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The Effects of Ocean Acidity and Elevated Temperature on Bacterioplankton Community Structure and Metabolism

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DOI: 10.4236/oje.2014.48038    4,223 Downloads   5,879 Views   Citations

ABSTRACT

By the end of the 21st century, mean sea surface temperatures are expected to increase 4?C, while atmospheric CO2 concentrations are predicted to triple causing seawater to become acidic. These compounding effects will undoubtedly have major consequences for the organisms and processes in the oceans. Bacterioplankton play a vital role in the marine carbon cycle and the oceans’ ability to sequester CO2. We utilized pCO2 perturbation experiments to investigate the effects of ocean acidity and elevated temperature on bacterioplankton community structure and metabolism. Terminal-restriction fragment length polymorphism (T-RFLP) of small subunit ribosomal (SSU) genes revealed that bacterioplankton incubated in lower pH conditions exhibited a reduction of species richness, evenness, and overall diversity, relative to those incubated in ambient pH conditions. Non-metric multidimensional scaling (MDS) of T-RFLP data resulted in clustering by pH suggesting that pH influenced the structure of these communities. Shifts in the dominant members of bacterioplankton communities incubated under different pH were observed in both T-RFLP and SSU clone library analyses. Both ambient and low pH communities were dominated by Gammaproteobacteria and Alphaproteobacteria, although abundance of Alphaproteobacteria increased in communities incubated at lower pH. This was expressed by the gamma to alpha ratio dropping from ~9 to 4, respectively. In general, the representative taxa from these two classes were distinctly different between the treatments, with a few taxa found to be persistent in both treatments. Changes in the structure of bacterioplankton communities coincided with significant changes to their overall metabolism. Bacterial production rates decreased, while bacterial respiration increased under lower pH conditions. This study highlights the ability of bacterioplankton communities to respond to ocean acidification both structurally and metabolically, which may have significant implications for their ecological function in the marine carbon cycle and the ocean’s response to global climate change.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Siu, N. , Apple, J. and Moyer, C. (2014) The Effects of Ocean Acidity and Elevated Temperature on Bacterioplankton Community Structure and Metabolism. Open Journal of Ecology, 4, 434-455. doi: 10.4236/oje.2014.48038.

References

[1] Pachauri, R.K. and Reisinger, A. (Eds.) (2008) Climate Change 2007. Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report. Cambridge University Press, Cambridge.
[2] Doney, S.C., Fabry, V.J., Feely, R.A. and Kleypas, J.A. (2009) Ocean Acidification: The Other CO2 Problem. Annual Review of Marine Science, 1, 169-192.
http://dx.doi.org/10.1146/annurev.marine.010908.163834
[3] Doney, S.C., Balch, W.M., Fabry, V.J. and Feely, R.A. (2009) Ocean Acidification: A Critical Emerging Problem for the Ocean Sciences. Oceanography, 22, 16-25. http://dx.doi.org/10.5670/oceanog.2009.93
[4] Caldeira, K. and Wickett, M.E. (2003) Oceanography: Anthropogenic Carbon and Ocean pH. Nature, 425, 365.
http://dx.doi.org/10.1038/425365a
[5] Hobbie, J.E., Daley, R.J. and Jasper, S. (1977) Use of Nuclepore Filters for Counting Bacteria by Fluorescence Microscopy. Applied and Environmental Microbiology, 33, 1225-1228.
[6] Pomerory, L.R. (1974) The Ocean’s Food Web, a Changing Paradigm. BioScience, 24, 499-504.
http://dx.doi.org/10.2307/1296885
[7] Robinson, C. and Williams, P.J.L.B. (2005) Respiration and Its Measurement in Surface Marine Waters. In: del Giorgio, P.A. and Williams, P.J.L.B., Eds., Respiration in Aquatic Ecosystems, Oxford University Press, Oxford, 147-180.
[8] Bidle, K.D. and Azam, F. (2001) Bacterial Control of Silicon Regeneration from Diatom Detritus: Significance of Bacterial Ectohydrolases and Species Identity. Limnology and Oceanography, 46, 1606-1623.
http://dx.doi.org/10.4319/lo.2001.46.7.1606
[9] Kirchman, D.L. (1994) The Uptake of Inorganic Nutrients by Heterotrophic Bacteria. Microbial Ecology, 28, 255-271.
http://dx.doi.org/10.1007/BF00166816
[10] Kirchman, D.L. (2012) Processes in Microbial Ecology. Oxford University Press, Oxford.
