Skip to main content

Advertisement

Log in

Microorganisms and ocean global change

  • Review Article
  • Published:

From Nature Microbiology

View current issue Submit your manuscript

Abstract

The prokaryotic and eukaryotic microorganisms that drive the pelagic ocean's biogeochemical cycles are currently facing an unprecedented set of comprehensive anthropogenic changes. Nearly every important control on marine microbial physiology is currently in flux, including seawater pH, pCO2, temperature, redox chemistry, irradiance and nutrient availability. Here, we examine how microorganisms with key roles in the ocean carbon and nitrogen cycles may respond to these changes in the Earth's largest ecosystem. Some functional groups such as nitrogen-fixing cyanobacteria and denitrifiers may be net beneficiaries of these changes, while others such as calcifiers and nitrifiers may be negatively impacted. Other groups, such as heterotrophic bacteria, may be relatively resilient to changing conditions. The challenge for marine microbiologists will be to predict how these divergent future responses of marine microorganisms to complex multiple variable interactions will be expressed through changing biogeography, community structure and adaptive evolution, and ultimately through large-scale alterations of the ocean's carbon and nutrient cycles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1: Anthropogenic global change effects on key chemical and physical factors that influence the growth and community composition of marine planktonic microorganisms.
Figure 2: Impacts of anthropogenic global change on physical, chemical and biological components of the ocean carbon cycle.
Figure 3: The diversity of CO2, temperature and light conditions used in six published coccolithophore global change experiments.
Figure 4: Anthropogenic global change effects on the microbially mediated ocean nitrogen cycle.
Figure 5: Possible biological responses of a model phytoplankton community to climate change.

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  1. Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).

    Article  CAS  PubMed  Google Scholar 

  2. Pachauri, R. K. Climate Change 2014: Synthesis Report Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (IPCC, 2014).

    Google Scholar 

  3. Gao, K., Helbling, E. W., Häder, D.-P. & Hutchins, D. A. Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar. Ecol. Prog. Ser. 470, 167–189 (2012).

    Article  CAS  Google Scholar 

  4. Thomas, M. K., Kremer, C. T., Klausmeier, C. A. & Litchman, E. A global pattern of thermal adaptation in marine phytoplankton. Science 338, 1085–1088 (2012).

    Article  CAS  PubMed  Google Scholar 

  5. Gruber N. Warming up, turning sour, losing breath: ocean biogeochemistry under global change. Phil. Trans. R Soc. A 369, 1980–1996 (2011).

    Article  CAS  PubMed  Google Scholar 

  6. Raven, J. A. & Falkowski, P. G. Oceanic sinks for atmospheric CO2 . Plant Cell Environ. 22, 741–755 (1999).

  7. Beardall, J. & Raven, J. A. in Carbon Acquisition by Microalgae Vol. 6 (eds Borowitzka, M. A., Beardall, J. & Raven, J. A.) 89–99 (2016).

  8. Sommer, U., Paul, C. & Moustaka-Gouni, M. Warming and ocean acidification effects on phytoplankton—from species shifts to size shifts within species in a mesocosm experiment. PLoS ONEhttp://dx.doi.org/10.1371/journal.pone.0125239 (2015).

  9. Hare, C. E. et al. Consequences of increased temperature and CO2 for algal community structure and biogeochemistry in the Bering Sea. Mar. Ecol. Prog. Ser. 352, 9–16 (2007).

    Article  CAS  Google Scholar 

  10. Hutchins, D. A. & Boyd, P. W. Marine phytoplankton and the changing ocean iron cycle. Nat. Clim. Change 6, 1071–1079 (2016).

    Article  CAS  Google Scholar 

  11. Paul, C. et al. Effects of increased CO2 concentration on nutrient limited coastal summer plankton depend on temperature. Limnol. Oceanogr. 61, 853–868 (2016).

    Article  CAS  Google Scholar 

  12. Pancic, M., Hansen, P. J., Tammilehto, A. & Lundholm, N. M. Resilience to temperature and pH changes in a future climate change scenario in six strains of the polar diatom Fragilariopsis cylindrus. Biogeosciences 12, 4235–4244 (2015).

    Article  CAS  Google Scholar 

  13. Taucher, J. et al. Effects of CO2 and temperature on carbon uptake and partitioning by the marine diatoms Thalassiosira weissflogii and Dactyliosolen fragilissimus. Limnol. Oceanogr. 60, 901–919 (2015).

