Abstract
Quorum sensing gives rise to biofilm formation on the membrane surface, which in turn causes a loss of water permeability in membrane bioreactors (MBRs) for wastewater treatment. Enzymatic quorum quenching was reported to successfully inhibit the formation of biofilm in MBRs through the decomposition of signal molecules, N-acyl homoserine lactones (AHLs). The aim of this study was to elucidate the mechanisms of quorum quenching in more detail in terms of microbial population dynamics and proteomics. Microbial communities in MBRs with and without a quorum quenching enzyme (acylase) were analyzed using pyrosequencing and compared with each other. In the quorum quenching MBR, the rate of transmembrane pressure (TMP) rise-up was delayed substantially, and the proportion of quorum sensing bacteria with AHL-like autoinducers (such as Enterobacter, Pseudomonas, and Acinetobacter) also decreased in the entire microbial community of mature biofilm in comparison to that in the control MBR. These factors were attributed to the lower production of extracellular polymeric substances (EPS), which are known to play a key role in the formation of biofilm. Proteomic analysis using the Enterobacter cancerogenus strain ATCC 35316 demonstrates the possible depression of protein expression related to microbial attachments to solid surfaces (outer membrane protein, flagellin) and the agglomeration of microorganisms (ATP synthase beta subunit) with the enzymatic quorum quenching. It has been argued that changes in the microbial population, EPS and proteins via enzymatic quorum quenching could inhibit the formation of biofilm, resulting in less biofouling in the quorum quenching MBR.
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References
Abbas A, Scully N, Adams C (2007) A role for TonB1 in biofilm formation and quorum sensing in Pseudomonas aeruginosa. FEMS Microbiol Lett 274(2):269–278
Ahmadian A, Ehn M, Hober S (2006) Pyrosequencing: history, biochemistry and future. Clin Chim Acta 363(1–2):83–94
Ahmed NA, Petersen FC, Scheie AA (2009) AI-2/LuxS is involved in increased biofilm formation by Streptococcus intermedius in the presence of antibiotics. Antimicrob Agents Ch 53(10):4258–4263
Atkinson S, Goldstone RJ, Joshua GWP (2011) Biofilm development on Caenorhabditis elegans by Yersiniais facilitated by quorum sensing-dependent repression of Type III secretion. Plos Pathog 7(1).
Choi E, Yun Z, Park Y (2001) Extracellular polymeric substances in relation to nutrient removal from a sequencing batch biofilm reactor. Water Sci Technol 43(6):185–192
Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, PRIMER-E Ltd.
Clemmer KM, Bonomo RA, Rather PN (2011) Genetic analysis of surface motility in Acinetobacter baumannii. Microbiology-Sgm 157:2534–2544
Dobretsov S, Teplitski M, Paul V (2011) Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25(5):413–427
Fuqua WC, Greenberg EP (2002) Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3(9):685–695
Fuqua WC, Winans SC (1996) Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes. J Bacteriol 178(2):435–440
Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria—the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176(2):269–275
Giraud C, Ruer S, Bernard C (2010) Biological ‘glue’ and ‘Velcro’: molecular tools for adhesion and biofilm formation in the hairy and gluey bug Pseudomonas aeruginosa. Env Microbiol Rep 2(3):343–358
Hasona A, Zuobi-Hasona K, Crowley PJ (2007) Membrane composition changes and physiological adaptation by Streptococcus mutans signal recognition particle pathway mutants. J Bacteriol 189(4):1219–1230
Jahangir D, Oh HS, Kim SR, Park PK, Lee CH, Lee JK (2012) Specific location of encapsulated quorum quenching bacteria for biofouling control in an external submerged membrane bioreactor. J Membr Sci 411–412:130–136
Kreft JU, Wimpenny JWT (2001) Effect of EPS on biofilm structure and function as revealed by an individual-based model of biofilm growth. Water Sci Technol 43(6):135–141
