Marine biofilms are ubiquitous in the marine environment. These complex microbial communities rapidly respond to environmental changes and encompass hugely diverse microbial structures, functions and metabolisms. Nevertheless, knowledge is limited on the microbial community structures and functions of natural marine biofilms and their influence on global geochemical cycles. Microbial cues, including secondary metabolites and microbial structures, regulate interactions between microorganisms, with their environment and with other benthic organisms, which affects their community succession and metamorphosis. Furthermore, marine biofilms are key mediators of marine biofouling, which greatly affect marine industries. In this Review, we discuss marine biofilm dynamics, including their diversity, abundance and functions. We also highlight knowledge gaps, areas for future research and potential biotechnological applications of marine biofilms.
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Zobell, C. & Allen, E. C. Attachment of marine bacteria to submerged slides. Proc. Soc. Exp. Biol. Med. 30, 1409–1411 (1933).
Zobell, C. & Allen, E. C. The significance of marine bacteria in the fouling of submerged surfaces. J. Bacteriol. 29, 239–251 (1935).
Flemming, H. C. & Wuertz, S. Bacteria and archaea on Earth and their abundance in biofilms. Nat. Rev. Microbiol. 17, 247–260 (2019). This study estimates the number of bacteria and archaea in biofilms in different environments on Earth.
de Carvalho, C. C. Marine biofilms: a successful microbial strategy with economic implications. Front. Mar. Sci. 5, 126 (2018).
Flemming, H. C. & Wingender, J. The biofilm matrix. Nat. Rev. Microbiol. 8, 623–633 (2010).
Koch, G. H., Brongers, M. P., Thompson, N. G., Virmani, Y. P. & Payer, J. H. In Handbook of Environmental Degradation of Materials (ed. Kutz, M.) 3–24 (William Andrew Publishing, 2005).
Schultz, M. P. Effects of coating roughness and biofouling on ship resistance and powering. Biofouling 23, 331–341 (2007).
Oberbeckmann, S. & Labrenz, M. Marine microbial assemblages on microplastics: diversity, adaptation, and role in degradation. Annu. Rev. Mar. Sci. 12, 209–232 (2020). This is an excellent overview of microplastic as a unique habitat for marine microbial biofilms.
Wright, R. J., Erni-Cassola, G., Zadjelovic, V., Latva, M. & Christie-Oleza, J. A. Marine plastic debris: a new surface for microbial colonization. Environ. Sci. Tech. 54, 11657–11672 (2020).
Rummel, C. D., Jahnke, A., Gorokhova, E., Kühnel, D. & Schmitt-Jansen, M. Impacts of biofilm formation on the fate and potential effects of microplastic in the aquatic environment. Environ. Sci. Tech. Let. 4, 258–267 (2017).
Zhao, S., Zettler, E. R., Amaral-Zettler, L. A. & Mincer, T. J. Microbial carrying capacity and carbon biomass of plastic marine debris. ISME J. 15, 67–77 (2021).
Wahl, M., Goecke, F., Labes, A., Dobretsov, S. & Weinberger, F. The second skin: ecological role of epibiotic biofilms on marine organisms. Front. Microbiol. 3, 292 (2012). This paper highlights the importance of epibiotic biofilms in modulating the abiotic and biotic interactions of marine organisms.
Wahl, M. et al. Ecology of antifouling resistance in the bladder wrack Fucus vesiculosus: patterns of microfouling and antimicrobial protection. Mar. Ecol. Prog. Ser. 411, 33–48 (2010).
Simon, H. M., Smith, M. W. & Herfort, L. Metagenomic insights into particles and their associated microbiota in a coastal margin ecosystem. Front. Microbiol. 5, 466 (2014).
Grossart, H. P. Ecological consequences of bacterioplankton lifestyles: changes in concepts are needed. Env. Microbiol. Rep. 2, 706–714 (2010).
Azam, F. & Long, R. A. Sea snow microcosms. Nature 414, 495–498 (2001).
Alcolombri, U. et al. Sinking enhances the degradation of organic particles by marine bacteria. Nat. Geosci. 14, 775–780 (2021).
Herndl, G. J. & Reinthaler, T. Microbial control of the dark end of the biological pump. Nat. Geosci. 6, 718–724 (2013).
Dang, H. & Lovell, C. R. Microbial surface colonization and biofilm development in marine environments. Microbiol. Mol. Biol. Rev. 80, 91–138 (2016).
Flemming, H. C. et al. Who put the film in biofilm? The migration of a term from wastewater engineering to medicine and beyong. NPJ Biofilms Microbiomes 7, 10 (2021). This paper provides a good brief history of the definition of the term ‘biofilm’ and recommends understanding biofilms in the broader sense of microbial aggregates.
Charette, M. A. & Smith, W. H. The volume of Earth’s ocean. Oceanography 23, 112–114 (2010).
Franklin, M. P. et al. Bacterial diversity in the bacterioneuston (sea surface microlayer): the bacterioneuston through the looking glass. Environ. Microbiol. 7, 723–736 (2005).
Berne, C., Ellison, C. K., Ducret, A. & Brun, Y. V. Bacterial adhesion at single-cell level. Nat. Rev. Microbiol. 16, 616–627 (2018).
