Ocean acidification and marine microorganisms : responses and consequences

• Autorzy: Das S. , Mangwani N.

Identyfikatory

DOI

10.1016/j.oceano.2015.07.003

• Języki publikacji: EN

Abstrakty

EN

Ocean acidification (OA) is one of the global issues caused by rising atmospheric CO₂. The rising pCO₂ and resulting pH decrease has altered ocean carbonate chemistry. Microbes are key components of marine environments involved in nutrient cycles and carbon flow in marine ecosystems. However, these marine microbes and the microbial processes are sensitive to ocean pH shift. Thus, OA affects the microbial diversity, primary productivity and trace gases emission in oceans. Apart from that, it can also manipulate the microbial activities such as quorum sensing, extracellular enzyme activity and nitrogen cycling. Short-term laboratory experiments, mesocosm studies and changing marine diversity scenarios have illustrated undesirable effects of OA on marine microorganisms and ecosystems. However, from the microbial perspective, the current understanding on effect of OA is based mainly on limited experimental studies. It is challenging to predict response of marine microbes based on such experiments for this complex process. To study the response of marine microbes towards OA, multiple approaches should be implemented by using functional genomics, new generation microscopy, small-scale interaction among organisms and/or between organic matter and organisms. This review focuses on the response of marine microorganisms to OA and the experimental approaches to investigate the effect of changing ocean carbonate chemistry on microbial mediated processes.

Słowa kluczowe

EN

Ocean acidification; climate change; Marine microorganisms; ecosystem; mesocosm

• Wydawca: Polish Academy of Sciences, Institute of Oceanology ; Elsevier
• Czasopismo: Oceanologia
• Rocznik: 2015
• Tom: No. 57 (4)
• Strony: 349--361
• Opis fizyczny: Bibliogr. 160 poz., rys., tab.

Twórcy

autor

Das S.

• Department of Life Science, National Institute of Technology, Rourkela, India

autor

Mangwani N.

