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Responses of Intertidal Bacterial Biofilm Communities to Increasing pCO2

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Abstract

The effects of ocean acidification on ecosystems remain poorly understood, because it is difficult to simulate the effects of elevated CO2 on entire marine communities. Natural systems enriched in CO2 are being used to help understand the long-term effects of ocean acidification in situ. Here, we compared biofilm bacterial communities on intertidal cobbles/boulders and bedrock along a seawater CO2 gradient off Japan. Samples sequenced for 16S rRNA showed differences in bacterial communities with different pCO2 and between habitat types. In both habitats, bacterial diversity increased in the acidified conditions. Differences in pCO2 were associated with differences in the relative abundance of the dominant phyla. However, despite the differences in community composition, there was no indication that these changes would be significant for nutrient cycling and ecosystem function. As well as direct effects of seawater chemistry on the biofilm, increased microalgal growth and decreased grazing may contribute to the shift in bacterial composition at high CO2, as documented by other studies. Thus, the effects of changes in bacterial community composition due to globally increasing pCO2 levels require further investigation to assess the implications for marine ecosystem function. However, the apparent lack of functional shifts in biofilms along the pCO2 gradient is a reassuring indicator of stability of their ecosystem functions in shallow ocean margins.

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References

  • Agostini S, Harvey BP, Wada S, Kon K, Milazzo M, Inaba K, Hall-Spencer JM (2018) Ocean acidification drives community shifts towards simplified non-calcified habitats in a subtropical−temperate transition zone. Sci Rep 8:11354

    PubMed  PubMed Central  Google Scholar 

  • Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5:782

    CAS  PubMed  Google Scholar 

  • Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343

    PubMed  Google Scholar 

  • Brown NE, Milazzo M, Rastrick SP, Hall-Spencer JM, Therriault TW, Harley CD (2018) Natural acidification changes the timing and rate of succession, alters community structure, and increases homogeneity in marine biofouling communities. Glob Chang Biol 24:e112–e127

    PubMed  Google Scholar 

  • Chun J, Lee J-H, Jung Y, Kim M, Kim S, Kim BK, Lim Y-W (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261

    CAS  PubMed  Google Scholar 

  • Connell SD, Kroeker KJ, Fabricius KE, Kline DI, Russell BD (2013) The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance. Philos Trans R Soc Lond B Biol Sci 368:20120442

    PubMed  PubMed Central  Google Scholar 

  • Cornwall CE, Revill AT, Hall-Spencer JM, Milazzo M, Raven JA, Hurd CL (2017) Inorganic carbon physiology underpins macroalgal responses to elevated CO2. Sci Rep 7:46297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Das S, Mangwani N (2015) Ocean acidification and marine microorganisms: responses and consequences. Oceanologia 57:349–361

    Google Scholar 

  • De Carvalho CC (2018) Marine biofilms: a successful microbial strategy with economic implications. Front Mar Sci 5:126

    Google Scholar 

  • Decho AW (2000) Microbial biofilms in intertidal systems: an overview. Cont Shelf Res 20:1257–1273

    Google Scholar 

  • Dickson AG (1990) Thermodynamics of the dissociation of boric acid in potassium chloride solutions from 273.15 to 318.15 K. J Chem Eng Data 35:253–257

    CAS  Google Scholar 

  • Dickson A, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part A 34:1733–1743

    CAS  Google Scholar 

  • Dong K, Tripathi B, Moroenyane I, Kim W, Li N, Chu H, Adams J (2016) Soil fungal community development in a high Arctic glacier foreland follows a directional replacement model, with a mid-successional diversity maximum. Sci Rep 6:26360

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

  • Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang 1:165

  • Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550

  • Hall-Spencer JM, Harvey BP (2019) Ocean acidification impacts on coastal ecosystem services due to habitat degradation. Emerging Top Life Sci 3:197–206

  • Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia M-C (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96

  • Hassenrück C, Hofmann LC, Bischof K, Ramette A (2015) Seagrass biofilm communities at a naturally CO2-rich vent. Environ Microbiol Rep 7:516–525

    PubMed  PubMed Central  Google Scholar 

  • Hassenrück C, Fink A, Lichtschlag A, Tegetmeyer HE, De Beer D, Ramette A (2016) Quantification of the effects of ocean acidification on sediment microbial communities in the environment: the importance of ecosystem approaches. FEMS Microbiol Ecol 92:fiw027