Zijnge, V. et al. Oral biofilm architecture on natural teeth. PLoS One 5, e9321 (2010).
Salta, M., Wharton, J. A., Blache, Y., Stokes, K. & Briand, J. F. Marine biofilms on artificial surfaces: structure and dynamics. Environ. Microbiol. 15, 2879–2893 (2013).
Freckelton, M. L., Nedved, B. T. & Hadfield, M. G. Induction of invertebrate larval settlement; different bacteria, different mechanisms? Sci. Rep. 7, 42557 (2017).
Hansen, M. F., Svenningsen, S. L., Røder, H. L., Middelboe, M. & Burmølle, M. Big impact of the tiny: bacteriophage-bacteria interactions in biofilms. Trends Microbiol. 27, 739–752 (2019).
Pires, D. P., Melo, L. D. & Azeredo, J. Understanding the complex phage-host interactions in biofilm communities. Annu. Rev. Virol. 8, 73–94 (2021).
Lau, S. C. K., Mak, K. K. W., Chen, F. & Qian, P. Y. Bioactivity of bacterial strains isolated from marine biofilms in Hong Kong waters for the induction of larval settlement in the marine polychaete Hydroides elegans. Mar. Ecol. Prog. Ser. 226, 301–310 (2002).
Chung, H. C. et al. Bacterial community succession and chemical profiles of subtidal biofilms in relation to larval settlement of the polychaete Hydroides elegans. ISME J. 4, 817–828 (2010). This study is the first to report variations in the chemical compositions of marine biofilms over time.
Qian, P. Y., Thiyagarajan, V., Lau, S. C. K. & Cheung, S. C. K. Relationship between bacterial community profile in biofilm and attachment of the acorn barnacle Balanus amphitrite. Aquat. Microb. Ecol. 33, 225–237 (2003).
Zhang, W. P. et al. Biofilms constitute a bank of hidden microbial diversity and functional potential in the oceans. Nat. Commun. 10, 517 (2019). This study provides the largest global survey of microbial diversity of marine biofilms.
Grzegorczyk, M., Pogorzelski, S. J., Pospiech, A. & Boniewicz-Szmyt, K. Monitoring of marine biofilm formation dynamics at submerged solid surfaces with multitechnique sensors. Front. Mar. Sci. https://doi.org/10.3389/fmars.2018.00363 (2018).
Whalan, S. & Webster, N. Sponge larval settlement cues: the role of microbial biofilms in a warming ocean. Sci. Rep. 4, 4072 (2014).
Doghri, I. et al. Marine bacteria from the French Atlantic coast displaying high forming-biofilm abilities and different biofilm 3D architectures. BMC Microbiol. 15, 231 (2015).
Battin, T. J., Besemer, K., Bengtsson, M. M., Romani, A. M. & Packmann, A. I. The ecology and biogeochemistry of stream biofilms. Nat. Rev. Microb. 14, 251–263 (2016).
Harrison, J. P. et al. In Freshwater Microplastics (eds. Wagner, M. & Lambert, S.) 181–201 (Springer Nature, 2018).
Dussud, C. et al. Evidence of niche partitioning among bacteria living on plastics, organic particles and surrounding seawaters. Environ. Pollut. 236, 807–816 (2018).
Catão C P, E. et al. Temperate and tropical coastal waters share relatively similar microbial biofilm communities while free-living or particle-attached communities are distinct. Mol. Ecol. 30, 2891–2904 (2021).
Antunes, J., Leão, P. & Vasconcelos, V. Marine biofilms: diversity of communities and of chemical cues. Env. Microbiol. Rep. 11, 287–305 (2019). This is one of the reviews summarizing the high biological and chemical diversity of marine biofilms.
Patil, J. S. & Anil, A. C. Biofilm diatom community structure: influence of temporal and substratum variability. Biofouling 21, 189–206 (2005).
Kettner, M. T., Rojas-Jimenez, K., Oberbeckmann, S., Labrenz, M. & Grossart, H. P. Microplastics alter composition of fungal communities in aquatic ecosystems. Environ. Microbiol. 19, 4447–4459 (2017).
von Ammon, U. et al. The impact of artificial surfaces on marine bacterial and eukaryotic biofouling assemblages: a high-throughput sequencing analysis. Mar. Environ. Res. 133, 57–66 (2018).
Briand, J. F. et al. Metabarcoding and metabolomics offer complementarity in deciphering marine eukaryotic biofouling community shifts. Biofouling 34, 657–672 (2018).
Debroas, D., Mone, A. & Ter Halle, A. Plastics in the north Atlantic garbage patch: a boat-microbe for hitchhikers and plastic degraders. Sci. Total Environ. 599, 1222–1232 (2017).
Kettner, M. T., Oberbeckmann, S., Labrenz, M. & Grossart, H. P. The eukaryotic life on microplastics in brackish ecosystems. Front. Microbiol. 10, 538 (2019).
Ding, W. et al. Expanding our understanding of marine viral diversity through metagenomic analyses of biofilms. Mar. Life Sci. Technol. 3, 395–404 (2021).
