Skip to main content

Advertisement

Log in

Extracellular polymeric substances mediate the coaggregation of aquatic biofilm-forming bacteria

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Coaggregation, a phenomenon contributing to biofilm formation, occurs among biofilm bacteria from different aquatic environments. However, not much is known about molecules involved in aggregation. In this study, freshwater, estuarine and marine biofilm bacteria were evaluated for aggregation capabilities, and their cell-bound extracellular polymeric substances (CB-EPS), known to play an important role in biofilm formation, were characterized for functional groups, and sugar composition via Fourier-transform infrared spectroscopy and high-pressure liquid chromatography. Biofilm-forming potential of estuarine and freshwater biofilm bacteria was higher as indicated by their coaggregation scores, attributed to CB-EPS with distinct sugar types, compared to marine. Most of the biofilm bacteria lost their ability to coaggregate after removal of CB-EPS, indicating its importance in coaggregation. Estuarine (Bacillus indicus, Bacillus cereus), and freshwater (Exiguobacterium spp., B. cereus) bacterial pairs, retained their aggregation capability probably via expression of lipids and proteins, suggesting their ability to rebuild themselves by expressing specific biomolecules under stressed conditions. A similar expression pattern was observed when these strains were exposed to abrupt salinity change (environmental stressor), indicating modulation of cell surface chemistry as a strategy to protect biofilm bacteria in harsh conditions. Unravelling role of these biomolecules as cues for settlement of macrofoulers is a step ahead.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abisado, R. G., S. Benomar, J. R. Klaus, A. A. Dandekar & J. R. Chandler, 2018. Bacterial quorum sensing and microbial community interactions. MBio 9(3): e02331-17.

    PubMed  PubMed Central  Google Scholar 

  • Adav, S. S., D. J. Lee & J. Y. Lai, 2008. Intergeneric coaggregation of strains isolated from phenol-degrading aerobic granules. Applied Microbiology and Biotechnology 79: 657–661.

    CAS  PubMed  Google Scholar 

  • Andrews, J. S., S. A. Rolfe, W. E. Huang, J. D. Scholes & S. A. Banwart, 2010. Biofilm formation in environmental bacteria is influenced by different macromolecules depending on genus and species. Environmental Microbiology 12: 2496–2507.

    CAS  PubMed  Google Scholar 

  • Azeredo, J. & R. Oliveira, 2000. The role of exopolymers in the attachment of Sphingomonas paucimobilis. Biofouling 16: 59–67.

    CAS  Google Scholar 

  • Bahulikar, R. A. & P. G. Kroth, 2008. The complex extracellular polysaccharides of mainly chain-forming freshwater diatom species from epilithic biofilms. Journal of Phycology 44: 1465–1475.

    CAS  PubMed  Google Scholar 

  • Basson, A., L. A. Flemming & H. Y. Chenia, 2008. Evaluation of adherence, hydrophobicity, aggregation, and biofilm development of Flavobacterium johnsoniae-like isolates. Microbial Ecology 55: 1–14.

    CAS  PubMed  Google Scholar 

  • Bengtsson, G., 1991. Bacterial exopolymer and PHB production in fluctuating ground-water habitats. FEMS Microbiology and Ecology 86: 15–24.

    CAS  Google Scholar 

  • Bhasker, P.V., 2003. Studies on some of aspects of marine microbial polysaccharides. PhD Thesis, Goa University

  • Bowden, G. H. W., D. C. Ellwood & I. R. Hamilton, 1979. Microbial Ecology of the Oral Cavity. Advances in Microbial Ecology. Springer, Boston: 135–217.

    Google Scholar 

  • Bramhachari, P. & S. Dubey, 2006. Isolation and characterization of exopolysaccharide produced by Vibrio harveyi strain VB23. Letters in Applied Microbiology 43: 571–577.

    CAS  PubMed  Google Scholar 

  • Buswell, C. M., Y. M. Herlihy, P. D. Marsh, C. W. Keevil & S. A. Leach, 1997. Coaggregation amongst aquatic biofilm bacteria. Journal of Applied Microbiology 83: 477–484.

    Google Scholar 

  • Cai, W., L. Xie, Y. Chen & H. Zhang, 2013. Purification, characterization and anticoagulant activity of the polysaccharides from green tea. Carbohydrate Polymers 92: 1086–1090.