• Department of Life Science, National Institute of Technology, Rourkela, India

Bibliografia

• Abbasi, T., Abbasi, S.A., 2011. Ocean acidification: the newest threat to the global environment. Crit. Rev. Environ. Sci. Technol. 41 (18), 1601—1663.
• Allgaier, M., Riebesell, U., Vogt, M., Thyrhaug, R., Grossart, H.P., 2008. Coupling of heterotrophic bacteria to phytoplankton bloom development at different pCO2 levels: a mesocosm study. Biogeosciences 5, 1007—1022.
• Anthony, K.R.N., Kline, D.I., Diaz-Pulido, G., Dove, S., Hoegh- Guldberg, O., 2008. Ocean acidification causes bleaching and productivity loss in coral reef builders. PNAS 105, 17442—17446.
• Archer, S.D., Kimmance, S.A., Stephens, J.A., Hopkins, F.E., Bellerby, R.G.J., Schulz, K.G., Piontek, J., Engel, A., 2013. Contrasting responses of DMS and DMSP to ocean acidification in Arctic waters. Biogeosciences 10, 1893—1908.
• Arnosti, C., 2011. Microbial extracellular enzymes and the marine carbon cycle. Annu. Rev. Mar. Sci. 3, 401—425.
• Azam, F., Malfatti, F., 2007. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782—791.
• Badger, M.R., Price, G.D., Long, B.M., Woodger, F.J., 2006. The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. J. Exp. Bot. 57 (2), 249—265.
• Barcelos e Ramos, J., Biswas, H., Schulz, K.G., LaRoche, J., Riebesell, U., 2007. Effect of rising atmospheric carbon dioxide on the marine nitrogen fixer Trichodesmium. Global Biogeochem. Cy. 21 (2), http://dx.doi.org/10.1029/2006GB002898.
• Barnes, R.S.K., Hughes, R.N., 1988. An Introduction to Marine Ecology. Blackwell Scientific Publications.
• Beaufort, L., Probert, I., de Garidel-Thoron, T., Bendif, E.M., Ruiz- Pino, D., Metzl, N., Goyet, C., Buchet, N., Coupel, P., Grelaud, M., Rost, B., Rickaby, R.E., de Vargas, C., 2011. Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476 (7358), 80—83.
• Beerling, D.J., Hewitt, C.N., Pyle, J.A., Raven, J.A., 2007. Critical issues in trace gas biogeochemistry and global change. Phil. Trans. R. Soc. A 365 (1856), 1629—1642.
• Beman, J.M., Chow, C.E., King, A.L., Feng, Y., Fuhrman, J.A., Andersson, A., Bates, N.R., Popp, B.N., Hutchins, D.A., 2011. Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc. Natl. Acad. Sci. U.S.A. 108, 208—213.
• Berelson, W.M., Balch, W.M., Najjar, R., Feely, R.A., Sabine, C., Lee, K., 2007. Relating estimates of CaCO3 production, export, and dissolution in the water column to measurements of CaCO3 rain into sediment traps and dissolution on the sea floor: a revised global carbonate budget. Global Biogeochem. Cy. 21, GB1024, http://dx.doi.org/10.1029/2006GB002803.
• Boyd, P.W., Sherry, N.D., Berges, J.A., Bishop, J.K.B., Calvert, S.E., Charette, M.A., Giovannoni, S.J., Goldblatt, R., Harrison, P.J., Moran, S.B., Roy, S., Soon, M., Strom, S., Thibault, D., Vergin, K. L., Whitney, F.A., Wong, C.S., 1999. Transformations of biogenic particulates from the pelagic to the deep ocean realm. Deep-Sea Res. Pt. II 46, 2761—2792.
• Brewer, P.G., 1997. Ocean chemistry of the fossil fuel CO2 signal: the haline signature of “Business as usual”. Geophys. Res. Lett. 24, 1367—1369.
• Brewer, P.G., 2013. A different ocean acidification hazard — the Kolumbo submarine volcano example. Geology 41 (9), 1039—1040.
• Burns, R.A., MacDonald, C.D., McGinn, P.J., Campbell, D., 2005. Inorganic carbon repletion disrupts photosynthetic acclimation to low temperature in the cyanobacterium Synechococcus elongatus S1. J. Phycol. 41 (2), 322—334.
• Caldeira, K., Wickett, M.E., 2003. Anthropogenic carbon and ocean pH. Nature 425, 365.
• Capone, D.G., Burns, J.A., Montoya, J.P., Subramaniam, A., Mahaffey, C., Gunderson, Y., Michaels, A.F., Carpenter, E.J., 2005. Nitrogen fixation by Trichodesmium spp.: an important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Global Biogeochem. Cy., http://dx.doi.org/10.1029/ 2004gb002331.
• Capone, D.G., Hutchins, D.A., 2013. Microbial biogeochemistry of coastal upwelling regimes in a changing ocean. Nat. Geosci. 6, 711—717.
• Carpenter, L.J., Archer, S.D., Beale, R., 2012. Ocean-atmosphere trace gas exchange. Chem. Soc. Rev. 41 (19), 6473—6506.
• Chavez, F.P., Messié, M., Pennington, J.T., 2011. Marine primary production in relation to climate variability and change. Annu. Rev. Mar. Sci. 3, 227—260.
• Chong, G., Kimyon, O., Rice, S.A., Kjelleberg, S., Manefield, M., 2012. The presence and role of bacterial quorum sensing in activated sludge. Microb. Biotechnol. 5 (5), 621—633.
• Collins, S., Rost, B., Rynearson, T.A., 2014. Evolutionary potential of marine phytoplankton under ocean acidification. Evol. Appl. 7 (1), 140—155.