    Article  CAS  Google Scholar 

  14. Shi, D. et al. Interactive effects of light, nitrogen source, and carbon dioxide on energy metabolism in the diatom Thalassiosira pseudonana. Limnol. Oceanogr. 60, 1805–1822 (2015).

    Article  CAS  Google Scholar 

  15. Hennon, G. M. M. et al. Acclimation conditions modify physiological response of the diatom Thalassiosira pseudonana to elevated CO2 concentrations in a nitrate-limited chemostat. J. Phycol. 50, 243–253 (2014).

    Article  CAS  PubMed  Google Scholar 

  16. Finkel, Z. V. et al. Phytoplankton in a changing world: cell size and elemental stoichiometry. J. Plankton Res. 32, 119–137 (2010).

    Article  CAS  Google Scholar 

  17. Marinov, I., Doney, S. C. & Lima, I. D. Response of ocean phytoplankton community structure to climate change over the 21st century: partitioning the effects of nutrients, temperature and light. Biogeosciences 7, 3941–3959 (2010).

    Article  Google Scholar 

  18. Dutkiewicz, S. et al. Impact of ocean acidification on the structure of future phytoplankton communities. Nat. Clim. Change 5, 1002–1009 (2015).

    Article  CAS  Google Scholar 

  19. Fu, F. X. et al. Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). J. Phycol. 43, 485–496 (2007).

    Article  Google Scholar 

  20. Lomas M. W. et al. Effect of ocean acidification on cyanobacteria in the subtropical North Atlantic. Aquat. Microb. Ecol. 66, 211–222 (2012).

    Article  Google Scholar 

  21. Paerl, H. W. & Otten, T. G. Harmful cyanobacterial blooms: causes, consequences, and controls. Microb. Ecol. 65, 995–1010 (2013).

    Article  CAS  PubMed  Google Scholar 

  22. Visser, P. M. et al. How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae 54, 145–149 (2016).

    Article  CAS  PubMed  Google Scholar 

  23. Zhu, Z. Future Impacts of Warming and Other Global Change Variables on Phytoplankton Communities of Coastal Antarctica and California. PhD thesis, Univ. Southern California (2017).

    Google Scholar 

  24. McCabe, R. M. et al. An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions. Geophys. Res. Lett. 43, 10366–10376 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Sun, J. et al. Effects of changing pCO2 and phosphate availability on domoic acid production and physiology of the marine harmful bloom diatom Pseudo-nitzschia multiseries. Limnol. Oceanogr. 56, 829–840 (2011).

    Article  CAS  Google Scholar 

  26. Tatters, A. O., Fu, F. X. & Hutchins, D. A. High CO2 and silicate limitation synergistically increase the toxicity of Pseudo-nitzschia fraudulenta. PLoS ONE 7, e32116 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Fu, F. X., Tatters, A. O. & Hutchins, D. A. Global change and the future of harmful algal blooms in the ocean. Mar. Ecol. Prog. Ser. 470, 207–233 (2012).

    Article  CAS  Google Scholar 

  28. Hattenrath-Lehmann, T. K. et al. The effects of elevated CO2 on the growth and toxicity of field populations and cultures of the saxitoxin-producing dinoflagellate, Alexandrium fundyense. Limnol. Oceanogr. 60, 198–214 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Errera, R. M., Yvon-Lewis, S., Kessler, J. D. & Campbell, L. Reponses of the dinoflagellate Karenia brevis to climate change: pCO2 and sea surface temperatures. Harmful Algae 37, 110–116 (2014).

    Article  CAS  Google Scholar 

  30. Van de Waal, D. B., Eberlein, T., John, U., Wohlrab, S. & Rost. B. Impact of elevated pCO2 on paralytic shellfish poisoning toxin content and composition in Alexandrium tamarense. Toxicon 78, 58–67 (2014).

    Article  CAS  PubMed  Google Scholar 

  31. Reusch, T. B. H. & Boyd, P. W. Experimental evolution meets marine phytoplankton. Evolution 67, 1849–1859 (2013).

    Article  PubMed  Google Scholar 

  32. Baker, K. G. et al. Thermal performance curves of functional traits aid understanding of thermally induced changes in diatom-mediated biogeochemical fluxes. Front. Mar. Sci. 3, 1–14 (2016).