    CAS  PubMed  Google Scholar 

  • Camilli, A. & B. L. Bassler, 2006. Bacterial small-molecule signaling pathways. Science 311: 1113–1116.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Casillo, A., R. Lanzetta, M. Parrilli & M. M. Corsaro, 2018. Exopolysaccharides from marine and marine extremophilic bacteria: structures, properties, ecological roles and applications. Marine Drugs 16(2): 69.

    PubMed Central  Google Scholar 

  • Cavalcante, T. T. A., N. S. A. Firmino, F. A. S. Tajra, C. R. de Andrade & R. A. Costa, 2014. Plant lectins as alternative tools against bacterial biofilms. African Journal of Microbiology Research 8: 2555–2564.

    CAS  Google Scholar 

  • Cheng, Y. P., P. Zhang, J. S. Guo, F. Fang, X. Gao & C. Li, 2013. Functional groups characteristics of EPS in biofilm growing on different carriers. Chemosphere 92: 633–638.

    Google Scholar 

  • Cheng, Z., X. Meng, H. Wang, M. Chen & M. Li, 2014. Isolation and characterization of broad spectrum coaggregating bacteria from different water systems for potential use in bioaugmentation. PLoS ONE 9(4): e94220.

    PubMed  PubMed Central  Google Scholar 

  • Cheung, H. Y., S. Q. Sun, B. Sreedhar, W. M. Ching & P. A. Tanner, 2000. Alterations in extracellular substances during the biofilm development of Pseudomonas aeruginosa on aluminium plates. Journal of Applied Microbiology 89: 100–106.

    CAS  PubMed  Google Scholar 

  • Cisar, J. O., P. E. Kolenbrander & F. C. McIntire, 1979. Specificity of coaggregation reactions between human oral streptococci and strains of Actinomyces viscosus or Actinomyces naeslundii. Infection and Immunity 24: 742–752.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke, K. R. & R. M. Warwick, 1994. Similarity-based testing for community pattern: the 2-way layout with no replication. Marine Biology 118: 167–176.

    Google Scholar 

  • Dang, H. & C. R. Lovell, 2016. Microbial surface colonization and biofilm development in marine environments. Microbiology and Molecular Biology Reviews 80: 91–138.

    CAS  PubMed  Google Scholar 

  • de Carvalho, C. C. C. R., 2018. Marine biofilms: a successful microbial strategy with economic implications. Frontiers in Marine Science 5: 126.

    Google Scholar 

  • De Gregoris, T. B., L. Khandeparker, A. C. Anil, E. Mesbahi, J. G. Burgess & A. S. Clare, 2012. Characterisation of the bacteria associated with barnacle, Balanus amphitrite, shell and their role in gregarious settlement of cypris larvae. Journal of Experimental Marine Biology and Ecology 413: 7–12.

    Google Scholar 

  • Decho, A. W., 1990. Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes. Oceanography and Marine Biology, An Annual Review 28: 73–153.

    Google Scholar 

  • Decho, A. W. & T. Gutierrez, 2017. Microbial extracellular polymeric substances (EPSs) in ocean systems. Frontiers in Microbiology 8: 922.

    PubMed  PubMed Central  Google Scholar 

  • Deepika, G., E. Karunakaran, C. R. Hurley, C. A. Biggs & D. Charalampopoulos, 2012. Influence of fermentation conditions on the surface properties and adhesion of Lactobacillus rhamnosus GG. Microbial Cell Factories 11: 116.

    PubMed  PubMed Central  Google Scholar 

  • Diomandé, S. E., M. H. Guinebretière, V. Broussolle & J. Brillard, 2015. Role of fatty acids in Bacillus environmental adaptation. Frontiers in Microbiology 6: 813.

    PubMed  PubMed Central  Google Scholar 

  • Dobretsov, S. & D. Rittschof, 2020. Love at first taste: induction of larval settlement by marine microbes. International Journal of Molecular Sciences 21(3): 731.

    CAS  PubMed Central  Google Scholar 

  • Dobretsov, S., M. Teplitski & V. Paul, 2009. Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25: 413–427.

    CAS  PubMed  Google Scholar 

  • D’Souza, F., 2004. Study on bacterial exopolysaccharides and their role in adhesion and corrosion. Doctoral Dissertation, Goa University.