• Cunha, A., Almeida, A., Coelho, F.J.R.C., Gomes, N.C.M., Oliveira, V., Santos, A.L., 2010. Bacterial extracellular enzymatic activity in globally changing aquatic ecosystems. In: Mendez-Vilas, A. (Ed.), Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology, vol. 1. FOR-MATEX, Spain, 124—135.
• Czerny, J., Barcelos e Ramos, J., Riebesell, U., 2009. Influence of elevated CO2 concentrations on cell division and nitrogen fixation rates in the bloom-forming cyanobacterium Nodularia spumigena. Biogeosciences 6, 1865—1875.
• Daley, S.M., Kappell, A.D., Carrick, M.J., Burnap, R.L., 2012. Regulation of the cyanobacterial CO2-concentrating mechanism involves internal sensing of NADP+ and α-ketoglutarate levels by transcription factor CcmR. PloS One 7 (7), e41286.
• Das, S., Lyla, P.S., Khan, S.A., 2006. Marine microbial diversity and ecology: importance and future perspectives. Curr. Sci. 90 (10), 1325—1335.
• Dash, H.R., Mangwani, N., Chakraborty, J., Kumari, S., Das, S., 2013. Marine bacteria: potential candidates for enhanced bioremediation. Appl. Microbiol. Biotechnol. 97 (2), 561—571.
• Dash, H.R., Mangwani, N., Das, S., 2014. Characterization and potential application in mercury bioremediation of highly mercury-resistant marine bacterium Bacillus thuringiensis PW-05. Environ. Sci. Pollut. Res. 21, 2642—2653.
• de Boer, M.L., Krupp, D.A., Weis, V.M., 2007. Proteomic and transcriptional analyses of coral larvae newly engaged in symbiosis with dinoflagellates. Comp. Biochem. Physiol. D2, 63—73.
• De Kievit, T.R., 2009. Quorum sensing in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 11 (2), 279—288.
• Dobretsov, S., Teplitski, M., Paul, V., 2009. Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25 (5), 413—427.
• Doney, S.C., Balch, W.M., Fabry, V.J., Feely, R.A., 2009a. Ocean acidification: a critical emerging problem for the ocean sciences. Oceanography 22, 16—25.
• Doney, S.C., Fabry, V.J., Feely, R.A., Kleypas, J.A., 2009b. Ocean acidification: the other CO2 problem. Annu. Rev. Mar. Sci. 1, 169—192.
• Dore, J.E., Lukas, R., Sadler, D.W., Church, M.J., Karl, D.M., 2009. Physical and biogeochemical modulation of ocean acidification in the central North Pacific. PNAS 106, 12235—12240.
• Dupont, S., Dorey, N., Thorndyke, M., 2010. What meta-analysis can tell us about vulnerability of marine biodiversity to ocean acidification? Estuar. Coast. Shelf Sci. 89, 182—185.
• Dutta, T.K., Jana, M., Pahari, P.R., Bhattacharya, T., 2006. The effect of temperature, pH, and salt on amylase in Heliodiaptomus viduus (Gurney) (Crustacea: Copepoda: Calanoida). Turk. J. Zool. 30, 187—195.
• Eggers, S.L., Lewandowska, A.M., Barcelos e Ramos, J., Blanco- Ameijeiras, S., Gallo, F., Matthiessen, B., 2014. Community composition has greater impact on the functioning of marine phytoplankton communities than ocean acidification. Glob. Change Biol. 20 (3), 713—723.
• Engel, A., Zondervan, I., Aerts, K., Beaufort, L., Benthien, A., Chou, L., Delille, B., Gattuso, J.P., Harlay, J., Heemann, C., Hoffmann, L., Jacquet, S., Nejstgaard, J., Pizay, M.D., Rochelle-Newall, E., Schneider, U., Terbrueggen, A., Riebesell, U., 2005. Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments. Limnol. Oceanogr. 50, 493—507.
• Fabry, V.J., Seibel, B.A., Feely, R.A., Orr, J.C., 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci. 65, 414—432.
• Fu, F.X., Warner, M.E., Zhang, Y., Feng, Y., Hutchins, D.A., 2007. Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (cyanobacteria). J. Phycol. 43 (3), 485—496.
• Gao, K., Helbling, E.W., Häder, D.P., Hutchins, D.A., 2012. Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar. Ecol. Prog. Ser. 470, 167—189.
• Gattuso, J.P., Allemand, D., Frankignoulle, M., 1999. Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Amer. Zool. 39, 160—183.
• Gattuso, J.P., Frankignoulle, M., Bourge, I., Romaine, S., Buddemeier, R.W., 1998. Effect of calcium carbonate saturation of seawater on coral calcification. Global Planet. Change 18 (1), 37—46.
• Generous, R.A., 2014. Environmental threats to the symbiotic relationship of coral reefs and quorum sensing. Consilience 11, 116—122.
• Gilbert, J.A., Field, D., Huang, Y., Edwards, R., Li, W., Gilna, P., Joint, I., 2008. Detection of large numbers of novel sequences in the metatranscriptomes of complex marine microbial communities. PLoS One 3, e3042.
• Golberg, K., Eltzov, E., Shnit-Orland, M., Marks, R.S., Kushmaro, A., 2011. Characterization of quorum sensing signals in coral-associated bacteria. Microb. Ecol. 61 (4), 783—792.