Hung, O. S., Thiyagarajan, V. & Qian, P. Y. Preferential attachment of barnacle larvae to natural multi-species biofilms: does surface wettability matter? J. Exp. Mar. Biol. Ecol. 361, 36–41 (2008).
Pedersen, K. Biofilm development on stainless steel and PVC surfaces in drinking water. Water Res. 24, 239–243 (1990).
Lee, O. O. et al. In situ environment rather than substrate type dictates microbial community structure of biofilms in a cold seep system. Sci. Rep. 4, 3587 (2014).
Zhang, W. P. et al. Species sorting during biofilm assembly by artificial substrates deployed in a cold seep system. Sci. Rep. 4, 6647 (2014).
Chiu, W. Y., Thiyagarajan, V., Tsoi, M. & Qian, P. Y. Qualitative and quantitative changes in marine microbial films as a function of temperature and salinity in summer and winter. Biofilms 2, 183–195 (2005).
Chiu, W. Y., Zhang, R., Thiyagarajan, V. & Qian, P. Y. Nutrient effects on intertidal community: from bacteria to invertebrates. Mar. Ecol. Prog. Ser. 358, 41–50 (2008).
Hung, O. S., Gosselin, L. A., Thiyagarajan, V., Wu, R. S. S. & Qian, P. Y. Do effects of ultraviolet radiation on microbial films have indirect effects on larval attachment of the barnacle Balanus amphitrite. J. Exp. Mar. Biol. Ecol. 323, 16–26 (2005).
Hung, O. S., Thiyagarajan, V., Wu, R. S. S. & Qian, P. Y. Effects of ultraviolet radiation on films and subsequent settlement of Hydroides elegans. Mar. Ecol. Prog. Ser. 304, 155–166 (2005).
Qian, P. Y., Rittschof, D. & Sreedhar, B. Macrofouling in unidirectional flow: miniature pipes as experimental models for studying the interaction of flow and surface characteristics on the attachment of barnacle, bryozoan and polychaete larvae. Mar. Ecol. Prog. Ser. 207, 109–121 (2000).
Wahl, M. Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar. Ecol. Prog. Ser. 58, 175–189 (1989).
Dang, H. & Lovell, C. R. Bacterial primary colonization and early succession on surfaces in marine waters as determined by amplified rRNA gene restriction analysis and sequence analysis of 16S rRNA genes. Appl. Environ. Microb. 66, 467–475 (2000).
Dang, H. & Lovell, C. R. Numerical dominance and phylotype diversity of marine Rhodobacter species during early colonization of submerged surfaces in coastal marine waters as determined by 16S ribosomal DNA sequence analysis and fluorescence in situ hybridization. Appl. Environ. Microbiol. 68, 496–504 (2002).
Flemming, H. C. Biofouling in water systems-cases, causes and countermeasures. Appl. Microbiol. Biotech. 59, 629–640 (2002).
Lawes, J. C., Neilan, B. A., Brown, M. V., Clark, G. F. & Johnston, E. L. Elevated nutrients change bacterial community composition and connectivity: high throughput sequencing of young marine biofilms. Biofouling 32, 57–69 (2016).
Antunes, J. T. et al. Distinct temporal succession of bacterial communities in early marine biofilms in a Portuguese Atlantic Port. Front. Microbiol. 11, 1938 (2020).
Lee, J. W., Nam, J. H., Kim, Y. H., Lee, K. H. & Lee, D. H. Bacterial communities in the initial stage of marine biofilm formation on artificial surfaces. J. Microbiol. 46, 174–182 (2008).
Pollet, T. et al. Prokaryotic community successions and interactions in marine biofilms: the key role of Flavobacteria. FEMS Microbiol. Ecol. 94, fiy083 (2018).
Datta, M. S., Sliwerska, E., Gore, J., Polz, M. F. & Cordero, O. X. Microbial interactions lead to rapid micro-scale successions on model marine particles. Nat. Commun. 7, 11965 (2016). This is one of the few studies about marine biofilm community succession with high temporal resolution.
Sushmitha, T. J. et al. Bacterial community structure of early-stage biofilms is dictated by temporal succession rather than substrate types in the southern coastal seawater of India. PLoS One 16, e0257961 (2021).
Bellou, N., Garcia, J. A. L., Colijn, F. & Herndl, G. J. Seasonality combined with the orientation of surfaces influences the microbial community structure of biofilms in the deep Mediterranean Sea. Deep Sea Res. II Top. Stud. Oceanogr. 171, 104703 (2020).
Jones, P. R., Cottrell, M. T., Kirchman, D. L. & Dexter, S. C. Bacterial community structure of biofilms on artificial surfaces in an estuary. Microb. Ecol. 53, 153–162 (2007).
Huggett, M., Nedved, B. & Hadfield, M. Effects of initial surface wettability on biofilm formation and subsequent settlement of Hydroides elegans. Biofouling 25, 387–399 (2009).
Caruso, G. Microbial colonization in marine environments: overview of current knowledge and emerging research topics. J. Mar. Sci. Eng. 8, 78 (2020).