    Article  Google Scholar 

  33. Boyd, P. W. et al. Physiological responses of a Southern Ocean diatom to complex future ocean conditions. Nat. Clim. Change 6, 207–216 (2016).

    Article  Google Scholar 

  34. Caron, D. A. & Hutchins, D. A. The effects of changing climate on microzooplankton community structure and grazing: drivers, predictions and knowledge gaps. J. Plankton Res. 35, 235–252 (2013).

    Article  Google Scholar 

  35. Boyd, P. W. & Hutchins, D. A. Understanding the responses of ocean biota to a complex matrix of cumulative anthropogenic change. Mar. Ecol. Prog. Ser. 470, 125–135 (2012).

    Article  Google Scholar 

  36. Riebesell, U. & Gattuso, J.-P. Commentary: lessons learned from ocean acidification research. Nat. Clim. Change 5, 12–14 (2015).

    Article  CAS  Google Scholar 

  37. Raven, J. & Crawfurd, K. Environmental controls on coccolithophore calcification. Mar. Ecol. Prog. Ser. 470, 137–166 (2012).

    Article  CAS  Google Scholar 

  38. Biermann, A. & Engel, A. Effect of CO2 on the properties and sinking velocity of aggregates of the coccolithophore Emiliania huxleyi. Biogeosciences 7, 1017–1029 (2010).

    Article  CAS  Google Scholar 

  39. Bach, L. T. et al. Dissecting the impact of CO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyi. New Phytol. 199, 121–134 (2013).

    Article  CAS  PubMed  Google Scholar 

  40. Hofmann, G. E. et al. The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism to ecosystem perspective. Annu. Rev. Ecol. Evol. Syst. 41, 127–148 (2010).

    Article  Google Scholar 

  41. Riebesell, U. et al. Reduced calcification of marine plankton in response to increased atmospheric CO2 . Nature 407, 364–367 (2000).

    Article  CAS  PubMed  Google Scholar 

  42. Langer, G., Nehrke, G., Probert, I., Ly, J. & Ziveri, P. Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6, 2637–2646 (2009).

    Article  CAS  Google Scholar 

  43. Müller, M. N., Trull, T. W. & Hallegraef, G. M. Differing responses of three Southern Ocean Emiliania huxleyi ecotypes to changing seawater carbonate chemistry. Mar. Ecol. Prog. Ser. 531, 81–90 (2015).

    Article  CAS  Google Scholar 

  44. Rickaby, R. E. M. et al. Environmental carbonate chemistry selects for phenotype of recently isolated strains of Emiliania huxleyi. Deep-Sea Res. II 127, 28–40 (2016).

    Article  CAS  Google Scholar 

  45. Beaufort, L. et al. Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476, 80–83 (2011).

    Article  CAS  PubMed  Google Scholar 

  46. Iglesias-Rodriguez, M. D. Phytoplankton calcification in a high-CO2 world. Science 320, 336–340 (2008).

    Article  CAS  PubMed  Google Scholar 

  47. Feng, Y. et al. Interactive effects of increased pCO2, temperature and irradiance on the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae). Eur. J. Phycol. 43, 87–98 (2008).

    Article  CAS  Google Scholar 

  48. Feng, Y. et al. The effects of increased pCO2 and temperature on the North Atlantic spring bloom. I. The phytoplankton community and biogeochemical response. Mar. Ecol. Prog. Ser. 388, 13–25 (2009).

    Article  CAS  Google Scholar 

  49. de Bodt, C. et al. Individual and interacting effects of pCO2 and temperature on Emiliania huxleyi calcification: study of the calcite production, the coccolith morphology and the coccosphere size. Biogeosciences 7, 1401–1412 (2010).

    Article  CAS  Google Scholar 

  50. Rokitta, S. D. & Rost, B. Effects of CO2 and their modulation by light in the life-cycle stages of the coccolithophore Emiliania huxleyi. Limnol. Oceanogr. 57, 607–618 (2012).

    Article  CAS  Google Scholar 

  51. Lefebvre, S. C. et al. Nitrogen sources and pCO2 synergistically affect carbon allocation, growth and morphology of the coccolithophore Emiliania huxleyi: potential implications of ocean acidification for the carbon cycle. Glob. Change Biol. 18, 493–503 (2012).