• Gracey, A.Y., 2007. Interpreting physiological responses to environmental change through gene expression profiling. J. Exp. Biol. 210, 1584—1592.
• Grossart, H.P., Allgaier, M., Passow, U., Riebesell, U., 2006. Testing the effect of CO2 concentration on the dynamics of marine heterotrophic bacterioplankton. Limnol. Oceanogr. 51, 1—11.
• Guinotte, J.M., Fabry, V.J., 2008. Ocean acidification and its potential effects on marine ecosystems. Ann. N.Y. Acad. Sci. 1134, 320—342.
• Gutowska, M.A., Pörtner, H.O., Melzner, F., 2008. Growth and calcification in the cephalopod Sepia officinalis under elevated sea-water pCO2. Mar. Ecol. Prog. Ser. 373, 303—309.
• Hein, M., Sand-Jensen, K., 1997. CO2 increases oceanic primary production. Nature 388, 526—527.
• Hill, R.W., White, B.A., Cottrell, M.T., Dacey, J.W., 1998. Virus- mediated total release of dimethylsulfoniopropionate from marine phytoplankton: a potential climate process. Aquat. Microb. Ecol. 14 (1), 1—6.
• Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greenfield, P., Gomez, E., Harvell, C.D., Sale, P.F., Edwards, A. J., Caldeira, K., Knowlton, N., Eakin, C.M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R.H., Dubi, A., Hatziolos, M.E., 2007. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737—1742.
• Hofmann, G.E., Barry, J.P., Edmunds, P.J., Gates, R.D., Hutchins, D. A., Klinger, K., Sewell, M.A., 2010. The effects of ocean acidification in polar, tropical and temperate marine calcifying organisms: an organism to ecosystem perspective. Annu. Rev. Ecol. Evol. Syst. 41, 127—147.
• Hofmann, G.E., Evans, T.G., Kelly, M.W., Padilla-Gamiño, J.L., Blanchette, C.A., Washburn, L., Chan, F., McManus, M.A., Menge, B.A., Gaylord, B., Hill, T.M., Sanford, E., LaVigne, M., Rose, J.M., Kapsenberg, L., Dutton, J.M., 2013. Exploring local adaptation and the ocean acidification seascape-studies in the California Current Large Marine Ecosystem. Biogeosci. Discuss. 10 (7), 11825—11856.
• Hofmann, G.E., O'Donnell, M.J., Todgham, A.E., 2008. Using functional genomics to explore the effects of ocean acidification on calcifying marine organisms. Mar. Ecol. Prog. Ser. 373, 219—222.
• Hopkins, F.E., Turner, S.M., Nightingale, P.D., Steinke, M., Bakker, D., Liss, P.S., 2010. Ocean acidification and marine trace gas emissions. Proc. Natl. Acad. Sci. U.S.A. 107, 760—765.
• Hutchins, D.A., Fu, F.X., Zhang, Y., Warner, M.E., Feng, Y., Portune, K., Bernhardt, P.W., Mulholland, M.R., 2007. CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr. 52 (4), 1293—1304.
• Hutchins, D.A., Mulholland, M.R., Fu, F., 2009. Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22 (4), 128—145.
• Ibrahim, H.A.H., El-Sayed, W.M.M., Shaltout, N.A., El-Shorbagi, E. K., 2014. Effects of different pCO2 concentrations on marine bacterial community structure, Eastern Harbor, Alexandria, Egypt. Life Sci J. 11, 781—789.
• Iglesias-Rodriguez, M.D., Halloran, P.R., Rickaby, R.E.M., Hall, I.R., Colmenero-Hidalgo, E., Gittins, J.R., Green, D.R.H., Tyrrell, T., Gibbs, S.J., von Dassow, P., Rehm, E., Armbrust, E.V., Boessenkool, K.P., 2008. Phytoplankton calcification in a high-CO2 world. Science 320, 336—340.
• Inbakandan, D., Sriyutha Murthy, P., Venkatesan, R., Ajmal Khan, S., 2010. 16S rDNA sequence analysis of culturable marine biofilm forming bacteria from a ship's hull. Biofouling 26 (8), 893—899.
• IPCC, 2013. Climate Change 2013: The Physical Science Basis, Summary for Policymakers. Intergovernmental Panel on Climate Change, Switzerland.
• Jain, K., Parida, S., Mangwani, N., Dash, H.R., Das, S., 2013. Isolation and characterization of biofilm-forming bacteria and associated extracellular polymeric substances from oral cavity. Ann. Microbiol. 63 (4), 1553—1562.
• Joint, I., Doney, S.C., Karl, D.M., 2011. Will ocean acidification affect marine microbes? ISME J. 5, 1—7.
• Joint, I., Karl, D.M., Doney, S.C., Armbrust, E., Balch, W., Beman, M., Bowler, C., Church, M., Dickson, A., Heidelberg, J., 2009. Consequences of high CO2 and ocean acidification for microbes in the global ocean. In: Symposium on Rising CO2, Ocean Acidification, and Their Impacts on Marine Microbes, 24—26 February 2009, Honolulu, HI.
• Kaplan, M.B., Mooney, T.A., McCorkle, D.C., Cohen, A.L., 2013. Adverse effects of ocean acidification on early development of squid (Doryteuthis pealeii). PLoS One 8 (5), e63714.
• Karvonen, A., Rintamäki, P., Jokela, J., Valtonen, E.T., 2010. Increasing water temperature and disease risks in aquatic systems: climate change increases the risk of some, but not all, diseases. Int. J. Parasitol. 40, 1483—1488.