Bellou, N., Papathanassiou, E., Dobretsov, S., Lykousis, V. & Colijn, F. The effect of substratum type, orientation and depth on the development of bacterial deep-sea biofilm communities grown on artificial substrata deployed in the Eastern Mediterranean. Biofouling 28, 199–213 (2012).
Oberbeckmann, S., Loeder, M. G., Gerdts, G. & Osborn, A. M. Spatial and seasonal variation in diversity and structure of microbial biofilms on marine plastics in Northern European waters. FEMS Microbiol. Ecol. 90, 478–492 (2014).
Oberbeckmann, S., Osborn, A. M. & Duhaime, M. B. Microbes on a bottle: substrate, season and geography influence community composition of microbes colonizing marine plastic debris. PLoS One 11, e0159289 (2016).
Underwood, A. J. The vertical distribution and seasonal abundance of intertidal microalgae on a rocky shore in New South Wales. J. Exp. Mar. Biol. Ecol. 78, 199–220 (1984).
Bengtsson, M. M., Sjøtun, K. & Øvreås, L. Seasonal dynamics of bacterial biofilms on the kelp Laminaria hyperborea. Aquat. Microbiol. Ecol. 60, 71–83 (2010).
Sawall, Y., Richter, C. & Ramette, A. Effects of eutrophication, seasonality and macrofouling on the diversity of bacterial biofilms in equatorial coral reefs. PLoS One 7, e39951 (2012).
Mancuso, F. P., D’hondt, S., Willems, A., Airoldi, L. & De Clerck, O. Diversity and temporal dynamics of the epiphytic bacterial communities associated with the canopy-forming seaweed Cystoseira compressa (Esper) Gerloff and Nizamuddin. Front. Microbiol. 7, 476 (2016).
Gulmann, L. K. et al. Bacterial diversity and successional patterns during biofilm formation on freshly exposed basalt surfaces at diffuse-flow deep-sea vents. Front. Microbiol. 6, 901 (2015).
O’Brien, C. E. et al. Microbial biofilms associated with fluid chemistry and megafaunal colonization at post-eruptive deep-sea hydrothermal vents. Deep Sea Res. II Top. Stud. Oceanogr. 121, 31–40 (2015).
Dick, G. J. The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally. Nat. Rev. Microbiol. 17, 271–283 (2019).
Woodall, L. C. et al. Deep-sea anthropogenic macrodebris harbours rich and diverse communities of bacteria and archaea. PLoS One 13, e0206220 (2018).
Mugge, R. L. et al. Deep-sea biofilms, historic shipwreck preservation and the Deepwater Horizon spill. Front. Mar. Sci. 6, 48 (2019).
Clark, M. S. et al. Lack of long-term acclimation in Antarctic encrusting species suggests vulnerability to warming. Nat. Commun. 10, 3383 (2019).
Lannuzel, D. et al. The future of Arctic sea-ice biogeochemistry and ice-associated ecosystems. Nat. Clim. Change 10, 983–992 (2020).
Webster, N. S. & Negria, A. P. Site-specific variation in Antarctic marine biofilms established on artificial surfaces. Env. Microbiol. 8, 1177–1190 (2006).
Lee, Y. M. et al. Succession of bacterial community structure during the early stage of biofilm development in the Antarctic marine environment. Korean J. Microbiol. 52, 49–58 (2015).
Thomas, D. N. & Dieckmann, G. S. Antarctic sea ice-a habitat for extremophiles. Science 295, 641–644 (2002).
Roukaerts, A. et al. The biogeochemical role of a microbial biofilm in sea ice: Antarctic landfast sea ice as a case study. The biogeochemical role of a microbial biofilm in sea ice: Antarctic landfast sea ice as a case study. Elementa 9, 00134 (2021).
Boetius, A., Anesio, A. M., Deming, J. W., Mikucki, J. A. & Rapp, J. Z. Microbial ecology of the cryosphere: sea ice and glacial habitats. Nat. Rev. Microbiol. 13, 677–690 (2015).
Arrigo, K. R. Sea ice ecosystems. Annu. Rev. Mar. Sci. 6, 439–467 (2014).
Ewert, M. & Deming, J. W. Sea ice microorganisms: environmental constraints and extracellular responses. Biology 2, 603–628 (2013).
Brown, M. V. & Bowman, J. P. A molecular phylogenetic survey of sea-ice microbial communities (SIMCO). FEMS Microbiol. Ecol. 35, 267–275 (2001).
Wang, R. et al. Profiling signal transduction in global marine biofilms. Front. Microbiol. 12, 768926 (2021).
Brazelton, W. J. & Baross, J. A. Abundant transposases encoded by the metagenome of a hydrothermal chimney biofilm. ISME J. 3, 1420–1424 (2009).
Ding, W. et al. Metagenomic analysis of zinc surface–associated marine biofilms. Microb. Ecol. 77, 406–416 (2019).
Zhang, Y. et al. Metagenomic resolution of functional diversity in copper surface-associated marine biofilms. Front. Microbiol. 10, 2863 (2019).
Yang, Y. et al. Plastics in the marine environment are reservoirs for antibiotic and metal resistance genes. Environ. Int. 123, 79–86 (2019).