    Article  Google Scholar 

  52. Rouco, M. et al. The effect of nitrate and phosphate availability on Emiliania huxleyi (NZEH) physiology under different CO2 scenarios. Front. Microbiol. 4, 155 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Gao, K. et al., Ocean acidification exacerbates the effect of UV radiation on the calcifying phytoplankter Emiliania huxleyi. Limnol. Oceanogr. 54, 1855–1862 (2009).

    Article  CAS  Google Scholar 

  54. Riviero-Calle, S. et al. Multidecadal increase in North Atlantic coccolithophores and the potential role of rising CO2 . Science 350, 1533–1537 (2015).

    Article  CAS  Google Scholar 

  55. Nanninga, H. J. & Tyrrell, T. Importance of light for the formation of algal blooms by Emiliania huxleyi. Mar. Ecol. Prog. Ser. 136, 195–203 (1996).

    Article  Google Scholar 

  56. Morris, R. M. et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420, 806–810 (2002).

    Article  CAS  PubMed  Google Scholar 

  57. Baltar, F. et al. Response of rare, common and abundant bacterioplankton to anthropogenic perturbations in a Mediterranean coastal site. FEMS Microbiol. Ecol. 91, fiv058 (2015).

    Article  PubMed  CAS  Google Scholar 

  58. Joint, I., Doney, S. C. & Karl, D. M. Will ocean acidification affect marine microbes? ISME J. 5, 1–7 (2011).

    Article  PubMed  Google Scholar 

  59. Hartmann, M. et al. Resilience of SAR11 bacteria to rapid acidification in the high-latitude open ocean. FEMS Microbiol. Ecol. 92, fiv161 (2016).

    Article  PubMed  CAS  Google Scholar 

  60. Grossart, H.-P., Allgaier, M., Passow, U. & Riebesell, U. Testing the effect of CO2 concentration on the dynamics of marine heterotrophic bacterioplankton. Limnol. Oceanogr. 51, 1–11 (2006).

    Article  CAS  Google Scholar 

  61. Krause E. et al. Small changes in pH have direct effects on marine bacterial community composition: a microcosm approach. PLoS ONE 7, e47035 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Lindh, M. V. et al. 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 (2013).

    Article  CAS  PubMed  Google Scholar 

  63. Roy, A. S. et al. Ocean acidification shows negligible impacts on high-latitude bacterial community structure in coastal pelagic mesocosms. Biogeosciences 10, 555–566 (2013).

    Article  Google Scholar 

  64. Oliver, A. E., Newbold, L. K., Whiteley, A. S. & van der Gast, C. J. Marine bacterial communities are resistant to elevated carbon dioxide levels. Environ. Microbiol. Rep. 6, 574–582 (2014).

    Article  CAS  PubMed  Google Scholar 

  65. Endres, S. et al. Stimulated bacterial growth under elevated pCO2: results from an off-shore mesocosm study. PLoS ONE 9, e99228 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Engel, A. et al. Impact of CO2 enrichment on organic matter dynamics during nutrient induced coastal phytoplankton blooms. J. Plankton Res. 36, 641–657 (2014).

    Article  CAS  Google Scholar 

  67. Zhang, R. et al. Response of bacterioplankton community structure to an artificial gradient of pCO2 in the Arctic Ocean. Biogeosciences 10, 3679–3689 (2013).

    Article  CAS  Google Scholar 

  68. Piontek, J. et al. Acidification increases microbial polysaccharide degradation in the ocean. Biogeosciences 7, 1615–1624 (2010).

    Article  CAS  Google Scholar 

  69. Bunse, C. et al. Response of marine bacterioplankton pH homeostasis gene expression to elevated CO2 . Nat. Clim. Change 6, 483–489 (2016).

    Article  CAS  Google Scholar 

  70. Hoppe, H.-G. et al. Climate warming in winter affects the coupling between phytoplankton and bacteria during the spring bloom: a mesocosm study. Aquat. Microb. Ecol. 51, 105–115 (2008).

    Article  Google Scholar 

  71. Sarmento, H. et al. Warming effects on marine microbial food web processes: how far can we go when it comes to predictions? Phil. Trans. R. Soc. B 365, 2137–2149 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Lara, E. et al. Experimental evaluation of the warming effect on viral, bacterial and protistan communities in two contrasting Arctic systems. Aquat. Microb. Ecol. 70, 17–32 (2013).