• Keeling, P.J., Burki, F., Wilcox, H.M., Allam, B., Allen, E.E., Amaral- Zettler, L.A., Armbrust, E.V., Archibald, J.M., Bharti, A.K., Bell, C.J., Beszteri, B., Bidle, K.D., Cameron, C.T., Campbell, L., Caron, D.A., Cattolico, R.A., Collier, J.L., Coyne, K., Davy, S. K., Deschamps, P., Dyhrman, S.T., Edvardsen, B., Gates, R.D., Gobler, C.J., Greenwood, S.J., Guida, S.M., Jacobi, J.L., Jakobsen, K.S., James, E.R., Jenkins, B., John, U., Johnson, M.D., Juhl, A.R., Kamp, A., Katz, L.A., Kiene, R., Kudryavtsev, A., Leander, B. S., Lin, S., Lovejoy, C., Lynn, D., Marchetti, A., McManus, G., Nedelcu, A.M., Deuer, S.M., Miceli, C., Mock, T., Montresor, M., Moran, M.A., Murray, S., Nadathur, G., Nagai, S., Ngam, P.B., Palenik, B., Pawlowski, J., Petroni, G., Piganeau, G., Posewitz, M. C., Rengefors, K., Romano, G., Rumpho, M.E., Rynearson, T., Schilling, K.B., Schroeder, D.C., Simpson, A.G.B., Slamovits, C. H., Smith, D.R., Smith, G.J., Smith, S.R., Sosik, H.M., Stief, P., Theriot, E., Twary, S.N., Umale, P.E., Vaulot, D., Wawrik, B., Wheeler, G.L., Wilson, W.H., Xu, Y., Zingone, A., Worden, A.Z., 2014. The marine microbial eukaryote transcriptome sequencing project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLOS Biol., http://dx.doi.org/10.1371/journal.pbio.1001889.
• Keeling, R.F., Körtzinger, A., Gruber, N., 2010. Ocean deoxygenation in a warming world. Annu. Rev. Mar. Sci. 2, 199—229.
• Kennedy, D.M., Woodroffe, C.D., Jones, B.G., Dickson, M.E., Phipps, C.V.G., 2002. Carbonate sedimentation on subtropical shelves around Lord Howe Island and Balls Pyramid Southwest Pacific. Mar. Geol. 188, 333—349.
• Keough, M.J., Raimondi, P.T., 1995. Responses of settling invertebrate larvae to bioorganic films: effects of different types of films. J. Exp. Mar. Biol. Ecol. 185, 235—253.
• Koch, M., Bowes, G., Ross, C., Zhang, X.H., 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Change Biol. 19 (1), 103—132.
• Koch, S., 2007. Growth and calcification of the coccolithophore Emiliana huxleyi under different CO2 concentrations. (Diploma Thesis). Carl von Ossietzky Universität Oldenburg.
• Kranz, S., Sültemeyer, D., Richter, K.U., Rost, B., 2009. Carbon acquisition in Trichodesmium: the effect of pCO2 and diurnal changes. Limnol. Oceanogr. 54 (2), 548—559.
• Kranz, S.A., Levitan, O., Richter, K.U., Prášil, O., Berman-Frank, I., Rost, B., 2010. Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: physiological responses. Plant Physiol. 154 (1), 334—345.
• Krause, E., Wichels, A., Giménez, L., Lunau, M., Schilhabel, M.B., Gerdts, G., 2012. Small changes in pH have direct effects on marine bacterial community composition: a microcosm approach. PLoS One 7 (10), e47035, http://dx.doi.org/10.1371/journal. pone.0047035.
• Krediet, C.J., Ritchie, K.B., Paul, V.J., Teplitski, M., 2013. Coral-associated microorganisms and their roles in promoting coral health and thwarting diseases. Proc. R. Soc. A 280 (1755), 20122328.
• Kroeker, K.J., Kordas, R.L., Crim, R., Hendriks, I.E., Ramajo, L., Singh, G.S., Duarte, C.M., Gattuso, J.P., 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19 (6), 1884—1896.
• Labare, M., Bays, J.T., Butkus, M., Snyder-Leiby, T., Smith, A., Goldstein, A., Schwartz, J., Wilson, K., Ginter, M., Bare, E., Watts, R., Michealson, E., Miller, N., LaBranche, R., 2010. The effects of elevated carbon dioxide levels on a Vibrio sp. isolated from the deep-sea. Environ. Sci. Pollut. Res. 17, 1009—1015.
• Larsen, J.B., Larsen, A., Thyrhaug, R., Bratbak, G., Sandaa, R.A., 2008. Response of marine viral populations to a nutrient induced phytoplankton bloom at different pCO2 levels. Biogeosciences 5, 523—533.
• Lau, S.C.K., Mak, K.K.W., Chen, F., Qian, P.Y., 2002. 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.
• Lau, S.C.K., Thiyagarajan, V., Cheung, S.C.K., 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.
• Leclercq, N., Gattuso, J.P., Jaubert, J., 2000. CO2 partial pressure controls the calcification rate of a coral community. Glob. Change Biol. 6, 329—334.
• Lee, Y.K., Kim, H.W., Liu, C.L., Lee, H.K., 2003. A simple method for DNA extraction from marine bacteria that produce extracellular materials. J. Microbiol. Meth. 52 (2), 245—250.
• Levitan, O., Rosenberg, G., Setlik, I., Setlikova, E., Grigel, J., Klepetar, J., Prasil, O., Berman-Frank, I., 2007. Elevated CO2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob. Change Biol. 13 (2), 531—538.
• Lidbury, I., Johnson, V., Hall-Spencer, J.M., Munn, C.B., Cunliffe, M., 2012. Community-level response of coastal microbial biofilms to ocean acidification. Mar. Pollut. Bull. 64, 1063—1066.