Liu, Y. et al. Microplastics are a hotspot for antibiotic resistance genes: progress and perspective. Sci. Total. Environ. 773, 145643 (2021).
Tait, K. et al. Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms. Environ. Microbiol. 7, 229–240 (2005).
Kjelleberg, S. & Molin, S. Is there a role for quorum sensing signals in bacterial biofilms? Curr. Opin. Microbiol. 5, 254–258 (2002).
Huang, Y. L., Ki, J. S., Lee, O. O. & Qian, P. Y. Evidence for the dynamics of Acyl homoserine lactone and AHL-producing bacteria during subtidal biofilm formation. ISME J. 3, 296–304 (2008). This study is one of the first attempts to investigate QS signals in natural marine biofilms.
Jones, S. E. & McMahon, K. D. Species-sorting may explain an apparent minimal effect of immigration on freshwater bacterial community dynamics. Environ. Microbiol. 11, 905–913 (2009).
Feng, K. et al. Biodiversity and species competition regulate the resilience of microbial biofilm community. Mol. Ecol. 26, 6170–6182 (2017).
Misic, C. & Harriague, A. C. Development of marine biofilm on plastic: ecological features in different seasons, temperatures, and light regimes. Hydrobiologia 835, 129–145 (2019).
Elias, S. & Banin, E. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol. Rev. 36, 990–1004 (2012).
Rendueles, O. & Ghigo, J.-M. Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiol. Rev. 36, 972–989 (2012).
Nadell, C. D., Drescher, K. & Foster, K. R. Spatial structure, cooperation and competition in biofilms. Nat. Rev. Microbiol. 14, 589–600 (2016).
Dou, W., Xu, D. & Gu, T. Biocorrosion caused by microbial biofilms is ubiquitous around us. Microb. Biotech. 14, 803–805 (2021).
Smith, P. & Schuster, M. Public goods and cheating in microbes. Cur. Biol. 29, 442–447 (2019).
Nadell, C. D. et al. Cutting through the complexity of cell collectives. Proc. Biol. Sci. 280, 20122770 (2013).
Drescher, K., Nadell, C. D., Stone, H. A., Wingreen, N. S. & Bassler, B. L. Solutions to the public goods dilemma in bacterial biofilms. Curr. Biol. 24, 50–55 (2014).
Balcázar, J. L., Subirats, J. & Borrego, C. M. The role of biofilms as environmental reservoirs of antibiotic resistance. Front. Microbiol. 6, 1216 (2015).
Guo, X. P. et al. Biofilms as a sink for antibiotic resistance genes (ARGs) in the Yangtze Estuary. Water Res. 129, 277–286 (2018).
Davies, D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2, 114–122 (2003).
Nyholm, S. V. & McFall-Ngai, M. J. Dominance of Vibrio fischeri in secreted mucus outside the light organ of Euprymna scolopes: the first site of symbiont specificity. Appl. Environ. Microbiol. 69, 3932–3937 (2003).
Nyholm, S. V. & McFall-Ngai, M. The winnowing: establishing the squid-vibrio symbiosis. Nat. Rev. Microbiol. 2, 632–642 (2004).
Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8, 15–25 (2010).
Han, Q. F. et al. Distribution, combined pollution and risk assessment of antibiotics in typical marine aquaculture farms surrounding the Yellow Sea, North China. Environ. Int. 138, 105551 (2020).
Goel, N., Fatima, S. W., Kumar, S., Sinha, R. & Khare, S. K. Antimicrobial resistance in biofilms: Exploring marine actinobacteria as a potential source of antibiotics and biofilm inhibitors. Biotech. Rep. 30, e00613 (2021).
Yan, L., Boyd, K. G., Adams, D. R. & Burgess, J. G. Biofilm-specific cross-species induction of antimicrobial compounds in bacilli. Appl. Environ. Microb. 69, 3719–3727 (2003).
Camilli, A. & Bassler, B. L. Bacterial small-molecule signaling pathways. Science 311, 1113–1116 (2006).
Hengge, R. Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol. 7, 263–273 (2009).
Bourret, R. B. & Silversmith, R. E. Two-component signal transduction. Curr. Opin. Microbiol. 13, 113 (2010).
Bassler, B. L. & Losick, R. Bacterially speaking. Cell 125, 237–246 (2006).
Miller, M. B. & Bassler, B. L. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55, 165–199 (2001).
Jenal, U. & Malone, J. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet. 40, 385–407 (2006).
Gotoh, Y. et al. Two-component signal transduction as potential drug targets in pathogenic bacteria. Curr. Opin. Microbiol. 13, 232–239 (2010).
Ono, K. et al. cAMP signaling affects irreversible attachment during biofilm formation by Pseudomonas aeruginosa PAO1. Microb. Environ. 29, 104–106 (2014).
Fong, J. C. & Yildiz, F. H. Interplay between cyclic AMP-cyclic AMP receptor protein and cyclic di-GMP signaling in Vibrio cholerae biofilm formation. J. Bacteriol. 190, 6646–6659 (2008).
Jenal, U. Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr. Opin. Microbiol. 7, 185–191 (2004).