    PubMed  PubMed Central  Google Scholar 

  • Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson VR, Brownlee C, Milazzo M, Hall-Spencer JM (2015) Marine microphytobenthic assemblage shift along a natural shallow-water CO2 gradient subjected to multiple environmental stressors. J Mar Sci Eng 3:1425–1447

    Google Scholar 

  • Joint I, Doney SC, Karl DM (2011) Will ocean acidification affect marine microbes? ISME J 5:1

    PubMed  Google Scholar 

  • Kerfahi D, Hall-Spencer JM, Tripathi BM, Milazzo M, Lee J, Adams JM (2014) Shallow water marine sediment bacterial community shifts along a natural CO2 gradient in the Mediterranean Sea Off Vulcano, Italy. Microb Ecol 67:819–828

    CAS  PubMed  Google Scholar 

  • Krause E, Wichels A, Giménez L, Lunau M, Schilhabel MB, Gerdts G (2012) Small changes in pH have direct effects on marine bacterial community composition: a microcosm approach. PLoS One 7:e47035

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kroeker KJ, Gambi MC, Micheli F (2013) Community dynamics and ecosystem simplification in a high-CO2 ocean. Proc Natl Acad Sci 110:12721–12726

    CAS  PubMed  PubMed Central  Google Scholar 

  • Langille MGI, Zaneveld J, Caporaso JG, Mcdonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821.

  • Lau SC, Thiyagarajan V, Cheung SC, Qian P-Y (2005) Roles of bacterial community composition in biofilms as a mediator for larval settlement of three marine invertebrates. Aquat Microb Ecol 38:41–51

    Google Scholar 

  • Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415

    CAS  Google Scholar 

  • Lewis JR (1964) The ecology of rocky shores. English Universities Press

  • Lidbury I, Johnson V, Hall-Spencer JM, Munn CB, Cunliffe M (2012) Community-level response of coastal microbial biofilms to ocean acidification in a natural carbon dioxide vent ecosystem. Mar Pollut Bull 64:1063–1066

    CAS  PubMed  Google Scholar 

  • Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F, Chaffron S, Ignacio-Espinosa JC, Roux S, Vincent F (2015) Determinants of community structure in the global plankton interactome. Science 348:1262073

    PubMed  Google Scholar 

  • Lin X, Huang R, Li Y, Li F, Wu Y, Hutchins DA, Dai M, Gao K (2018) Interactive network configuration maintains bacterioplankton community structure under elevated CO2 in a eutrophic coastal mesocosm experiment. Biogeosciences 15:551–565

    CAS  Google Scholar 

  • Lindh MV, Riemann L, Baltar F, Romero-Oliva C, Salomon PS, Granéli E, Pinhassi J (2013) Consequences of increased temperature and acidification on bacterioplankton community composition during a mesocosm spring bloom in the Baltic Sea. Environ Microbiol Rep 5:252–262

    CAS  PubMed  Google Scholar 

  • Liu J, Weinbauer MG, Maier C, Dai M, Gattuso J-P (2010) Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aquat Microb Ecol 61:291–305

    Google Scholar 

  • Mehrbach C, Culberson CH, Hawley JE, Pytkowicx RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    CAS  Google Scholar 

  • Mendes LW, Kuramae EE, Navarrete AA, Van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1577–1587

  • Meron D, Rodolfo-Metalpa R, Cunning R, Baker AC, Fine M, Banin E (2012) Changes in coral microbial communities in response to a natural pH gradient. ISME J 6:1775

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morrow KM, Bourne DG, Humphrey C, Botté ES, Laffy P, Zaneveld J, Uthicke S, Fabricius KE, Webster NS (2014) Natural volcanic CO2 seeps reveal future trajectories for host–microbial associations in corals and sponges. ISME J 9:894

  • O’brien PA, Morrow KM, Willis BL, Bourne DG (2016) Implications of ocean acidification for marine microorganisms from the free-living to the host-associated. Front Mar Sci 3:47

    Google Scholar 

  • Oksanen, J., Kindt, R., Legendre, P., O’hara, B., Stevens, M.H.H., Oksanen, M.J. & Suggests, M. (2007). The vegan package. Community ecology package. 10:631–637

  • Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pierrot D, Lewis E, Wallace D (2006) CO2SYS DOS Program developed for CO2 system calculations. ORNL/CDIAC-105 Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge

    Google Scholar 

  • Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Biol Ecol 400:278–287

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Rastrick SSP, Graham H, Azetsu-Scott K, Calosi P, Chierici M, Fransson A, Hop H, Hall-Spencer J, Milazzo M, Thor P, Kutti T, Woodson HECB (2018) Using natural analogues to investigate the effects of climate change and ocean acidification on northern ecosystems. ICES J Mar Sci 75:2299–2311

    Google Scholar 

  • Riebesell U, Gattuso J-P (2014) Lessons learned from ocean acidification research. Nat Clim Chang 5:12

    Google Scholar 

  • Rodríguez-Gironés MA, Santamaría L (2006) A new algorithm to calculate the nestedness temperature of presence–absence matrices. J Biogeogr 33:924–935

    Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sunday JM, Fabricius KE, Kroeker KJ, Anderson KM, Brown NE, Barry JP, Connell SD, Dupont S, Gaylord B, Hall-Spencer JM, Klinger T, Milazzo M, Munday PL, Russell BD, Sanford E, Thiyagarajan V, Vaughan MLH, Widdicombe S, Harley CDG (2016) Ocean acidification can mediate biodiversity shifts by changing biogenic habitat. Nat Clim Chang 7:81

  • Taylor JD, Ellis R, Milazzo M, Hall-Spencer JM, Cunliffe M (2014) Intertidal epilithic bacteria diversity changes along a naturally occurring carbon dioxide and pH gradient. FEMS Microbiol Ecol 89:670–678

    CAS  PubMed  Google Scholar 

  • Tolker-Nielsen T, Molin S (2000) Spatial organization of microbial biofilm communities. Microb Ecol 40:75–84

    CAS  PubMed  Google Scholar 

  • Tripathi BM, Kim M, Singh D, Lee-Cruz L, Lai-Hoe A, Ainuddin A, Go R, Rahim RA, Husni M, Chun J (2012) Tropical soil bacterial communities in Malaysia: pH dominates in the equatorial tropics too. Microb Ecol 64:474–484

    PubMed  Google Scholar 

  • Uppström LR (1974) The boron/chlorinity ratio of deep-sea water from the Pacific Ocean. Deep Sea Res Oceanogr Abstr 21:161–162

  • Wagg C, Bender SF, Widmer F, Van Der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci 111:5266–5270

    CAS  PubMed  PubMed Central  Google Scholar 

  • Webster N, Negri A, Flores F, Humphrey C, Soo R, Botte E, Vogel N, Uthicke S (2013) Near-future ocean acidification causes differences in microbial associations within diverse coral reef taxa. Environ Microbiol Rep 5:243–251

    CAS  PubMed  Google Scholar 

  • Webster N, Negri A, Botté E, Laffy P, Flores F, Noonan S, Schmidt C, Uthicke S (2016) Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci Rep 6:19324

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weinbauer MG, Mari X, Gattuso J-P (2011) Effect of ocean acidification on the diversity and activity of heterotrophic marine microorganisms. Ocean acidification. Oxford University Press, Oxford, pp 83–98

  • Williams GA, Davies MS, Nagarkar S (2000) Primary succession on a seasonal tropical rocky shore: the relative roles of spatial heterogeneity and herbivory. Mar Ecol Prog Ser 203:81–94

    Google Scholar 

  • Witt V, Wild C, Anthony KR, Diaz-Pulido G, Uthicke S (2011) Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the Great Barrier Reef. Environ Microbiol 13:2976–2989

    CAS  PubMed  Google Scholar 

  • Wootton JT, Pfister CA, Forester JD (2008) Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proc Natl Acad Sci 105:18848–18853

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Dr. Rich Boden, University of Plymouth, UK for his suggestions in improving the paper. We also thank Dr. Matthew Chidozie Ogwe, University of Camerino, Italy for his assistance on data analyses and paper editing.

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Kerfahi, D., Harvey, B.P., Agostini, S. et al. Responses of Intertidal Bacterial Biofilm Communities to Increasing pCO2. Mar Biotechnol 22, 727–738 (2020). https://doi.org/10.1007/s10126-020-09958-3

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