[11] del Giorgio, P.A. and Duarte, C.M. (2002) Respiration in the Open Ocean. Nature, 420, 379-384.
http://dx.doi.org/10.1038/nature01165
[12] Azam, F., Fenchel, T., Field, J.G., Gray, J.S., Meyer-Reil, L.A. and Thingstad, F. (1983) The Ecological Role of Water-Column Microbes in the Sea. Marine Ecology-Progress Series, 10, 257-263. http://dx.doi.org/10.3354/meps010257
[13] Longhurst, A.R. and Harrison, W.G. (1989) The Biological Pump: Profiles of Plankton Production and Consumption in the Upper Ocean. Progress in Oceanography, 22, 47-123.
http://dx.doi.org/10.1016/0079-6611(89)90010-4
[14] Siegenthaler, U. and Sarmiento, J.L. (1993) Atmospheric Carbon Dioxide and the Ocean. Nature, 365, 119-125.
http://dx.doi.org/10.1038/365119a0
[15] Joint, I., Karl, D.M., Doney, S.C., Armbrust, E.V., Balch, W., Berman, M., Bowler, C., Church, M., Dickson, A., Heidelberg, J., Iglesias-Rodriguez, D., Kirchman, D., Kolber, Z.S., Letelier, R., Lupp, C., Maberly, S., Park, S., Raven, J., Repeta, D.J., Riebesell, U., Steward, G., Tortell, P., Zeebe, R.E. and Zehr, J.P. (2009) Consequences of High CO2 and Ocean Acidification for Microbes in the Global Ocean. University of Hawaii, Honolulu.
[16] Fuhrman, J.A. (2009) Microbial Community Structure and Its Functional Implications. Nature, 459, 193-199.
http://dx.doi.org/10.1038/nature08058
[17] Joint, I., Doney, S.C. and Karl, D.M. (2011) Will Ocean Acidification Affect Marine Microbes. The ISME Journal, 5, 1-7. http://dx.doi.org/10.1038/ismej.2010.79
[18] Liu, J., Weinbauer, M.G., Maier, C., Dai, M. and Gattuso, J.P. (2010) Effect of Ocean Acidification on Microbial Diversity and on Microbe-Driven Biogeochemistry and Ecosystem Functioning. Aquatic Microbial Ecology, 61, 291-305.
http://dx.doi.org/10.3354/ame01446
[19] Grossart, H.P., Allgaier, M., Passow, U. and Riebesell, U. (2006) Testing the Effect of CO2 Concentration on Dynamics of Marine Heterotrophic Bacterioplankton. Limnology and Oceanography, 51, 1-11.
http://dx.doi.org/10.4319/lo.2006.51.1.0001
[20] Allgaier, M., Riebesell, U., Vogt, M., Thyrhaug, R. and Grossart, H.P. (2008) Coupling of Heterotrophic Bacteria to Phytoplankton Bloom Development at Different pCO2 Levels: A Mesocosm Study. Biogeosciences, 5, 1007-1022.
http://dx.doi.org/10.5194/bg-5-1007-2008
[21] Lidbury, I., Johnson, V., Hall-Spencer, J.M., Munn, C.B. and Cunliffe, M. (2012) Community-Level Response of Coastal Microbial Biofilms to Ocean Acidification in a Natural Carbon Dioxide Vent Ecosystem. Marine Pollution Bulletin, 64, 1063-1066. http://dx.doi.org/10.1016/j.marpolbul.2012.02.011
[22] Zhang, R., Xia, X., Lau, S.C.K., Motegi, C., Weinbauer, M.G. and Jiao, N. (2013) Response of Bacterioplankton Community Structure to an Artificial Gradient of pCO2 in the Arctic Ocean. Biogeosciences, 10, 3679-3689.