  • Ellwood, D. C. & D. W. Tempest, 1972. Effects of environment on bacterial wall content and composition. Advances in Microbial Physiology 7: 83–117.

    CAS  Google Scholar 

  • Elnahas, M., M. Amin, M. Hussein, V. Shanbhag, A. Ali & J. Wall, 2017. Isolation, characterization and bioactivities of an extracellular polysaccharide produced from Streptomyces sp MOE6. Molecules 22: 1396.

    PubMed Central  Google Scholar 

  • Fang, F., W. T. Lu, Q. Shan & J. S. Cao, 2014. Characteristics of extracellular polymeric substances of phototrophic biofilms at different aquatic habitats. Carbohydrate Polymers 106: 1–6.

    CAS  PubMed  Google Scholar 

  • Freitas, F., V. D. Alves, J. Pais, N. Costa, C. Oliveira, L. Mafra, L. Hilliou, R. Oliveira & M. A. Reis, 2009. Characterization of an extracellular polysaccharide produced by a Pseudomonas strain grown on glycerol. Bioresources and Technology 100: 859–865.

    CAS  Google Scholar 

  • Gershenzon, J. & N. Dudareva, 2007. The function of terpene natural products in the natural world. Nature Chemical Biology 3: 408.

    CAS  PubMed  Google Scholar 

  • Gibbons, R. J. & M. Nygaard, 1970. Inter bacterial aggregation of plaque bacteria. Archives of Oral Biology 15: 1397–1400.

    CAS  PubMed  Google Scholar 

  • Guezennec, J., P. Pignet, Y. Lijour, E. Gentric, J. Ratiskol & S. Colliec-Jouault, 1998. Sulfation and depolymerization of a bacterial exopolysaccharide of hydrothermal origin. Carbohydrate Polymers 37: 19–24.

    CAS  Google Scholar 

  • Guillonneau, R., C. Baraquet, A. Bazire & M. Molmeret, 2018. Multispecies biofilm development of marine bacteria implies complex relationships through competition and synergy and modification of matrix components. Frontiers in Microbiology 9: 1960.

    PubMed  PubMed Central  Google Scholar 

  • Hadfield, M. G., 2011. Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Annual Review of Marine Science 3: 453–470.

    PubMed  Google Scholar 

  • Hede, N. & L. Khandeparker, 2018. Influence of darkness and aging on marine and freshwater biofilm microbial communities using microcosm experiments. Microbial Ecology 76: 314–317.

    PubMed  Google Scholar 

  • Helgason, E., D. A. Caugant, I. Olsen & A. B. Kolsto, 2000. Genetic structure of population of Bacillus cereus and B. thuringiensis isolates associated with periodontitis and other human infections. Journal of Clinical Microbiology 38: 1615–1622.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hmelo, L. R., 2017. Quorum sensing in marine microbial environments. Annual Review of Marine Science 9: 257–281.

    PubMed  Google Scholar 

  • Hoagland, K. D., J. R. Rosowski, M. R. Gretz & S. C. Roemer, 1993. Diatom extracellular polymeric substances: function, fine structure, chemistry, and physiology. Journal of Phycology 29: 537–566.

    CAS  Google Scholar 

  • Irie, Y. & M. R. Parsek, 2008. Quorum sensing and microbial biofilms. In Bacterial Biofilms. Springer, Berlin: 67–84.

  • Jain, A. & N. B. Bhosle, 2008. Role of β 1–4 linked polymers in the biofilm structure of marine Pseudomonas sp. CE-2 on 304 stainless steel coupons. Biofouling 24: 283–291.

    PubMed  Google Scholar 

  • Jain, A. & N. B. Bhosle, 2009. Biochemical composition of the marine conditioning film: implications for bacterial adhesion. Biofouling 25: 13–19.

    CAS  PubMed  Google Scholar 

  • Jemielita, M., N. S. Wingreen & B. L. Bassler, 2018. Quorum sensing controls Vibrio cholerae multicellular aggregate formation. eLife 7: e42057.

    PubMed  PubMed Central  Google Scholar 

  • Kalwasinska, A., T. Felföldi, A. Szabó, E. Deja-Sikora, P. Kosobucki & M. Walczak, 2017. Microbial communities associated with the anthropogenic, highly alkaline environment of a saline soda lime, Poland. Antonie Van Leeuwenhoek 110: 945–962.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kamnev, A. A., 2008. FT-IR spectroscopic studies of bacterial cellular responses to environmental factors, plant–bacterial interactions and signalling. Journal of Spectroscopy 22: 83–95.