• Liss, P.S., 2007. Trace gas emissions from the marine biosphere. Phil. Trans. Math. Phys. Eng. Sci. 365, 1697—1704.
• Liu, J., Weinbauer, M.G., 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.
• Lohbeck, K.T., Riebesell, U., Reusch, T.B., 2012. Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 5 (5), 346—351.
• Lomas, M.W., Hopkinson, B.M., Losh, J.L., Ryan, D.E., Shi, D.L., Xu, Y., Morel, F.M.M., 2012. Effect of ocean acidification on cyanobacteria in the subtropical North Atlantic. Aquat. Microb. Ecol. 66, 211—222.
• Maas, E.W., Law, C.S., Hall, J.A., Pickmere, S., Currie, K.I., Chang, F. H., Matt-Voyles, K., Caird, D., 2013. Effect of ocean acidification on bacterial abundance, activity and diversity in the Ross Sea, Antarctica. Aquat. Microb. Ecol. 70 (1), 1—15.
• Maki, J.S., Rittschof, D., Costlow, J.D., Mitchell, R., 1988. Inhibition of attachment of larval barnacles, Balanus amphitrite, by bacterial surface films. Mar. Biol. 97, 199—206.
• Manefield, M., Turner, S.L., 2002. Quorum sensing in context: out of molecular biology and into microbial ecology. Microbiology 148, 3762—3764.
• Manefield, M., Whiteley, A.S., 2007. Acylated homoserine lactones in the environment: chameleons of bioactivity. Phil. Trans. R. Soc. Lond. B: Biol. Sci. 362 (1483), 1235—1240.
• Mangwani, N., Dash, H.R., Chauhan, A., Das, S., 2012. Bacterial quorum sensing: functional features and potential applications in biotechnology. J. Mol. Microbiol. Biotechnol. 22 (4), 215—227.
• Mangwani, N., Kumari, S., Shukla, S.K., Rao, T.S., Das, S., 2014b. Phenotypic switching in biofilm-forming marine bacterium Paenibacillus lautus NE3B01. Curr. Microbiol. 68, 648—656.
• Mangwani, N., Shukla, S.K., Rao, T.S., Das, S., 2014a. Calcium-mediated modulation of Pseudomonas mendocina NR802 biofilm influences the phenanthrene degradation. Colloids Surf. B 114, 301—309.
• McCulloch, M., Falter, J., Trotter, J., Montagna, P., 2012. Coral resilience to ocean acidification and global warming through pH up-regulation. Nat. Clim. Change 2 (8), 623—627.
• Meron, D., Atias, E., Kruh, L.I., Elifantz, H., Minz, D., Fine, M., Banin, E., 2011. The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J. 5, 51—60.
• Meyer, J., Riebesell, U., 2015. Reviews and syntheses: responses of coccolithophores to ocean acidification: a meta-analysis. Biogeosciences 12, 1671—1682.
• Miller, M.B., Bassler, B.L., 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55 (1), 165—199.
• Mobley, D.M., Chengappa, M.M., Kadel, W.L., Stuart, J.G., 1984. Effect of pH, temperature and media on acid and alkaline phosphatase activity in “clinical” and “nonclinical” isolates of Bordetella bronchiseptica. Can. J. Comp. Med. 48, 175—178.
• Moisander, P.H., Serros, T., Paerl, R.W., Beinart, R.A., Zehr, J.P., 2014. Gammaproteobacterial diazotrophs and nifH gene expression in surface waters of the South Pacific Ocean. ISME J. 8, 1962—1973.
• Motegi, C., Tanaka, T., Piontek, J., Brussaard, C.P.D., Gattuso, J. P., Weinbauer, M.G., 2013. Effect of CO2 enrichment on bacterial metabolism in an Arctic fjord. Biogeosciences 10, 3285—3296.
• Nielsen, L.T., Jakobsen, H.H., Hansen, P.J., 2010. High resilience of two coastal plankton communities to twenty-first century seawater acidification: evidence from microcosm studies. Mar. Biol. Res. 6, 542—555.
• Orr, J.C., Fabry, V.J., Aumont, O., Bopp, L., Doney, S.C., Feely, R.A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R.M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R.G., Plattner, G.K., Rodgers, K.B., Sabine, C.L., Sarmiento, J.L., Schlitzer, R., Slater, R.D., Totterdell, I.J., Weirig, M.F., Yamanaka, Y., Yool, A., 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681—686.
• Partensky, F., Hess, W.R., Vaulot, D., 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63, 106—127.
• Piontek, J., Lunau, M., Handel, N., Borchard, C., Wurst, M., Engel, A., 2010. Acidification increases microbial polysaccharide degradation in the ocean. Biogeosciences 7, 1615—1624.
• Pomeroy, L.R., Williams, P.J.L., Azam, F., Hobbie, J.E., 2007. The microbial loop. Oceanography 20, 28—33.
• Price, N.N., Hamilton, S.L., Tootell, J.S., Smith, J.E., 2011. Species-specific consequences of ocean acidification for the calcareous tropical green algae Halimeda. Mar. Ecol. Prog. Ser. 440, 67—78.
• Qian, P.Y., Lau, S.C.K., Dahms, H.U., Dobretsov, S., Harder, T., 2007. Marine biofilms as mediators of colonization by marine microorganisms: implications for antifouling and aquaculture. Mar. Biotechnol. 9 (4), 399—410.