Cotter, P. A. & Stibitz, S. c-di-GMP-mediated regulation of virulence and biofilm formation. Curr. Opin. Microbiol. 10, 17–23 (2007).
Liang, X. et al. Bacterial cellulose synthesis gene regulates cellular c-di-GMP that control biofilm formation and mussel larval settlement. Int. Biodeterior. Biodegrad 165, 105330 (2021).
Huang, Y. L., Dobretsov, S., Xiong, H. & Qian, P. Y. Effect of biofilm formation by Pseudoalteromonas spongiae on induction of larval settlement of the polychaete Hydroides elegans. Appl. Environ. Microbiol. 73, 6284–6288 (2007).
Wang, R. et al. Exploring the influence of signal molecules on marine biofilms development. Front. Microbiol. 11, 571400 (2020).
Wahl, M. & Lafargue, F. Marine epibiosis. Oecologia 82, 275–282 (1990).
Koren, O. & Rosenberg, E. Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl. Environ. Microbiol. 72, 5254–5259 (2006).
Trias, R. et al. Abundance and composition of epiphytic bacterial and archaeal ammonia oxidizers of marine red and brown macroalgae. Appl. Environ. Microbiol. 78, 318–325 (2012).
Lee, O. O. et al. Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME J. 5, 650–664 (2011). This is one of the first studies that applied pyrosequencing techniques to study the species diversity of epibiotic bacterial communities in different species of sponges.
Lachnit, T., Wahl, M. & Harder, T. Isolated thallus-associated compounds from the macroalga Fucus vesiculosus mediate bacterial surface colonization in the field similar to that on the natural alga. Biofouling 26, 247–255 (2009).
Sapp, M., Wichels, A., Wiltshire, K. H. & Gerdts, G. Bacterial community dynamics during the winter-spring transition in the North Sea. FEMS Microbiol. Ecol. 59, 622–637 (2007).
Liu, Y. et al. A deep dive into the epibiotic communities on aquacultured sugar kelp Saccharina latissima in southern New England. Algal Res. 63, 102654 (2022).
Berggren, H. et al. Fish skin microbiomes are highly variable among individuals and populations but not within individuals. Front. Microbiol. 12, 12767770 (2022).
Leinberger, J. et al. Microbial epibitic community of the deep-sea galatheid sqaat lobster Munidopsis alvisca. Sci. Rep. 12, 2675 (2022).
Bermont-Bouis, D., Janvier, M., Grimont, P., Dupont, I. & Vallaeys, T. Both sulfate-reducing bacteria and Enterobacteriaceae take part in marine biocorrosion of carbon steel. J. Appl. Microbiol. 102, 161–168 (2007).
Zhang, Y. et al. Analysis of marine microbial communities colonizing various metallic materials and rust layers. Biofouling 35, 429–442 (2019).
Li, X. et al. Analysis of bacterial community composition of corroded steel immersed in Sanya and Xiamen seawaters in China via method of Illumina MiSeq sequencing. Front. Microbiol. 8, 1737 (2017).
Garrison, C. E. & Field, E. K. Introducing a “core steel microbiome” and community functional analysis associated with microbially influenced corrosion. FEMS Microbiol. Ecol. 97, fiaa237 (2021).
McCully, A. L. & Spormann, A. M. Direct cathodic electron uptake coupled to sulfate reduction by Desulfovibrio ferrophilus IS5 biofilms. Environ. Microbiol. 22, 4794–4807 (2020).
Procópio, L. The era of ‘omics’ technologies in the study of microbiologically influenced corrosion. Biotech. Lett. 42, 341–356 (2020).
Dou, W. W. et al. Corrosion of Cu by a sulfate reducing bacterium in anaerobic vials with different headspace volumes. Bioelectrochemistry 133, 107478 (2020).
Loto, C. A. Microbiological corrosion: mechanism, control and impact-a review. Int. J. Adv. Manuf. Technol. 92, 4241–4252 (2017).
Procópio, L. The role of biofilms in the corrosion of steel in marine environments. World J. Microbiol. Biotechnol. 35, 73 (2019).
Dinh, H. T. et al. Iron corrosion by novel anaerobic microorganisms. Nature 427, 829–832 (2004).
Enning, D. et al. Marine sulfate-reducing bacteria cause serious corrosion of iron under electroconductive biogenic mineral crust. Environ. Microbiol. 14, 1772–1787 (2012).
Tang, H. Y. et al. Stainless steel corrosion via direct iron-to-microbe electron transfer by Geobacter species. ISME J. 15, 3084–3093 (2021). This study proves that direct iron-to-microorganism electron transfer exists in stainless steel corrosion.
Flemming, H. C. In Biofilm highlights (eds Flemming, H. C., Wingender, J. & Szewzyk, U.) 81–109 (Springer Berlin Heidelberg, 2011).
Ma, Y. et al. Microbiologically influenced corrosion of marine steels within the interaction between steel and biofilms: a brief view. Appl. Microbiol. Biotech. 104, 515–525 (2020).
Zuo, R. J. Biofilms: strategies for metal corrosion inhibition employing microorgansims. Appl. Microbiol. Biotech. 76, 1245–1253 (2007).
