. Sun FY, Wang XM, Li XY: Effect of biopolymer clusters on the fouling property of sludge from a membrane bioreactor (MBR) and its control by ozonation. Process Biochem. 2011, 46: 162-167. 10.1016/j.procbio.2010.08.003.View ArticleGoogle Scholar
  67. Ibeid S, Elektorowicz M, Oleszkiewicz JA: Impact of electro-coagulation on the fate of soluble microbial products (SMP) in submerged membrane electro-bioreactor (SMEBR). Annual Conference - Canadian Society for Civil Engineering (CSCE). 2010, 1: 634-640.Google Scholar
  68. Marsolek MD, Torres CI, Hausner M, Rittmann BE: Intimate coupling of photocatalysis and biodegradation in a photocatalytic circulating-bed biofilm reactor. Biotechnol Bioeng. 2008, 101: 83-92. 10.1002/bit.21889.View ArticleGoogle Scholar
  69. Zhang Y, Wang L, Rittmann BE: Integrated photocatalytic-biological reactor for accelerated phenol mineralization. Appl Microbiol Biotechnol. 2010, 86: 1977-1985. 10.1007/s00253-010-2458-x.View ArticleGoogle Scholar
  70. Booth SDJ: PhD Thesis. Formation and removal of ozonation By -products in drinking water biofil ters. 1998, Waterloo, Canada: University of WaterlooGoogle Scholar
  71. Mafirad S, Mehrnia MR, Sarrafzadeh MH: Effect of membrane characteristics on the performance of membrane bioreactors for oily wastewater treatment. Water Sci Technol. 2012, 64: 1154-1160.View ArticleGoogle Scholar
  72. Rasouli Kenari H, Sarrafzadeh MH, Tavakoli O: An investigation on the nitrogen content of a petroleum refinery wastewater and its removal by biological treatment. Iran J Environ Health and Sci Eng. 2010, 7: 391-394.Google Scholar
  73. Parkin GF, McCarty PL: Characteristics and removal of soluble organic nitrogen in treated effluents. Progress in Water Technology. 1975, 7: 435-445.Google Scholar
  74. Randtke SJ, McCarty PL: Removal of soluble secondary effluent organics. J Environ Eng. 1979, 105: 727-743.Google Scholar
  75. Schultz JR, Keinath TM: Powdered activated carbon treatment process mechanisms. J WPCF. 1984, 56: 143-151.Google Scholar
  76. Guo J, Wang BG, Sheng F, Ying FF: Effluent organic matter removal during advanced wastewater treatment process: O3-BAC and AC/O3-BAC, Second International Conference on Mechanic Automation and Control Engineering (MACE). 2001, China: Inner MongoliaGoogle Scholar

Copyright

© Azami et al.; licensee BioMed Central Ltd. 2012

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Advertisement