http://dx.doi.org/10.5194/bg-10-3679-2013
[23] Engebretson, J.J. and Moyer, C.L. (2003) Fidelity of Select Restriction Endonucleases in Determining Microbial Diversity by Terminal-Restriction Fragment Length Polymorphism. Applied and Environmental Microbiology, 69, 4823-4829. http://dx.doi.org/10.1128/AEM.69.8.4823-4829.2003
[24] Ray, J.L., Topper, B., An, S., Silyakova, A., Spindelbock, J., Thyrhaug, R., Dubow, M.S., Thingstad, T.F. and Sandaa, R.A. (2012) Effect of Increased pCO2 on Bacterial Assemblage Shifts in Response to Glucose Addition in Fram Strait Seawater Mesocosms. FEMS Microbiology Ecology, 82, 713-723. http://dx.doi.org/10.1111/j.1574-6941.2012.01443.x
[25] Riebesell, U., Schulz, K.G., Bellerby, R.G.J., Botros, M., Fritsche, P., Meyerhofer, M., Neill, C., Nondal, G., Oschlies, A., Wohlers, J. and Zollner, E. (2007) Enhanced Biological Carbon Consumption in a High CO2 Ocean. Nature, 450, 545-548. http://dx.doi.org/10.1038/nature06267
[26] Teira, E., Fernández, A., álvarez-Salgado, X.A., García-Martín, E.E., Serret, P. and Sobrino, C. (2012) Response of Two Marine Bacterial Isolates to High CO2 Concentration. Marine Ecology Progress Series, 453, 27-36.
http://dx.doi.org/10.3354/meps09644
[27] Borges, A.V., Delille, B. and Frankignoulle, M. (2005) Budgeting Sinks and Sources of CO2 in the Coastal Ocean: Diversity of Ecosystems Counts. Geophysical Research Letters, 32, Published Online.
http://dx.doi.org/10.1029/2005gl023053
[28] Delille, B., Harlay, J., Zondervan, I., Jacquet, S., Chou, L., Wollast, R., Bellerby, R.G.J., Frankignoulle, M., Borges, A.V., Riebesell, U. and Gattuso, J.P. (2005) Response of Primary Production and Calcification to Changes of pCO2 during Experimental Blooms of the Coccolithophorid Emiliania huxleyi. Global Biogeochemical Cycles, 19, Published Online. http://dx.doi.org/10.1029/2004GB002318
[29] Mari, X. (2008) Does Ocean Acidification Induce an Upward Flux of Marine Aggregates? Biogeosciences, 5, 1023-1031. http://dx.doi.org/10.5194/bg-5-1023-2008
[30] Piontek, J., Borchard, C., Sperling, M., Schulz, K.G., Riebesell, U. and Engel, A. (2013) Response of Bacterioplankton Activity in an Arctic Fjord System to Elevated pCO2: Results from a Mesocosm Perturbation Study. Biogeosciences, 10, 297-314. http://dx.doi.org/10.5194/bg-10-297-2013
[31] Piontek, J., Lunau, M., Handel, N., Borchard, C., Wurst, M. and Engel, A. (2010) Acidification Increases Microbial Polysaccharide Degradation in the Ocean. Biogeosciences, 7, 1615-1624. http://dx.doi.org/10.5194/bg-7-1615-2010
[32] Apple, J.K., Del Giorgio, P.A. and Kemp, M.W. (2006) Temperature Regulation of Bacterial Production, Respiration, and Growth Efficiency in a Temperate Salt-Marsh Estuary. Aquatic Microbial Ecology, 43, 243-254.
http://dx.doi.org/10.3354/ame043243
[33] del Giorgio, P.A. and Bouvier, T.C. (2002) Linking the Physiologic and Phylogenetic Successions in Free-Living Bacterial Communities along an Estuarine Salinity Gradient. Limnology and Oceanography, 47, 471-486.
http://dx.doi.org/10.4319/lo.2002.47.2.0471
[34] Riebesell, U., Fabry, V.J., Hansson, L. and Gattuso, J.P. (2010) Guide to Best Practices for Ocean Acidification Research and Data Reporting. Publications Office of the EU, Luxembourg, 258.
[35] Lewis, E., Wallace, D. and Allison, L.J. (1998) Program Developed for CO2 System Calculations. Carbon Dioxide Information Analysis Center, Managed by Lockheed Martin Energy Research Corporation for the U.S. Department of Energy, 38.
[36] Hane, B.G., Jager, K. and Drexler, H.G. (1993) The Pearson Product-Moment Correlation Coefficient is Better Suited for Identification of DNA Fingerprint Profiles Than Band Matching Algorithms. Electrophoresis, 14, 967-972.
http://dx.doi.org/10.1002/elps.11501401154
[37] Clarke, K.R. and Gorley, R.N. (2006) PRIMER v6. Plymouth Marine Laboratory, Plymouth.