Kip, N. & van Veen, J. A. The dual role of microbes in corrosion. ISME J. 9, 542–551 (2014). This is one of the good summaries of microbially influenced corrosion on different materials.
Videla, H. A. & Herrera, L. K. Understanding microbial inhibition of corrosion. A comprehensive overview. Int. Biodeterior. Biodegrad. 62, 896–900 (2009).
Beech, I. B. & Campbell, S. A. Accelerated low water corrosion of carbon steel in the presence of biofilm harbouring sulphate-reducing and sulphur-oxidising bacteria recovered from a marine sediments. Electrochim. Acta 54, 14–21 (2008).
Cavalcanti, G. S., Alker, A. T., Delherbe, N., Malter, K. E. & Shikuma, N. J. The influence of bacteria on animal metamorphosis. Annu. Rev. Microbiol. 76, 137–158 (2020).
Duan, J. et al. Corrosion of carbon steel influenced by anaerobic biofilm in natural seawater. Electrochim. Acta 54, 22–28 (2008).
Chongdar, S., Gunasekaran, G. & Kumar, P. Corrosion inhibition of mild steel by aerobic biofilm. Electrochim. Acta 50, 4655–4665 (2005).
Wieczorek, S. K., Clare, A. S. & Todd, C. D. Inhibitory and facilitatory effects of microbial films on settlement of Balanus amphitrite larvae. Mar. Ecol. Prog. Ser. 119, 221–228 (1995).
Hadfield, M. G. Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Annu. Rev. Mar. Sci. 3, 453–470 (2011). This review highlights that biofilm bacteria are a source of settlement cues and larvae are bearers of receptors for bacterial cues.
Holmstrom, C., Rittschof, D. & Kjelleberg, S. Inhibition of settlement of larvae of Balanus amphitrite and Ciona intestinalis by a surface-colonizing marine bacterium. Appl. Environ. Microbiol. 58, 2111–2115 (1992).
O’Connor, N. J. & Richarson, D. L. Attachment of barnacle (Balanus amphitrite Darwin) larvae: responses to bacterial films and extracellular materials. J. Exp. Mar. Biol. Ecol. 226, 115–129 (1998).
Harder, T., Lam, C. K. S. & Qian, P. Y. Induction of larval settlement of the polychaete Hydroides elegans (Haswell) by marine biofilms: an investigation of monospecific fouling diatoms as settlement cues. Mar. Ecol. Prog. Ser. 229, 105–112 (2002).
Unabia, C. R. C. & Hadfield, M. G. Role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans. Mar. Biol. 133, 55–64 (1999).
Huang, S. Y. & Hadfield, M. G. Composition and density of bacterial biofilms determine larval settlement of the polychaete Hydroides elegans. Mar. Ecol. Prog. Ser. 260, 161–172 (2003).
Maki, J. S., Rittschof, D., Costlow, J. D. & Mitchell, R. Inhibition of attachment of larval barnacles, Balanus amphitrite, by bacterial surface films. Mar. Biol. 97, 199–206 (1988).
Olivier, F., Tremblay, R., Bourget, E. & Ritschoff, D. Barnacle settlement: field experiments on the influence of larval supply, tidal level, biofilm quality and age on Balanus Amphitrite cyprids. Mar. Ecol. Prog. Ser. 199, 185–204 (2000).
Lau, S. C. K., Thiyagarajan, V., Cheung, S. C. K. & Qian, P. Y. Roles of bacterial community composition in biofilms as a mediator for larval settlement of three marine invertebrates. Aquat. Microb. Ecol. 38, 41–51 (2005).
Hung, O. S., Thiyagarajan, V., Zhang, R., Wu, R. S. S. & Qian, P. Y. Attachment of Balanus amphitrite larvae to biofilms originated from contrasting environments. Mar. Ecol. Prog. Ser. 333, 229–242 (2007).
Norton, T. A. et al. Using confocal laser scanning microscopy, scanning electron microscopy and phase contrast light microscopy to examine marine biofilms. Aquat. Microb. Ecol. 16, 199–204 (1998).
Joint, I., Tait, K. & Wheeler, G. Cross-kingdom signalling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Philos. Trans. R. Soc. Lond. B 362, 1223–1233 (2007).
Wheeler, G. L., Tait, K., Taylor, A., Brownlee, C. & Joint, I. Acyl-homoserine lactones modulate the settlement rate of zoospores of the marine alga Ulva intestinalis via a novel chemokinetic mechanism. Plant Cell Environ. 29, 608–618 (2006).
Tait, K. et al. Turnover of quorum sensing signal molecules modulates cross-kingdom signalling. Environ. Microbiol. 11, 1792–1802 (2009).
Shikuma, N. & Hadfield, M. G. Temporal variation of an initial marine biofilm community and its effects on larval settlement and metamorphosis of the tubeworm Hydroides elegans. Biofilms 2, 231–238 (2005).
Shikuma, N. J. et al. Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures. Science 343, 529–533 (2014). This study shows a novel form of interaction between biofouling animals and biofilm bacteria.
Ding, W. et al. Distribution, diversity and functional dissociation of the mac genes in marine biofilms. Biofouling 35, 230–243 (2019).
