Abstract
Membrane biofouling, resulting from biofilm formation on the membrane, has become the main obstacle hindering wider application of membrane technology. Initial biofouling proves to be crucial which involves early stages of microbial adhesion and biofilm formation. Biological control of microbial attachment seems to be a promising strategy due to its high efficiency and eco-friendliness. The present study investigated the effects of a bacterium Bacillus pumilus SW9 on controlling the initial fouling formed by four target bacterial strains which were pioneer species responsible for biofouling in membrane bioreactors, using microfiltration membranes as the abiotic surfaces. The results suggested that strain SW9 exhibited excellent antibiofilm activity by decreasing the attached biomass of target strains. The production of extracellular polysaccharides and proteins by four target strains was also reduced. A distinct improvement of permeate flux in dead-end filtration systems was achieved when introducing strain SW9 to microfiltration experiments. Scanning electron microscopy and confocal laser scanning microscopy were performed to further ascertain significant changes of the biofouling layers. A link between biofilm inhibition and initial biofouling mitigation was thus provided, suggesting an alternatively potential way to control membrane biofouling through bacterial interactions.
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References
Agarwal A, Xu H, Ng WJ, Liu Y (2012) Biofilm detachment by self-collapsing air microbubbles: a potential chemical-free cleaning technology for membrane biofouling. J Mater Chem 22:2203–2207
Aoki SK, Pamma R, Hernday AD, Bickham JE, Braaten BA, Low DA (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309:1245
Aryal R, Lebegue J, Vigneswaran S, Kandasamy J, Grasmick A (2009) Identification and characterisation of biofilm formed on membrane bio-reactor. Sep Purif Technol 67:86–94
Blanpain-Avet P, Faille C, Delaplace G, Bénézech T (2011) Cell adhesion and related fouling mechanism on a tubular ceramic microfiltration membrane using Bacillus cereus spores. J Membr Sci 385–386:200–216
Burmolle M, Webb JS, Rao D, Hansen LH, Sorensen SJ, Kjelleberg S (2006) Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 72:3916–3923
Chao Y, Zhang T (2011) Growth behaviors of bacteria in biofouling cake layer in a dead-end microfiltration system. Bioresour Technol 102:1549–1555
Chellam S, Cogan N (2011) Colloidal and bacterial fouling during constant flux microfiltration: comparison of classical blocking laws with a unified model combining pore blocking and EPS secretion. J Membr Sci 382:148–157
Chen W, Westerhoff P, Leenheer JA, Booksh K (2003) Fluorescence excitation–emission matrix regional integration to quantify spectra for dissolved organic matter. Environ Sci Technol 37:5701–5710
Chen MY, Lee DJ, Yang Z, Peng X, Lai J (2006) Fluorescent staining for study of extracellular polymeric substances in membrane biofouling layers. Environ Sci Technol 40:6642–6646
Das P, Mukherjee S, Sen R (2008) Antimicrobial potential of a lipopeptide biosurfactant derived from a marine Bacillus circulans. J Appl Microbiol 104:1675–1684
Das P, Mukherjee S, Sen R (2009) Antiadhesive action of a marine microbial surfactant. Colloids Surf B Biointerfaces 71:183–186
Dheilly A, Soum-Soutera E, Klein GL, Bazire A, Compere C, Haras D, Dufour A (2010) Antibiofilm activity of the marine bacterium Pseudoalteromonas sp. strain 3J6. Appl Environ Microbiol 76:3452–3461
Diagne F, Malaisamy R, Boddie V, Holbrook RD, Eribo B, Jones KL (2012) Polyelectrolyte and silver nanoparticle modification of microfiltration membranes to mitigate organic and bacterial fouling. Environ Sci Technol 46:4025–4033
Dusane DH, Nancharaiah YV, Zinjarde SS, Venugopalan VP (2010) Rhamnolipid mediated disruption of marine Bacillus pumilus biofilms. Colloids Surf B Biointerfaces 81:242–248
Dusane DH, Pawar VS, Nancharaiah Y, Venugopalan V, Kumar AR, Zinjarde SS (2011) Anti-biofilm potential of a glycolipid surfactant produced by a tropical marine strain of Serratia marcescens. Biofouling 27:645–654
Feng L, Li X, Du G, Chen J (2009) Adsorption and fouling characterization of Klebsiella oxytoca to microfiltration membranes. Proc Biochem 44:1289–1292
Gao D, Fu Y, Tao Y, Li X, Xing M, Gao X, Ren N (2011) Linking microbial community structure to membrane biofouling associated with varying dissolved oxygen concentrations. Bioresour Technol 102:5626–5633
Guo F, Zhang SH, Yu X, Wei B (2011) Variations of both bacterial community and extracellular polymers: the inducements of increase of cell hydrophobicity from biofloc to aerobic granule sludge. Bioresour Technol 102:6421–6428
Haber M, Carbone M, Mollo E, Gavagnin M, Ilan M (2011) Chemical defense against predators and bacterial fouling in the Mediterranean sponges Axinella polypoides and A. verrucosa. Mar Ecol Prog Ser 422:113–122
Holt JG, Krieg NR, Sneath PH, Staley JT, Williams ST (1994) International edition: Bergey's manual of determinative bacteriology. Williams & Wilkins, Baltimore
Huang LN, De Wever H, Diels L (2008) Diverse and distinct bacterial communities induced biofilm fouling in membrane bioreactors operated under different conditions. Environ Sci Technol 42:8360–8366