[38] Lane, D.J. (1991) 16S/23S rRNA Sequencing. In: Stackebrandt, E. and Goodfellow, M., Eds., Nucleic Acid Techniques in Bacterial Systematics, John Wiley & Sons Ltd., Chichester, 115-175.
[39] Pruesse, E., Quast, C., Knittel, K., Fuchs, B.M., Ludwig, W., Peplies, J. and Glockner, F.O. (2007) SILVA: A Comprehensive Online Resource for Quality Checked and Aligned Ribosomal RNA Sequence Data Compatible with ARB. Nucleic Acids Research, 35, 7188-7196. http://dx.doi.org/10.1093/nar/gkm864
[40] Hall, T.A. (1999) BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
[41] Schloss, P.D. and Handelsman, J. (2005) Introducing DOTUR, a Computer Program for Defining Operational Taxonomic Units and Estimating Species Richness. Applied and Environmental Microbiology, 71, 1501-1506.
http://dx.doi.org/10.1128/AEM.71.3.1501-1506.2005
[42] Mullins, T.D., Britschgi, T.B., Krest, R.L. and Giovannoni, S.J. (1995) Genetic Comparisons Reveal the Same Unknown Bacterial Lineages in Atlantic and Pacific Bacterioplankton Communities. Limnology and Oceanography, 40, 148-158. http://dx.doi.org/10.4319/lo.1995.40.1.0148
[43] Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., Kulam-Syed-Mohideen, A.S., McGarrell, D.M., Marsh, T., Garrity, G.M. and Tiedje, J.M. (2009) The Ribosomal Database Project: Improved Alignments and New Tools for rRNA Analysis. Nucleic Acids Research, 37, D141-D145. http://dx.doi.org/10.1093/nar/gkn879
[44] Ashelford, K.E., Chuzhanova, N.A., Fry, J.C., Jones, A.J. and Weightman, A.J. (2006) New Screening Software Shows That Most Recent Large 16S rRNA Gene Clone Libraries Contain Chimeras. Applied Environmental Microbiology, 72, 5734-5741. http://dx.doi.org/10.1128/AEM.00556-06
[45] Carignan, R., Blais, A.M. and Vis, C. (1998) Measurement of Primary Production and Community Respiration in Oligotrophic Lakes Using the Winkler Method. Canadian Journal of Fisheries and Aquatic Sciences, 55, 1078-1084.
http://dx.doi.org/10.1139/f97-319
[46] Kirchman, D., K’nees, E. and Hodson, R. (1985) Leucine Incorporation and Its Potential as a Measure of Protein Synthesis by Bacteria in Natural Aquatic Systems. Applied and Environmental Microbiology, 49, 599-607.
[47] Newbold, L.K., Oliver, A.E., Booth, T., Tiwari, B., Desantis, T., Maguire, M. andersen, G., van der Gast, C.J. and Whiteley, A.S. (2012) The Response of Marine Picoplankton to Ocean Acidification. Environmental Microbiology, 14, 2293-2307. http://dx.doi.org/10.1111/j.1462-2920.2012.02762.x
[48] Sperling, M., Piontek, J., Gerdts, G., Wichels, A., Schunck, H., Roy, A.S., La Roche, J., Gilbert, J., Nissimov, J.I., Bittner, L., Romac, S., Riebesell, U. and Engel, A. (2013) Effect of Elevated CO2 on the Dynamics of Particle-Attached and Free Living Bacterioplankton Communities in an Arctic Fjord. Biogeosciences, 10, 181-191.
http://dx.doi.org/10.5194/bg-10-181-2013
[49] Arnosti, C., Grossart, H.P., Mühling, M., Joint, I. and Passow, U. (2011) Dynamics of Extracellular Enzyme Activities in Seawater under Changed Atmospheric pCO2: A Mesocosm Investigation. Aquatic Microbial Ecology, 64, 285-298.
http://dx.doi.org/10.3354/ame01522
[50] Tortell, P.D., Ditullio, G.R., Sigman, D.M. and Morel, F.M.M. (2002) CO2 Effects on Taxonomic Composition and Nutrient Utilization in an Equatorial Pacific Phytoplankton Assemblage. Marine Ecology Progress Series, 236, 37-43.