    CAS  Google Scholar 

  • Katharios-Lanwermeyer, S., C. Xi, N. S. Jakubovics & A. H. Rickard, 2014. Mini-review: microbial coaggregation: ubiquity and implications for biofilm development. Biofouling 30: 1235–1251.

    CAS  PubMed  Google Scholar 

  • Kavita, K., A. Mishra & B. Jha, 2011. Isolation and physico-chemical characterisation of extracellular polymeric substances produced by the marine bacterium Vibrio parahaemolyticus. Biofouling 27: 309–317.

    CAS  PubMed  Google Scholar 

  • Kavita, K., A. Mishra & B. Jha, 2013. Extracellular polymeric substances from two biofilm forming Vibrio species: characterization and applications. Carbohydrate Polymers 94: 882–888.

    CAS  PubMed  Google Scholar 

  • Kavita, K., V. K. Singh, A. Mishra & B. Jha, 2014. Characterisation and anti-biofilm activity of extracellular polymeric substances from Oceanobacillus iheyensis. Carbohydrate Polymers 101: 29–35.

    CAS  PubMed  Google Scholar 

  • Kerr, C. J., K. S. Osborn, A. H. Rickard, G. D. Robson & P. S. Handley, 2003. Biofilms in water distribution systems. In Duncan, M. & N. J. Horan (eds), Water and Wastewater Engineering. Academic, London: 757–776.

    Google Scholar 

  • Khandeparker, L. & A. C. Anil, 2011. Role of conspecific cues and sugars in the settlement of cyprids of the barnacle, Balanus amphitrite. Journal of Zoology 284(3): 206–214.

    Google Scholar 

  • Khandeparker, L., A. C. Anil & S. Raghukumar, 2002. Factors regulating the production of different inducers in Pseudomonas aeruginosa with reference to larval metamorphosis in Balanus amphitrite. Aquatic Microbial Ecology 28: 37–54.

    Google Scholar 

  • Khandeparker, L., A. C. Anil & S. Raghukumar, 2003. Barnacle larval destination: piloting possibilities by bacteria and lectin interaction. Journal of Experimental Marine Biology and Ecology 289: 1–13.

    Google Scholar 

  • Khandeparker, R., P. Verma, R. M. Meena & D. D. Deobagkar, 2011. Phylogenetic diversity of carbohydrate degrading culturable bacteria from Mandovi and Zuari Estuaries, Goa, west coast of India. Estuarine, Coastal and Shelf Science 95: 359–366.

    CAS  Google Scholar 

  • Khandeparker, L., N. Hede, R. Eswaran, A. Usgaonkar & A. C. Anil, 2017. Microbial dynamics in a tropical monsoon influenced estuary: elucidation through field observations and microcosm experiments on biofilms. Journal of Experimental Marine Biology and Ecology 497: 86–98.

    Google Scholar 

  • Khandeparker, L., A. C. Anil & D. V. Desai, 2019. Immuno-modulation of settlement cues in the barnacle, Amphibalanus amphitrite: significance of circulating haemocytes. Hydrobiologia 830: 229–241.

    CAS  Google Scholar 

  • Khodse, V. B. & N. B. Bhosle, 2010. Differences in carbohydrate profiles in batch culture grown planktonic and biofilm cells of Amphora rostrata Wm. Sm. Biofouling 26: 527–537.

    CAS  PubMed  Google Scholar 

  • Kim, L. H. & T. H. Chong, 2017. Physiological responses of salinity-stressed Vibrio sp. and the effect on the biofilm formation on a nanofiltration membrane. Environmental Science and Technology 51(3): 1249–1258.

    CAS  PubMed  Google Scholar 

  • Kodali, V. P., S. Das & R. K. Sen, 2009. An exopolysaccharide from a probiotic: biosynthesis dynamics, composition and emulsifying activity. Food Research International 42: 695–699.

    CAS  Google Scholar 

  • Kolenbrander, P. E., N. Ganeshkumar, F. J. Cassels & C. V. Hughes, 1993. Coaggregation: specific adherence among human oral plaque bacteria. The FASEB Journal 7: 406–413.