Kim JH, Choi DC, Yeon KM, Kim SR, Lee CH (2011) Enzyme-immobilized nanofiltration membrane to mitigate biofouling based on quorum quenching. Environ Sci Technol 45:1601–1607
Korenblum E, Sebastián G, Paiva M, Coutinho CMLM, Magalhães FCM, Peyton B, Seldin L (2008) Action of antimicrobial substances produced by different oil reservoir Bacillus strains against biofilm formation. Appl Microbiol Biotechnol 79:97–103
Miura Y, Watanabe Y, Okabe S (2007) Membrane biofouling in pilot-scale membrane bioreactors (MBRs) treating municipal wastewater: impact of biofilm formation. Environ Sci Technol 41:632–638
Nithya C, Begum MF, Pandian SK (2010) Marine bacterial isolates inhibit biofilm formation and disrupt mature biofilms of Pseudomonas aeruginosa PAO1. Appl Microbiol Biotechnol 88:341–358
Nithya C, Devi MG, Pandian SK (2011) A novel compound from the marine bacterium Bacillus pumilus S6-15 inhibits biofilm formation in Gram-positive and Gram-negative species. Biofouling 27:519–528
Okamura D, Mori Y, Hashimoto T, Hori K (2010) Effects of microbial degradation of biofoulants on microfiltration membrane performance in a membrane bioreactor. Environ Sci Technol 44:8644–8648
Pang CM, Hong P, Guo H, Liu WT (2005) Biofilm formation characteristics of bacterial isolates retrieved from a reverse osmosis membrane. Environ Sci Technol 39:7541–7550
Rivardo F, Turner R, Allegrone G, Ceri H, Martinotti M (2009) Anti-adhesion activity of two biosurfactants produced by Bacillus spp. prevents biofilm formation of human bacterial pathogens. Appl Microbiol Biotechnol 83:541–553
Seo H, Kim J, Jung J, Jin HM, Jeon CO, Park W (2012) Complexity of cell–cell interactions between Pseudomonas sp. AS1 and Acinetobacter oleivorans DR1: metabolic commensalism, biofilm formation and quorum quenching. Res Microbiol 163(3):173–181
Sheng GP, Yu HQ (2006) Characterization of extracellular polymeric substances of aerobic and anaerobic sludge using three-dimensional excitation and emission matrix fluorescence spectroscopy. Water Res 40:1233–1239
Siddiqui MF, Sakinah M, Ismail A, Matsuura T, Zularisam A (2012) The anti-biofouling effect of Piper betle extract against Pseudomonas aeruginosa and bacterial consortium. Desalination 288:24–30
Simoes LC, Simoes M, Vieira MJ (2007) Biofilm interactions between distinct bacterial genera isolated from drinking water. Appl Environ Microbiol 73:6192–6200
Teodósio JS, Simões M, Melo LF, Mergulhão FJ (2011) Flow cell hydrodynamics and their effects on E. coli biofilm formation under different nutrient conditions and turbulent flow. Biofouling 27:1–11
Thenmozhi R, Nithyanand P, Rathna J, Karutha Pandian S (2009) Antibiofilm activity of coral-associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunol Med Microbiol 57:284–294
Wu Z, Ye C, Guo F, Zhang S, Yu X (2013) Evidence for broad-spectrum biofilm inhibition by a bacterium Bacillus sp. strain SW9. Appl Environ Microbiol 79:1735–1738
Xiong Y, Liu Y (2010) Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling. Appl Microbiol Biotechnol 86:825–837
Xu W, Chellam S (2005) Initial stages of bacterial fouling during dead-end microfiltration. Environ Sci Technol 39:6470–6476
Yao M, Ladewig B, Zhang K (2011) Identification of the change of soluble microbial products on membrane fouling in membrane bioreactor (MBR). Desalination 278:126–131
Yeon KM, Cheong WS, Oh HS, Lee WN, Hwang BK, Lee CH, Beyenal H, Lewandowski Z (2009) Quorum sensing: a new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environ Sci Technol 43:380–385
Yu GH, Tang Z, Xu YC, Shen QR (2011) Multiple fluorescence labeling and two dimensional FTIR-13C NMR heterospectral correlation spectroscopy to characterize extracellular polymeric substances in biofilms produced during composting. Environ Sci Technol 45:9224–9231
Zaky A, Escobar I, Motlagh AM, Gruden C (2012) Determining the influence of active cells and conditioning layer on early stage biofilm formation using cellulose acetate ultrafiltration membranes. Desalination 286:296–303
Zhang K, Choi H, Dionysiou DD, Sorial GA, Oerther DB (2006) Identifying pioneer bacterial species responsible for biofouling membrane bioreactors. Environ Microbiol 8:433–440
Zuo R, Örnek D, Syrett B, Green R, Hsu CH, Mansfeld F, Wood T (2004) Inhibiting mild steel corrosion from sulfate-reducing bacteria using antimicrobial-producing biofilms in Three-Mile-Island process water. Appl Microbiol Biotechnol 64:275–283
Acknowledgments
This work was supported by the Knowledge Innovation Project (KZCX2-YW-JC406) and the 100 talent Program of Chinese Academy of Sciences, National High-Tech R&D Program of China (2012AA062607) and National Natural Science Foundation of China (NSFC, 50678080 & 51078343). The authors are grateful to all those who had kindly provided assistance.
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Zhang, Y., Yu, X., Gong, S. et al. Antibiofilm activity of Bacillus pumilus SW9 against initial biofouling on microfiltration membranes. Appl Microbiol Biotechnol 98, 1309–1320 (2014). https://doi.org/10.1007/s00253-013-4991-x
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DOI: https://doi.org/10.1007/s00253-013-4991-x