• Range, P., Chicharo, M.A., Ben-Hamadou, R., Pilo, D., Matias, D., Joaquim, S., Oliveira, A.P., Chicharo, L., 2011. Calcification, growth and mortality of juvenile clams Ruditapes decussatus under increased pCO2 and reduced pH: variable responses to ocean acidification at local scales. J. Exp. Biol. 396, 177—184.
• Ransome, E., Munn, C.B., Halliday, N., Cámara, M., Tait, K., 2013. Diverse profiles of N-acyl-homoserine lactone molecules found in cnidarians. FEMS Microbiol. Ecol. 87, 315—329.
• Raulf, F.F., Fabricius, K., Uthicke, S., de Beer, D., Abed, R.M.M., Ramette, A., 2015. Changes in microbial communities in coastal sediments along natural CO2 gradients at a volcanic vent in Papua New Guinea. Environ. Microbiol., http://dx.doi.org/10.1111/ 1462-2920.12729.
• Raupach, M.R., Marland, G., Ciais, P., Quéré, C.L., Canadell, J.G., Klepper, G., Field, C.B., 2007. Global and regional drivers of accelerating CO2 emissions. Proc. Natl. Acad. Sci. U.S.A. 104, 10288—10293.
• Raven, J.A., 2005. Ocean acidification due to increasing atmospheric carbon dioxide. Royal Society, London, UK, Policy document 12/05.
• Reid, P.C., Fischer, A.C., Lewis-Brown, E., Meredith, M.P., Sparrow, M., Andersson, A.J., Antia, A., Bates, N.R., Bathmann, U., Beaugrand, G., Brix, H., Dye, S., Edwards, M., Furevik, T., Gangstø, R., Hátún, H., Hopcroft, R.R., Kendall, M., Kasten, S., Keeling, R., Le Quéré, C., Mackenzie, F.T., Malin, G., Mauritzen, C., Olafsson, J., Paull, C., Rignot, E., Shimada, K., Vogt, M., Wallace, C., Wang, Z., Washington, R., 2009. Impacts of the oceans on climate change. Adv. Mar. Biol. 56, 1—150.
• Reinfelder, J.R., 2011. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Mar. Sci. 3, 291—315.
• Ridgwell, A., Schmidt, D.N., Turley, C., Brownlee, C., Maldonado, M. T., Tortell, P., Young, J.R., 2009. From laboratory manipulations to Earth system models: scaling calcification impacts of ocean acidification. Biogeosciences 6, 2611—2623.
• Riebesell, U., Schulz, K.G.R., Bellerby, G.J., Botros, M., Fritsche, P., Meyerhofer, M., Neill, C., Nondal, G., Oschlies, A., Wohlers, J., Zöllner, E., 2007. Enhanced biological carbon consumption in a high CO2 ocean. Nature 45, 545—548.
• Riemann, L., Farnelid, H., Steward, G.F., 2010. Nitrogenase genes in non-cyanobacterial plankton: prevalence, diversity and regulation in marine waters. Aquat. Microb. Ecol. 61, 235—247.
• Roberts, D., Rittschof, D., Holm, E., Schmidt, A.R., 1991. Factors influencing initial larval settlement: temporal, spatial and surface molecular components. J. Exp. Mar. Biol. Ecol. 150, 203—211.
• Rost, B., Zondervan, I., Wolf-Gladrow, D., 2008. Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions. Mar. Ecol. Prog. Ser. 373, 227—237.
• Roy, A.S., Gibbons, S.M., Schunck, H., Owens, S., Caporaso, J.G., Sperling, M., Nissimov, J.I., Romac, S., Bittner, L., Riebesell, U., LaRoche, J., Gilbert, J.A., 2013. Ocean acidification shows negligible impacts on high-latitude bacterial community structure in coastal pelagic mesocosms. Biogeosciences 10, 555—556.
• Ruiz-González, C., Simó, R., Sommaruga, R., Gasol, J.M., 2013. Away from darkness: a review on the effects of solar radiation on heterotrophic bacterioplankton activity. Front. Microbiol. 4, 131.
• Schimel, J.P., Gulledge, J.A.Y., 1998. Microbial community structure and global trace gases. Glob. Change Biol. 4 (7), 745—758.
• Sciandra, A., Harlay, J., Lefevre, D., Lemee, R., Rimmelin, P., Denis, M., Gattuso, J.P., 2003. Response of coccolithophorid Emiliania huxleyi to elevated partial pressure of CO2 under nitrogen limitation. Mar. Ecol. Prog. Ser. 261, 111—122.
• Sharp, K.H., Ritchie, K.B., 2012. Multi-partner interactions in corals in the face of climate change. Biol. Bull. 223 (1), 66—77.
• Shetye, S., Sudhakar, M., Jena, B., Mohan, R., 2013. Occurrence of nitrogen fixing cyanobacterium Trichodesmium under elevated pCO2 conditions in the Western Bay of Bengal. Int. J. Oceanogr., http://dx.doi.org/10.1155/2013/350465.
• Shi, D., Kranz, S.A., Kim, J.M., Morel, F.M., 2012. Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions. Proc. Natl. Acad. Sci. U.S.A. 109 (45), E3094—E3100.
• Shi, D., Xu, Y., Hopkinson, B.M., Morel, F.M., 2010. Effect of ocean acidification on iron availability to marine phytoplankton. Science 327 (5966), 676—679.
• Shirayama, Y., Kogure, K., Brewer, P.G., Ohsumi, T., Ishizaka, J., Kita, J., Watanabe, Y., 2004. Advances in biological research for CO2 ocean sequestration. J. Oceanogr. 60, 691—816.