    CAS  PubMed  Google Scholar 

  • Kolenbrander Jr., P. E., R. J. Palmer, A. H. Rickard, N. S. Jakubovics, N. I. Chalmers & P. I. Diaz, 2006. Bacterial interactions and successions during plaque development. Periodontology 42: 47–79.

    Google Scholar 

  • Kragh, K. N., J. B. Hutchison, G. Melaugh, C. Rodesney, A. E. Roberts, Y. Irie, P. Ø. Jensen, S. P. Diggle, R. J. Allen, V. Gordon & T. Bjarnsholt, 2016. Role of multicellular aggregates in biofilm formation. MBio 7: e00237-16.

    PubMed  PubMed Central  Google Scholar 

  • Kumar, K. V., A. Pal, P. Bai, A. Kour, E. Sheeba, P. Rajarajan, A. Kausar, M. Chatterjee, G. Prasad, S. Balayan & P. Dutta, 2019. Co-aggregation of bacterial flora isolated from the human skin surface. Microbial Pathogenesis 135: 103630.

    PubMed  Google Scholar 

  • Kviatkovski, I. & D. Minz, 2015. A member of the Rhodobacteraceae promotes initial biofilm formation via the secretion of extracellular factor (s). Aquatic Microbial Ecology 75(2): 155–167.

    Google Scholar 

  • Ledder, R. G., T. Madhwani, P. K. Sreenivasan, W. De Vizio & A. I. McBain, 2009. An in vitro evaluation of hydrolytic enzymes as dental plaque control agents. Journal of Medical Microbiology 58: 482–491.

    CAS  PubMed  Google Scholar 

  • Lloyd, A. G., K. S. Dodgson, R. G. Price & F. A. Rose, 1961. I. Polysaccharide sulphates. Biochimica et Biophysica Acta 46: 108–115.

    CAS  PubMed  Google Scholar 

  • Lorite, G. S., C. M. Rodrigues, A. A. De Souza, C. Kranz, B. Mizaikoff & M. A. Cotta, 2011. The role of conditioning film formation and surface chemical changes on Xylella fastidiosa adhesion and biofilm evolution. Journal of Colloid and Interface Science 359: 289–295.

    CAS  PubMed  Google Scholar 

  • Malik, A., M. Sakamoto, S. Hanazaki, M. Osawa, T. Suzuki, M. Tochigi & K. Kakii, 2003. Coaggregation among non-flocculating bacteria isolated from activated sludge. Applied and Environmental Microbiology 69: 6056–6060.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Melaugh, G., J. Hutchison, K. N. Kragh, Y. Irie, A. E. L. Roberts, T. Bjarnsholt, S. P. Diggle, V. D. Gordon & R. J. Allen, 2015. Shaping the growth behaviour of bacterial aggregates in biofilms. arXiv:1506.08168.

  • Min, K. R. & A. H. Rickard, 2009. Coaggregation by the freshwater bacterium Sphingomonas natatoria alters dual-species bio-film formation. Applied and Environmental Microbiology 75: 3987–3997.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Min, K. R., M. N. Zimmer & A. H. Rickard, 2010. Physicochemical parameters influencing coaggregation between the freshwater bacteria Sphingomonas natatoria 2.1 and Micrococcus luteus 2.13. Biofouling 26(8): 931–940.

    CAS  PubMed  Google Scholar 

  • Mora-Gómez, J., A. Freixa, N. Perujo & L. Barral-Fraga, 2016. Limits of the biofilm concept and types of aquatic biofilms. In Aquatic Biofilms: Ecology, Water Quality and Wastewater Treatment. Caister Academic Press, Norfolk: 3–27.

  • Naumann, D., 2000. Infrared spectroscopy in microbiology. Encyclopedia of Analytical Chemistry 102: 131.

    Google Scholar 

  • Neal, A. L. & A. B. Yule, 1996. The effects of dissolved sugars upon the temporary adhesion of barnacle cyprids. Journal of the Marine Biological Association of the United Kingdom 76: 649–655.

    CAS  Google Scholar 

  • Ojeda, J. J., M. E. Romero-González & S. A. Banwart, 2009. Analysis of bacteria on steel surfaces using reflectance micro-Fourier transform infrared spectroscopy. Analytical Chemistry 81: 6467–6473.

