Skip to main content

Advertisement

Log in

Antibiofilm activity of Bacillus pumilus SW9 against initial biofouling on microfiltration membranes

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

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

    Article  CAS  Google Scholar 

  • Aoki SK, Pamma R, Hernday AD, Bickham JE, Braaten BA, Low DA (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309:1245

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Chao Y, Zhang T (2011) Growth behaviors of bacteria in biofouling cake layer in a dead-end microfiltration system. Bioresour Technol 102:1549–1555

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Das P, Mukherjee S, Sen R (2009) Antiadhesive action of a marine microbial surfactant. Colloids Surf B Biointerfaces 71:183–186

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Dusane DH, Nancharaiah YV, Zinjarde SS, Venugopalan VP (2010) Rhamnolipid mediated disruption of marine Bacillus pumilus biofilms. Colloids Surf B Biointerfaces 81:242–248

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Feng L, Li X, Du G, Chen J (2009) Adsorption and fouling characterization of Klebsiella oxytoca to microfiltration membranes. Proc Biochem 44:1289–1292

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Holt JG, Krieg NR, Sneath PH, Staley JT, Williams ST (1994) International edition: Bergey's manual of determinative bacteriology. Williams & Wilkins, Baltimore

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Simoes LC, Simoes M, Vieira MJ (2007) Biofilm interactions between distinct bacterial genera isolated from drinking water. Appl Environ Microbiol 73:6192–6200

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xiong Y, Liu Y (2010) Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling. Appl Microbiol Biotechnol 86:825–837

    Article  CAS  PubMed  Google Scholar 

  • Xu W, Chellam S (2005) Initial stages of bacterial fouling during dead-end microfiltration. Environ Sci Technol 39:6470–6476

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xin Yu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 25.8 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-4991-x

Keywords

Navigation