http://dx.doi.org/10.3354/meps236037
[51] Witt, V., Wild, C., Anthony, K.R.N., Diaz-Pulido, G. and Uthicke, S. (2011) Effects of Ocean Acidification on Microbial Community Composition of, and Oxygen Fluxes through, Biofilms from the Great Barrier Reef. Environmental Microbiology, 13, 2976-2989. http://dx.doi.org/10.1111/j.1462-2920.2011.02571.x
[52] Meakin, N.G. and Wyman, M. (2011) Rapid Shifts in Picoeukaryote Community Structure in Response to Ocean Acidification. The ISME Journal, 5, 1397-1405. http://dx.doi.org/10.1038/ismej.2011.18
[53] Morris, J.J., Lenski, R.E. and Zinser, E.R. (2012) The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss. mBio, 3, e00036-12. http://dx.doi.org/10.1128/mBio.00036-12
[54] Sogin, M.L., Morrison, H.G., Huber, J.A., Welch, D.M., Huse, S.M., Neal, P.R., Arrieta, J.M. and Herndl, G.J. (2006) Microbial Diversity in the Deep Sea and the Underexplored “Rare Biosphere”. Proceedings of the National Academy of Sciences of the United States of America, 103, 12115-12120. http://dx.doi.org/10.1073/pnas.0605127103
[55] DeLong, E.F., Preston, C.M., Mincer, T., Rich, V., Hallam, S.J., Frigaard, N.U., Martinez, A., Sullivan, M.B., Edwards, R., Brito, B.R., Chisholm, S.W. and Karl, D.M. (2006) Community Genomics among Stratified Microbial Assemblages in the Ocean’s Interior. Science, 311, 496-503.
http://dx.doi.org/10.1126/science.1120250
[56] Moreno, E. (1998) Genome Evolution within the Alpha Proteobacteria: Why Do Some Bacteria Not Possess Plasmids and Others Exhibit More Than One Different Chromosome? FEMS Microbiology Reviews, 22, 255-275.
http://dx.doi.org/10.1111/j.1574-6976.1998.tb00370.x
[57] Teeling, H., Fuchs, B.M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C.M., Kassabgy, M., Huang, S., Mann, A.J., Waldmann, J., Weber, M., Klindworth, A., Otto, A., Lange, J., Bernhardt, J., Reinsch, C., Hecker, M., Peplies, J., Bockelmann, F.D., Callies, U., Gerdts, G., Wichels, A., Wiltshire, K.H., Glockner, F.O., Schweder, T. and Amann, R. (2012) Substrate-Controlled Succession of Marine Bacterioplankton Populations Induced by a Phytoplankton Bloom. Science, 336, 608-611.
http://dx.doi.org/10.1126/science.1218344
[58] Imhoff, J.F., Trüper, H.G. and Pfennig, N. (1984) Rearrangement of the Species and Genera of the Phototrophic “Purple Nonsulfur Bacteria”. International Journal of Systematic Bacteriology, 34, 340-343.
http://dx.doi.org/10.1099/00207713-34-3-340
[59] Brinkhoff, T., Giebel, H.A. and Simon, M. (2008) Diversity, Ecology, and Genomics of the Roseobacter Clade: A Short Overview. Archives of Microbiology, 189, 531-539. http://dx.doi.org/10.1007/s00203-008-0353-y
[60] Moran, M.A., Belas, R., Schell, M.A., González, J.M., Sun, F., Sun, S., Binder, B.J., Edmonds, J., Ye, W., Orcutt, B., Howard, E.C., Meile, C., Palefsky, W., Goesmann, A., Ren, Q., Paulsen, I., Ulrich, L.E., Thompson, L.S., Saunders, E. and Buchan, A. (2007) Ecological Genomics of Marine Roseobacters. Applied and Environmental Microbiology, 73, 4559-4569. http://dx.doi.org/10.1128/AEM.02580-06
[61] Newton, R.J., Griffin, L.E., Bowles, K.M., Meile, C., Gifford, S., Givens, C.E., Howard, E.C., King, E., Oakley, C.A., Reisch, C.R., Rinta-Kanto, J.M., Sharma, S., Sun, S., Varaljay, V., Vila-Costa, M., Westrich, J.R. and Moran, M.A. (2010) Genome Characteristics of a Generalist Marine Bacterial Lineage. The ISME Journal, 4, 784-798.