    CAS  PubMed  Google Scholar 

  • Palmer Jr., R. J., S. M. Gordon, J. O. Cisar & P. E. Kolenbrander, 2003. Coaggregation-mediated interactions of Streptococci and Actinomyces detected in initial human dental plaque. Journal of Bacteriology 185: 3400–3409.

    CAS  PubMed  Google Scholar 

  • Pan, M., K. K. Kumaree & N. P. Shah, 2017. Physiological changes of surface membrane in Lactobacillus with prebiotics. Journal of Food Science 82: 744–750.

    CAS  PubMed  Google Scholar 

  • Patt, M. W., L. Conte, M. Blaha & B. J. Plotkin, 2018. Steroid hormones as interkingdom signaling molecules: innate immune function and microbial colonization modulation. AIMS Molecular Science 5: 117–130.

    CAS  Google Scholar 

  • Purevdorj-Gage, B., W. J. Costerton & P. Stoodley, 2005. Phenotypic differentiation and seeding dispersal in non-mucoid and mucoid Pseudomonas aeruginosa biofilms. Microbiology 151: 1569–1576.

    CAS  PubMed  Google Scholar 

  • Qian, P. Y., S. C. Lau, H. U. Dahms, S. Dobretsov & T. Harder, 2007. Marine biofilms as mediators of colonization by marine macroorganisms: implications for antifouling and aquaculture. Marine Biotechnology 9(4): 399–410.

    CAS  PubMed  Google Scholar 

  • Raju, K. S. & L. Anitha, 2015. Isolation and identification of oral flora from individuals belonging to ages 7 to 16 years. Research Journal of Science and IT Management 4: 5–11.

    Google Scholar 

  • Rani, A. A., S. Jeeva, S. M. J. Punitha, N. P. Lexshmi & J. R. Brindha, 2016. Biochemical and molecular analysis of bacteria isolated from dental caries. Journal of Chemical and Pharmaceutical Research 8: 512–519.

    CAS  Google Scholar 

  • Remonsellez, F., J. Castro-Severyn, P. M. Aguilar Espinosa, J. Fortt, C. Salinas, S. Barahona, J. León, C. Pardo-Esté, B. Fuentes, C. Areche & K. Hernández, 2018. Characterization and salt response in recurrent halotolerant Exiguobacterium spp. SH31 isolated from sediments of Salar de Huasco, Chilean Altiplano. Frontiers in Microbiology 9: 2228.

    PubMed  PubMed Central  Google Scholar 

  • Rickard, A. H., S. A. Leach, C. M. Buswell, N. J. High & P. S. Handley, 2000. Coaggregation between aquatic bacteria is mediated by specific-growth-phase-dependent lectin–saccharide interactions. Applied Environmental Microbiology 66: 431–434.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rickard, A. H., S. A. Leach, L. S. Hall, C. M. Buswell, N. J. High & P. S. Handley, 2002. Phylogenetic relationships and coaggregation ability of freshwater biofilm bacteria. Applied Environmental Microbiology 68: 3644–3650.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rickard, A. H., P. Gilbert, N. J. High, P. E. Kolenbrander & P. S. Handley, 2003. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends in Microbiology 11: 94–100.

    CAS  PubMed  Google Scholar 

  • Rickard, A. H., P. Gilbert & P. S. Handley, 2004. Influence of growth environment on coaggregation between freshwater biofilm bacteria. Journal of Applied Microbiology 96: 136773.

    Google Scholar 

  • Ruger, H. J., 1989. Benthic studies of the northwest African upwelling region psychrophilic bacterial communities from areas with different upwelling intensities. Marine Ecological Progress Series 57: 45–52.

    Google Scholar 

  • Rumbaugh, K. P. & A. Armstrong, 2014. The role of quorum sensing in biofilm development. In Rumbaugh, K. & I. Ahmad (eds), Antibiofilm Agents. Springer Series on Biofilms, Vol. 8. Springer, Berlin: 97–113.

    Google Scholar 

  • Sahoo, G. & L. Khandeparker, 2018. Role of epibiotic diatoms isolated from the barnacle shell in the cyprid metamorphosis of Balanus amphitrite. Hydrobiologia 822: 129–142.