Qian, P. Y., Lau, S. C. K., Dahms, H. U., Harder, T. & Dobretsov, S. Marine biofilms as mediators of colonization by marine macroorganisms implications for antifouling and aquaculture. Mar. Biotech. 9, 399–410 (2007).
Intergovernmental Maritime Organisation. International convention on the control of harmful anti-fouling systems on ships https://www.imo.org/en/About/Conventions/Pages/International-Convention-on-the-Control-of-Harmful-Anti-fouling-Systems-on-Ships-(AFS).aspx (2008).
Schultz, M. P., Bendick, J. A., Holm, E. R. & Hertel, W. M. Economic impact of biofouling on a naval surface ship. Biofouling 27, 87–98 (2011).
Bannister, J., Sievers, M., Bush, F. & Bloecher, N. Biofouling in marine aquaculture: a review of recent research and developments. Biofouling 35, 631–648 (2019).
Lane, A. & Willemsen, P. Collaborative effort looks into biofouling. Fish. Farming Int. 44, 34–35 (2004).
Fitridge, I., Dempster, T., Guenther, J. & de Nys, R. The impact and control of biofouling in marine aquaculture: a review. Biofouling 28, 649–669 (2012).
Seneviratne, C. J. et al. Multi-omics tools for studying microbial biofilms: current perspectives and future directions. Crit. Rev. Microbiol. 46, 759–778 (2020).
Blattman, S. B., Jiang, W., Oikonomou, P. & Tavazoie, S. Prokaryotic single-cell RNA sequencing by in situ combinatorial indexing. Nat. Microbiol. 5, 1192–1201 (2020).
Kreth, J., Abdelrahman, Y. M. & Merritt, J. Multiplex imaging of polymicrobial communities-murine models to study oral microbiome interactions. Methods Mol. Biol. 2081, 107–126 (2020).
Bellin, D. L. et al. Electrochemical camera chip for simultaneous imaging of multiple metabolites in biofilms. Nat. Commun. 7, 10535 (2016).
Boldelon, G. et al. Detection and imaging of quorum sensing in Pseudomonas aeruginosa biofilm communities by surface-enhanced resonance Raman scattering. Nat. Mater. 15, 1203–1211 (2016).
Geier, B. et al. Spatial metabolomics of in situ host-microbe interactions at the micrometer scale. Nat. Microbiol. 5, 498–510 (2020).
Dobretsov, S. et al. The oceans are changing: impact of ocean warming and acidification on biofouling communities. Biofouling 35, 585–595 (2019).
Doney, S. C. et al. Climate change impacts on marine ecosystems. Annu. Rev. Mar. Sci. 4, 11–37 (2012).
Beech, I. B. & Sunner, J. Biocorrosion: towards understanding interactions between biofilms and metals. Cur. Opin. Biotech. 15, 181–186 (2004).
The authors are thankful for financial support from the Major Project of Basic and Applied Basic Research of Guangdong Province (2019B030302004), Key Special Project for Introduced Talents Team of the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD409), the Hong Kong Branch of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (SMSEGL20SC01), and Hong Kong Special Administrative Region (16101269, C6026-19G-A).
The authors declare no competing interests.
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Biofouling is the colonization of submerged surfaces by microorganisms, plants, algae or small animals; it has destructive effects on the substrate.
Biocorrosion refers to the deterioration of metal surfaces owing to the presence of biofilms.
Aquaculture refers to the rearing of aquatic animals or the cultivation of aquatic plants, including breeding, raising and harvesting, for the production of food and commercial products, restoring and creating healthier habitats as well as rebuilding threatened or endangered species populations.
- Marine snow
Small organic detritus and inorganic particles drifting towards the seafloor from the upper layers of the water column. Marine snow is formed by dead organisms, faecal matter, sand, soot and other dust.
Metamorphosis refers to a biological process of evident and sudden change in animal body structure through cell growth and differentiation after birth or hatching.
- Surface wettability
Surface wettability is the tendency of a liquid to spread on or adhere to a solid surface. It is controlled by a balance between adhesive (liquid–surface) and cohesive (liquid–liquid) forces.
- Marine benthos
Organisms that are living in or on the surface of the continental shelf and seafloor (sediments and rocks).
The formation of complex benthic community on man-made marine surfaces after biofilm formation, leading to the substantial build-up of biological and abiotic materials that affects the performance and function of marine surfaces.
Biofilm development on man-made marine surfaces, leading to changes in the physical and chemical properties of the surfaces.
- Phage tail-like structures
Protein structures produced by Pseudoalteromonas luteoviolacea that can stimulate larval metamorphosis of the tube-building polychaete Hydroides elegans.
- Microbial fuel cells
In a fuel cell system, the microbes on the anode oxidize reduced compounds (known as fuel or electron donors) and divert electrons to high-energy oxidized compounds (also known as oxidizing agents or electron acceptors) on the cathode to generate an electric current through an external electrical circuit.
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Qian, PY., Cheng, A., Wang, R. et al. Marine biofilms: diversity, interactions and biofouling. Nat Rev Microbiol 20, 671–684 (2022). https://doi.org/10.1038/s41579-022-00744-7