    Article  Google Scholar 

  73. von Scheibner, M. et al. Impact of warming on phytobacterioplankton coupling and bacterial community composition in experimental mesocosms. Environ. Microbiol. 16, 718–733 (2014).

    Article  PubMed  Google Scholar 

  74. Engel, A. et al. Effects of sea surface warming on the production and composition of dissolved organic matter during phytoplankton blooms: results from a mesocosm study. J. Plankton Res. 33, 357–372 (2011).

    Article  CAS  Google Scholar 

  75. Thornton, D. C. O. Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean. Eur. J. Phycol. 49, 20–46 (2014).

    Article  CAS  Google Scholar 

  76. Huete-Stauffer, T. M., Arandia-Gorostidi, N., Alonso-Sáez, L. & Morán, X. A. G. Experimental warming decreases the average size and nucleic acid content of marine bacterial communities. Front. Microbiol. 7, 730 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  77. Morán, X. A. G. et al. More, smaller bacteria in response to ocean's warming? Proc. R. Soc. B 282, 20150371 (2015).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  78. Ruiz-Gonzalez, C., Simo, R., Sommaruga, R. & Gasol, J. M. Away from darkness: a review on the effects of solar radiation on heterotrophic bacterioplankton activity. Front. Microbiol. 4, 131 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Löscher, C. R. et al. Hidden biosphere in an oxygen-deficient Atlantic open-ocean eddy: future implications of ocean deoxygenation on primary production in the eastern tropical North Atlantic. Biogeosciences 12, 7467–7482 (2015).

    Article  CAS  Google Scholar 

  80. Sohm, J. A., Webb, E. A. & Capone, D. A. Emerging patterns of marine nitrogen fixation, Nat. Rev. Microbiol. 9, 499–508 (2011).

    CAS  Google Scholar 

  81. Fu, F.-X. et al. Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera. Limnol. Oceanogr. 53, 2472–2484 (2008).

    Article  CAS  Google Scholar 

  82. Garcia, N. S. et al. Combined effects of CO2 and light on large and small isolates of the unicellular N2-fixing cyanobacterium Crocosphaera watsonii from the western tropical Atlantic Ocean. Eur. J. Phycol. 48, 128–139 (2013).

    Article  CAS  Google Scholar 

  83. Hutchins, D. A. et al. Taxon-specific response of marine nitrogen fixers to elevated carbon dioxide concentrations. Nat. Geosci. 6, 790–795 (2013).

    Article  CAS  Google Scholar 

  84. Gradoville, M. R., White, A. E. & Letelier, R. M. Physiological response of Crocosphaera watsonii to enhanced and fluctuating carbon dioxide conditions. PLoS ONE 9, e110660 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Hutchins, D. A. et al. Irreversibly increased N2 fixation in Trichodesmium experimentally adapted to high CO2 . Nat. Commun. 6, 8155 (2015).

    Article  PubMed  Google Scholar 

  86. Hutchins, D. A., Mulholland, M. R. & Fu, F.-X. Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22, 128–145 (2009).

    Article  Google Scholar 

  87. Shetye, S., Sudhakar, M., Jena, B. & Mohan, R. Occurrence of nitrogen fixing cyanobacterium Trichodesmium under elevated pCO2 conditions in the Western Bay of Bengal. Int. J. Oceanogr. 2013, 350465 (2013).

    Article  Google Scholar 

  88. Law, C. S. et al. No stimulation of nitrogen fixation by non-filamentous diazotrophs under elevated CO2 in the South Pacific. Glob. Change Biol. 18, 3004–3014 (2012).

    Article  Google Scholar 

  89. Böttjer, D. et al. Experimental assessment of diazotrophs responses to elevated seawater pCO2 in the North Pacific Subtropical Gyre. Global Biogeochem. Cyc. 28, 601–616 (2014).

    Article  CAS  Google Scholar 

  90. Gradoville, M. R. et al. Diversity trumps acidification: lack of evidence for carbon dioxide enhancement of Trichodesmium community nitrogen or carbon fixation at station ALOHA. Limnol. Oceanogr. 59, 645–659 (2014).

    Article  CAS  Google Scholar 

  91. Fu, F.-X. et al. Differing responses of marine N2 fixers to warming and consequences for future diazotroph community structure. Aquat. Microb. Ecol. 72, 33–46 (2014).