    CAS  Google Scholar 

  • Sakthivel, M., P. M. Ayyasamy & D. Arvind Prasanth, 2016. Identification and antimicrobial susceptibility testing of pathogenic microorganism from dental patients. Asian Journal of Pharmaceutical and Clinical Research 9: 226–230.

    CAS  Google Scholar 

  • Saravanan, N., P. Verma, V. P. Mol, R. S. Kumar, S. T. Somasundaram, G. Dharani & R. Kirubagaran, 2014. Role of microbial aggregation in biofilm formation by bacterial strains isolated from offshore finfish culture environment. Indian Journal of Geo-marine Sciences 43: 2118–2129.

    Google Scholar 

  • Sauer, K., A. K. Camper, G. D. Ehrlich, J. W. Costerton & D. G. Davies, 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. Journal of Bacteriology 184: 1140–1154.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seedevi, P., S. Sudharsan, S. V. Kumar, A. Srinivasan, S. Vairamani & A. Shanmugan, 2013. Isolation and characterization of sulphated polysaccharides from Codium tomentosum (J. Stackhouse, 1797) collected from southeast coast of India. Advances in Applied Science Research 4: 72–77.

    CAS  Google Scholar 

  • Sheng, G. P., H. Q. Yu & Z. Yu, 2005. Extraction of extracellular polymeric substances from the photosynthetic bacterium Rhodopseudomonas acidophila. Applied Microbiology and Biotechnology 67: 125–130.

    CAS  PubMed  Google Scholar 

  • Sigma-Aldrich, 2009. Glycobiology. Life Science BioFiles 5: 1–32.

    Google Scholar 

  • Simões, L. C., M. Simoes & M. J. Vieira, 2008. Intergeneric coaggregation among drinking water bacteria: evidence of a role for Acinetobacter calcoaceticus as a bridging bacterium. Applied and Environmental Microbiology 74: 1259–1263.

    PubMed  Google Scholar 

  • Smyth, K. & M. Elliott, 2016. Effects of changing salinity on the ecology of the marine environment. In Solan, M. & N. M. Whiteley (eds), Stressors in the Marine Environment. Oxford University Press, Oxford: 161–174.

    Google Scholar 

  • Sonak, S. M., 1998. Studies on marine fouling bacteria. Doctoral Dissertation, Goa University.

  • Sravankumar, G., Y. V. K. Durgaprasad, T. Ramana & C. S. L. V. Devi, 2014. Isolation and identification of bacteria from marine biofilm on the artificial plat forms (iron panels) from Visakhapatnam Coast, India. Indian Journal of Geo-marine Sciences 43: 961–965.

    Google Scholar 

  • Stevens, M. R., T. L. Luo, J. Vornhagen, N. S. Jakubovics, J. R. Gilsdorf, C. F. Marrs, T. Møretrø & A. H. Rickard, 2015. Coaggregation occurs between microorganisms isolated from different environments. FEMS Microbiology Ecology 91: p.fiv123.

    Google Scholar 

  • Stewart, P. S. & J. W. Costerton, 2001. Antibiotic resistance of bacteria in biofilms. The Lancet 358: 135–138.

    CAS  Google Scholar 

  • Stoodley, P., L. Hall-Stoodley & H. M. Lappin-Scott, 2001. Detachment, surface migration, and other dynamic behavior in bacterial biofilms revealed by digital time-lapse imaging. Methods Enzymology 337: 306–319.

    CAS  Google Scholar 

  • Strathmann, M., J. Wingender & H. C. Flemming, 2002. Application of fluorescently labelled lectins for the visualization and biochemical characterization of polysaccharides in biofilms of Pseudomonas aeruginosa. Journal of Microbiological Methods 50: 237–248.

    CAS  PubMed  Google Scholar 

  • Stratil, S. B., S. C. Neulinger, H. Knecht, A. K. Friedrichs & M. Wahl, 2014. Salinity affects compositional traits of epibacterial communities on the brown macroalga Fucus vesiculosus. FEMS Microbiology Ecology 88(2): 272–279.

    CAS  PubMed  Google Scholar 

  • Suh, H. H., G. S. Kwon, C. H. Lee, H. S. Kim, H. M. Oh & B. D. Yoon, 1997. Characterization of bioflocculant produced by Bacillus sp. DP-152. Journal of Fermentation and Bioengineering 84: 108–112.