http://dx.doi.org/10.1038/ismej.2009.150
[62] Yamada, N. and Suzumura, M. (2010) Effects of Seawater Acidification on Hydrolytic Enzyme Activities. Journal of Oceanography, 66, 233-241. http://dx.doi.org/10.1007/s10872-010-0021-0
[63] Yamada, N., Tsurushima, N. and Suzumura, M. (2010) Effects of Seawater Acidification by Ocean CO2 Sequestration on Bathypelagic Prokaryote Activities. Journal of Oceanography, 66, 571-580.
http://dx.doi.org/10.1007/s10872-010-0047-3
[64] del Giorgio, P.A., Condon, R., Bouvier, T., Longnecker, K., Bouvier, C., Sherr, E. and Gasol, J.M. (2011) Coherent Patterns in Bacterial Growth, Growth Efficiency, and Leucine Metabolism along a Northeastern Pacific Inshore-Offshore Transect. Limnology and Oceanography, 56, 1-16. http://dx.doi.org/10.4319/lo.2011.56.1.0001
[65] Hall, E.K. and Cotner, J.B. (2007) Interactive Effect of Temperature and Resources on Carbon Cycling by Freshwater Bacterioplankton Communities. Aquatic Microbial Ecology, 49, 35-45.
[66] Vázquez-Domínguez, E., Vaqué, D. and Gasol, J.M. (2007) Ocean Warming Enhances Respiration and Carbon Demand of Coastal Microbial Plankton. Global Change Biology, 13, 1327-1334.
http://dx.doi.org/10.1111/j.1365-2486.2007.01377.x
[67] Karl, D.M., Laws, E.A., Morris, P., Williams, P.J.L. and Emerson, S. (2003) Global Carbon Cycle (Communication Arising): Metabolic Balance of the Open Sea. Nature, 426, 32.
http://dx.doi.org/10.1038/426032a
[68] Adams, H.E., Crump, B.C. and Kling, G.W. (2010) Temperature Controls on Aquatic Bacterial Production and Community Dynamics in Arctic Lakes and Streams. Environmental Microbiology, 12, 1319-1333.
http://dx.doi.org/10.1111/j.1462-2920.2010.02176.x
[69] Dziallas, C. and Grossart, H.P. (2011) Temperature and Biotic Factors Influence Bacterial Communities Associated with the Cyanobacterium microcystis sp. Environmental Microbiology, 13, 1632-1641.
http://dx.doi.org/10.1111/j.1462-2920.2011.02479.x
[70] Hall, E.K., Dzialowski, A.R., Stoxen, S.M. and Cotner, J.B. (2009) The Effect of Temperature on the Coupling between Phosphorus and Growth in Lacustrine Bacterioplankton Communities. Limnology and Oceanography, 54, 880-889. http://dx.doi.org/10.4319/lo.2009.54.3.0880
[71] Lindh, M.V., Riemann, L., Baltar, F., Romero-Oliva, C., Salomon, P.S., Granéli, E. and Pinhassi, J. (2012) Consequences of Increased Temperature and Acidification on Bacterioplankton Community Composition during a Mesocosm Spring Bloom in the Baltic Sea. Environmental Microbiology Reports, 5, 252-262.
http://dx.doi.org/10.1111/1758-2229.12009
[72] Pearce, D.A. (2005) The Structure and Stability of the Bacterioplankton Community in Antarctic Freshwater Lakes, Subject to Extremely Rapid Environmental Change. FEMS Microbiology Ecology, 53, 61-72.
http://dx.doi.org/10.1016/j.femsec.2005.01.002
[73] Simon, M., Gloeckner, F.O. and Amann, R. (1999) Different Community Structure and Temperature Optima of Heterotrophic Picoplankton in Various Regions of the Southern Ocean. Aquatic Microbial Ecology, 18, 275-284.
http://dx.doi.org/10.3354/ame018275
[74] Kana, T.M., Darkangelo, C., Hunt, M.D., Oldham, J.B., Bennett, G.E. and Cornwell, J.C. (1994) Membrane Inlet Mass Spectrometer for Rapid High-Precision Determination of N2, O2, and Ar in Environmental Water Samples. Analytical Chemistry, 66, 4166-4170. http://dx.doi.org/10.1021/ac00095a009
[75] Pomeroy, L.R. and Wiebe, W.J. (2001) Temperature and Substrates as Interactive Limiting Factors for Marine Heterotrophic Bacteria. Aquatic Microbial Ecology, 23, 187-204.