• Siu, N., Apple, J.K., Moyer, K.L., 2014. The effects of ocean acidity and elevated temperature on bacterioplankton community structure and metabolism. Open J. Ecol. 4, 434—455.
• Skindersoe, M.E., Ettinger-Epstein, P., Rasmussen, T.B., Bjarnsholt, T., de Nys, R., Givskov, M., 2008. Quorum sensing antagonism from marine organisms. Mar. Biotechnol. 10 (1), 56—63.
• Sohm, J.A., Webb, E.A., Capone, D.G., 2011. Emerging patterns of marine nitrogen fixation. Nat. Rev. Microbiol. 9 (7), 499—508.
• Solomon, S., Plattner, G.K., Knutti, R., Friedlingstein, P., 2009. Irreversible climate change due to carbon dioxide emissions. Proc. Natl. Acad. Sci. U.S.A. 106, 1704—1709.
• Spalding, M.D., Ravilious, C., Green, E.P., 2001. World Atlas of Coral Reefs. University of California Press, Berkeley, 424 pp.
• Stewart, R.I.A., Dossena, M., Bohan, D.A., Jeppesen, E., Kordas, R. L., Ledger, M.E., Meerhoff, M., Moss, B., Mulder, C., Shurin, J.B., Suttle, B., Thompson, R., Trimmer, M., Woodward, G., 2013. Mesocosm experiments as a tool for ecological climate-change research. Adv. Ecol. Res. 48, 71—166.
• Tait, K., Hutchison, Z., Thompson, F.L., Munn, C.B., 2010. Quorum sensing signal production and inhibition by coral-associated Vibrios. Environ. Microbiol. Rep. 2 (1), 145—150.
• Takahashi, T., Sweeney, C., Hales, B., Chipman, D.W., Newberger, T., Goddard, J.G., Iannuzzi, R.A., Sutherland, S.C., 2012. The changing carbon cycle in the Southern Ocean. Oceanography 25, 26—37.
• Tanaka, T., Thingstad, T., Lovdal, T., Grossart, H.P., Larsen, A., Allgaier, M., Meyerhöfer, M., Schulz, K., Wohlers, J., Zöllner, E., 2008. Availability of phosphate for phytoplankton and bacteria and of labile organic carbon for bacteria at different pCO2 levels in a mesocosm study. Biogeosciences 5, 669—678.
• Ti, M., 2013. “Eco-omics”: a review of the application of genomics, transcriptomics, and proteomics for the study of the ecology of harmful algae. Microb. Ecol. 65, 901—915.
• Totti, C., Cucchiari, E., De Stefano, M., Pennesi, C., Romagnoli, T., Bavestrello, G., 2007. Seasonal variations of epilithic diatoms on different hard substrates, in the northern Adriatic Sea. J. Mar. Biol. Assoc. U.K. 87, 649—658.
• Turley, C.M., Roberts, J.M., Guinotte, J.M., 2007. Corals in deep-water: will the unseen hand of ocean acidification destroy cold-water ecosystems? Coral Reefs 26, 445—448.
• Volk, T., Hoffert, M.I., 1985. Ocean carbon pumps: analysis of relative strengths and efficiencies in ocean-driven atmospheric CO2 changes. Geophys. Monogr. Ser. 32, 99—110.
• Weber, B., Hasic, M., Chen, C., Wai, S.N., Milton, D.L., 2009. Type VI secretion modulates quorum sensing and stress response in Vibrio anguillarum. Environ. Microbiol. 11 (12), 3018—3028.
• Webster, N.S., Negri, A.P., 2006. Site-specific variation in Antarctic marine biofilms established on artificial surfaces. Environ. Microbiol. 8, 1177—1190.
• Weinbauer, M.G., 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, 83—98.
• Weiss, M.S., Abele, U., Weckesser, J., Welte, W.U., Schiltz, E., Schulz, G.E., 1991. Molecular architecture and electrostatic properties of a bacterial porin. Science 254 (5038), 1627—1630.
• Wingenter, O.W., Haase, K.B., Zeigler, M., Blake, D.R., Rowland, F.S., Sive, B., Riebesell, U., 2007. Unexpected consequences of in-creasing CO2 and ocean acidity on marine production of DMS and CH2ClI: potential climate impacts. Geophys. Res. Lett. 34 (5), L05710, http://dx.doi.org/10.1029/2006GL028139.
• Witt, V., Wild, C., Anthony, K.R.N., 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.
• Wolf-Gladrow, D.A., Riebesell, U., Burkhardt, S., Bijma, J., 1999. Direct effects of CO2 concentration on growth and isotopic composition of marine plankton. Tellus B: Chem. Phys. Meterol. 51, 461—476.
• Yamada, N., Fukuda, H., Ogawa, H., Saito, H., Suzumura, M., 2012. Heterotrophic bacterial production and extracellular enzymatic activity in sinking particulate matter in the western North Pacific Ocean. Front. Microbiol. 3, 379.
• Yamada, N., Suzumura, M., 2010. Effects of seawater acidification on hydrolytic enzyme activities. J. Oceanogr. 66, 233—241.
• Yang, X., Wu, X., Hao, H., He, Z., 2008. Mechanisms and assessment of water eutrophication. J. Zhejiang Univ. Sci. B 9, 197—209.
• Yoch, D.C., 2002. Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl. Environ. Microbiol. 68, 5804—5815.
• Yool, A., Popova, E.E., Coward, A.C., Bernie, D., Anderson, T.R., 2013. Climate change and ocean acidification impacts on lower trophic levels and the export of organic carbon to the deep ocean. Biogeosciences 10 (9), 3455—3522.