Labbate M, Zhu H, Thung L (2007) Quorum-sensing regulation of adhesion in Serratia marcescens MG1 is surface dependent. J Bacteriol 189(7):2702–2711
Langille SE, Geesey GG, Weiner RM (2000) Polysaccharide-specific probes inhibit adhesion of Hyphomonas rosenbergii strain VP-6 to hydrophilic surfaces. J Ind Microbiol Biot 25(2):81–85
Lim S, Kim S, Yeon KM, Sang BI, Chun J, Lee CH (2012) Correlation between microbial community structure and biofouling in a laboratory scale membrane bioreactor with synthetic wastewater. Desalination 287:209–215
Mohamed NM, Cicirelli EM, Kan JJ, Chen F, Fuqua WC, Hill RT (2008) Diversity and quorum-sensing signal production of Proteobacteria associated with marine sponges. Environ Microbiol 10(1):75–86
Oh HS, Yeon KM, Yang CS, Kim SR, Lee CH, Park SY, Han JY, Lee JK (2012) Control of membrane biofouling in MBR for wastewater treatment by quorum quenching bacteria encapsulated in microporous membrane. Environ Sci Techno 46(9):4877–4884
Okabe S, Nielsen PH, Jones WL (1994) Estimation of cellular and extracellular carbon contents in sulfate-reducing bacteria biofilms by lipopolysaccharide assay and epifluorescence microscopic technique. Water Res 28(11):2263–2266
Sauer K, Camper AK (2001) Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J Bacteriol 183(22):6579–6589
Sawasdidoln C, Taweechaisupapong S, Sermswan RW (2010) Growing Burkholderia pseudomallei in biofilm stimulating conditions significantly induces antimicrobial resistance. PLoS One 5(2)
Sharma VK, Bearson SMD, Bearson BL (2010) Evaluation of the effects of sdiA, a luxR homologue, on adherence and motility of Escherichia coil O157:H7. Microbiology-Sgm 156:1303–1312
American Public Health Association (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, Washington
Tashiro Y, Nomura N, Nakao R (2008) Opr86 is essential for viability and is a potential candidate for a protective antigen against biofilm formation by Pseudomonas aeruginosa. J Bacteriol 190(11):3969–3978
Vanoyan N, Walker SL, Gillor O (2010) Reduced bacterial deposition and attachment by quorum-sensing inhibitor 4-Nitro-pyridine-N-oxide: the role of physicochemical effects. Langmuir 26(14):12089–12094
Wen ZT, Nguyen AH, Bitoun JP (2011) Transcriptome analysis of LuxS-deficient Streptococcus mutans grown in biofilms. Molecular Oral Microbiology 26(1):2–18
Williams P, Winzer K, Chan W, Camara M (2007) Look who’s talking: communication and quorum sensing in the bacterial world. Philos Trans R SocLond B BiolSci 362(1483):1119–1134
Wolfgang MC, Jyot J, Goodman AL (2004) Pseudomonas aeruginosa regulates flagellin expression as part of a global response to airway fluid from cystic fibrosis patients. Proc Natl Acad Sci USA 101(17):6664–6668
Xiong YH, Liu Y (2010) Involvement of ATP and Autoinducer-2 in aerobic granulation. Biotechnol Bioeng 105(1):51–58
Xu F, Byun T, Dussen HJ, Duke KR (2003) Degradationof N-acylhomoserine lactones, the bacterial quorum-sensingmolecules, by acylase. J Biotechnol 101:89–96
Yeon KM, Cheong WS, Oh HS (2009a) Quorum sensing: a new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environ Sci Technol 43(2):380–385
Yeon KM, Lee CH, Kim J (2009b) Magnetic enzyme carrier for effective biofouling cntrol in the mmbrane boreactor bsed on ezymatic quorum quenching. Environ Sci Technol 43(19):7403–7409
Zhu XN, Long F, Chen YH (2008) A putative ABC transporter is involved in negative regulation of biofilm formation by Listeria monocytogenes. Appl Environ Microbiol 74(24):7675–7683
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This work was supported by the National Research Foundation of Korea (NRF) grants funded by the government (MEST; No. 2010-0018903 and No. 2009-0089695).
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Kim, HW., Oh, HS., Kim, SR. et al. Microbial population dynamics and proteomics in membrane bioreactors with enzymatic quorum quenching. Appl Microbiol Biotechnol 97, 4665–4675 (2013). https://doi.org/10.1007/s00253-012-4272-0
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DOI: https://doi.org/10.1007/s00253-012-4272-0