    CAS  Google Scholar 

  • Tallon, R., P. Bressollier & M. C. Urdaci, 2003. Isolation and characterization of two exopolysaccharides produced by Lactobacillus plantarum EP56. Research in Microbiology 154: 705–712.

    CAS  PubMed  Google Scholar 

  • Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tien, C. J., D. C. Sigee & K. N. White, 2005. Characterization of surface sugars on algal cells with fluorescein isothiocyanate-conjugated lectins. Protoplasma 225: 225–233.

    CAS  PubMed  Google Scholar 

  • Trunk, T., H. S. Khalil & J. C. Leo, 2018. Bacterial autoaggregation. AIMS Microbiology 4: 140.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuneda, S., H. Aikawa, H. Hayashi, A. Yuasa & A. Hirata, 2003. Extracellular polymeric substances responsible for bacterial adhesion onto solid surface. FEMS Microbiology Letters 223: 287–292.

    CAS  PubMed  Google Scholar 

  • van Loosdrecht, M., W. Norde, L. Lyklema & J. Zehnder, 1990. Hydrophobic and electrostatic parameters in bacterial adhesion. Aquatic Sciences 51: 103–114.

    Google Scholar 

  • Vandervivere, P. & D. L. Kirchman, 1993. Attachment stimulates exopolysaccharide synthesis by a bacterium. Applied and Environmental Microbiology 59: 3280–3286.

    Google Scholar 

  • Vasudevan, R., 2017. Dental plaques: microbial community of the oral cavity. Journal of Microbiology and Experimentation 4: 1–9.

    Google Scholar 

  • Vornhagen, J., M. Stevens, D. W. McCormick, S. E. Dowd, J. N. Eisenberg, B. R. Boles & A. H. Rickard, 2013. Coaggregation occurs amongst bacteria within and between biofilms in domestic showerheads. Biofouling 29: 53–68.

    PubMed  PubMed Central  Google Scholar 

  • Wahl, M., F. Goecke, A. Labes, S. Dobretsov & F. Weinberger, 2012. The second skin: ecological role of epibiotic biofilms on marine organisms. Frontiers in Microbiology 3: 292.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Watnick, P. & R. Kolter, 2000. Biofilm, city of microbes. Journal of Bacteriology 182: 2675–2679.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng, J., J. M. Gao, Y. P. Chen, P. Yan, Y. Dong, Y. Shen, J. S. Guo, N. Zeng & P. Zhang, 2016. Composition and aggregation of extracellular polymeric substances (EPS) in hypersaline and municipal wastewater treatment plants. Scientific Reports 6: 26721.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, M., N. Yang, B. Yang, Y. Jiang & G. Zhang, 2007. Structural characterization of water-soluble polysaccharides from Opuntia monacantha cladodes in relation to their anti-glycated activities. Food Chemistry 105: 1480–1486.

    CAS  Google Scholar 

  • Zhao, L., Z. She, C. Jin, S. Yang, L. Guo, Y. Zhao & M. Gao, 2016. Characteristics of extracellular polymeric substances from sludge and biofilm in a simultaneous nitrification and denitrification system under high salinity stress. Bioprocess and Biosystems Engineering 39(9): 1375–1389.

    PubMed  Google Scholar 

Download references

Acknowledgements

We are thankful to the Director, National Institute of Oceanography, for his support and encouragement. We are also thankful to Bio-organic Chemical Laboratory for providing access to FT-IR spectroscopy, and Dr. Maria Brenda Mascarenhas for providing access to Scanning Electronic Microscopy (SEM) Facility. The first author acknowledges Jawaharlal Nehru Memorial Fund for the Award of JNMF Scholarship and is a Registered PhD Student at the School of Atmospheric, Earth and Ocean Sciences, Goa University. This work was funded by the Ballast Water Management Program, India (Ministry of Shipping and DG shipping) (GAP 2429) and CSIR funded Ocean Finder Program (PSC 0105). This is NIO Contribution No. 6598.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lidita Khandeparker.

Additional information

Handling editor: Stefano Amalfitano

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hede, N., Khandeparker, L. Extracellular polymeric substances mediate the coaggregation of aquatic biofilm-forming bacteria. Hydrobiologia 847, 4249–4272 (2020). https://doi.org/10.1007/s10750-020-04411-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-020-04411-x

Keywords

Navigation