http://dx.doi.org/10.3354/ame023187
[76] Reinthaler, T. and Herndl, G.J. (2005) Seasonal Dynamics of Bacterial Growth Efficiencies in Relation to Phytoplankton in the Southern North Sea. Aquatic Microbial Ecology, 39, 7-16.
http://dx.doi.org/10.3354/ame039007
[77] Bellerby, R.G.J., Schulz, K.G., Riebesell, U., Neill, C., Nondal, G., Heegaard, E., Johannessen, T. and Brown, K.R. (2008) Marine Ecosystem Community Carbon and Nutrient Uptake Stoichiometry under Varying Ocean Acidification during the PeECE III Experiment. Biogeosciences, 5, 1517-1527.
http://dx.doi.org/10.5194/bg-5-1517-2008
[78] Hutchins, D.A., Mulholland, M.R. and Fu, F. (2009) Nutrient Cycles and Marine Microbes in a CO2-Enriched Ocean. Oceanography, 22, 128-145. http://dx.doi.org/10.5670/oceanog.2009.103
[79] Losh, J.L., Morel, F.M.M. and Hopkinson, B.M. (2012) Modest Increase in the C:N Ratio of N-Limited Phytoplankton in the California Current in Response to High CO2. Marine Ecology Progress Series, 468, 31-42.
http://dx.doi.org/10.3354/meps09981
[80] Apple, J.K. and del Giorgio, P.A. (2007) Organic Substrate Quality as the Link between Bacterioplankton Carbon Demand and Growth Efficiency in a Temperate Salt-Marsh Estuary. The ISME Journal, 1, 729-742.
http://dx.doi.org/10.1038/ismej.2007.86
[81] Kirchman, D.L., Moran, X.A.G. and Ducklow, H. (2009) Microbial Growth in the Polar Oceans—Role of Temperature and Potential Impact of Climate Change. Nature Reviews Microbiology, 7, 451-459.
[82] Eiler, A., Langenheder, S., Bertilsson, S. and Tranvik, L.J. (2003) Heterotrophic Bacterial Growth Efficiency and Community Structure at Different Natural Organic Carbon Concentrations. Applied and Environmental Microbiology, 69, 3701-3709. http://dx.doi.org/10.1128/AEM.69.7.3701-3709.2003
[83] Finkel, Z.V., Beardall, J., Flynn, K.J., Quigg, A., Rees, T.A.V. and Raven, J.A. (2010) Phytoplankton in a Changing World: Cell Size and Elemental Stoichiometry. Journal of Plankton Research, 32, 119-137.
http://dx.doi.org/10.1093/plankt/fbp098
[84] Riebesell, U., Kortzinger, A. and Oschlies, A. (2009) Sensitivities of Marine Carbon Fluxes to Ocean Change. Proceedings of the National Academy of Sciences of the United States of America, 106, 20602-20609.
http://dx.doi.org/10.1073/pnas.0813291106
[85] Harley, C.D.G., Hughes, A.R., Hultgren, K.M., Miner, B.G., Sorte, C.J.B., Thornber, C.S., Rodriguez, L.F., Tomanek, L. and Williams, S.L. (2006) The Impacts of Climate Change in Coastal Marine Systems. Ecology Letters, 9, 228-241.
http://dx.doi.org/10.1111/j.1461-0248.2005.00871.x
[86] Cai, W.J., Hu, X., Huang, W.J., Murrell, M.C., Lehrter, J.C., Lohrenz, S.E., Chou, W.C., Zhai, W., Hollibaugh, J.T., Wang, Y., Zhao, P., Guo, X., Gundersen, K., Dai, M. and Gong, G.C. (2011) Acidification of Subsurface Coastal Waters Enhanced by Eutrophication. Nature Geoscience, 4, 766-770.
http://dx.doi.org/10.1038/ngeo1297
[87] Feely, R.A., Alin, S.R., Newton, J., Sabine, C.L., Warner, M., Devol, A., Krembs, C. and Maloy, C. (2010) The Combined Effects of Ocean Acidification, Mixing, and Respiration on pH and Carbonate Saturation in an Urbanized Estuary. Estuarine, Coastal and Shelf Science, 88, 442-449.
http://dx.doi.org/10.1016/j.ecss.2010.05.004
[88] Mucci, A., Starr, M., Gilbert, D. and Sundby, B. (2011) Acidification of Lower St. Lawrence Estuary Bottom Waters. Atmosphere-Ocean, 49, 206-218.

  
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