    Article  Google Scholar 

  92. Lesser, M. P. Effects of ultraviolet radiation on productivity and nitrogen fixation in the cyanobacterium, Anabaena sp. (Newton's strain). Hydrobiologia 598, 1–9 (2008).

    Article  CAS  Google Scholar 

  93. Singh, S. P., Häder, D.-P. & Sinha, R. P. Cyanobacteria and ultraviolet radiation (UVR) stress: mitigation strategies. Ageing Res. Rev. 9, 79–90 (2010).

    Article  CAS  PubMed  Google Scholar 

  94. Garcia, N. S. et al. Interactive effects of irradiance and CO2 on CO2 fixation and N2 fixation in the diazotroph Trichodesmium erythraeum (Cyanobacteria). J. Phycol. 47, 1292–1303 (2011).

    Article  CAS  PubMed  Google Scholar 

  95. Garcia, N. S., Fu, F.-X. & Hutchins, D. A. Colimitation of the unicellular photosynthetic diazotroph Crocosphaera watsonii by phosphorus, light, and carbon dioxide. Limnol. Oceanogr. 58, 1501–1512 (2013).

    Article  CAS  Google Scholar 

  96. Kranz, S. A. et al. Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: physiological responses. Plant Physiol. 154, 334–345 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Snow. J. T. et al. Environmental controls on the biogeography of diazotrophy and Trichodesmium in the Atlantic Ocean. Global Biogeochem. Cyc. 29, 865–884 (2015).

    Article  CAS  Google Scholar 

  98. Shi, D., Kranz, S. A., Kim, J.-M. & Morel, F. M. M. Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions. Proc. Natl Acad. Sci. USA 109, E3094–E3100 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Hutchins, D. A. et al. CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr. 52, 1293–1304 (2007).

    Article  CAS  Google Scholar 

  100. Walworth, N. G. et al. Mechanisms of increased Trichodesmium fitness under iron and phosphorus co-limitation in the present and future ocean. Nat. Commun. 7, 12081 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Hawley, A. K. et al. Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes. Proc. Natl Acad. Sci. USA 111, 11395–11400 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Yool, A., Martin, A. P., Fernández, C. & Clark, D. R. The significance of nitrification for oceanic new production. Nature 447, 999–1002 (2007).

    Article  CAS  PubMed  Google Scholar 

  103. Voss, M. et al. The marine nitrogen cycle: recent discoveries, uncertainties and the potential relevance of climate change. Phil. Trans. R. Soc. B 368, 20130121 (2013).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  104. Beman, J. M. et al. Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc. Natl Acad. Sci. USA 108, 208–213 (2011).

    Article  CAS  PubMed  Google Scholar 

  105. Kitidis, V. et al. Impact of ocean acidification on benthic and water column ammonia oxidation. Geophys. Res. Lett. 38, L21603 (2011).

    Article  CAS  Google Scholar 

  106. Rees, A. P., Brown, Jayakumar, A. & Ward, B. B. The inhibition of N2O production by ocean acidification in cold temperate and polar waters. Deep-Sea Res. II 127, 93–101 (2016).

    Article  CAS  Google Scholar 

  107. Fulweiler, R. W., Emery, H. E., Heiss, E. M. & Berounsky, V. M. Assessing the role of pH in determining water column nitrification rates in a coastal system. Estuar. Coast 34, 1095–1102 (2011).

    Article  CAS  Google Scholar 

  108. Gazeau, F., van Rijswijk, P., Pozzato, L. & Middelburg, J. J. Impacts of ocean acidification on sediment processes in shallow waters of the Arctic Ocean. PLoS ONE 9, e94068 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. Qin, W. et al. Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proc. Natl Acad. Sci. USA 111, 12504–12509 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Raven, J. et al. Ocean Acidification due to Increasing Atmospheric Carbon Dioxide (The Royal Society, 2005).

    Google Scholar 

  111. Bowen, J. L., Kearns, P. J., Holcomb, M. & Ward, B. B. Acidification alters the composition of ammonia-oxidizing microbial assemblages in marine mesocosms. Mar. Ecol. Prog. Ser. 492, 1–8 (2013).

    Article  CAS  Google Scholar 

  112. Koops, H. P., Böttcher, B., Moller, U. C., Pommerening-Roser, A. & Stehr, G. Classification of eight new species of ammonia-oxidizing bacteria: Nitrosomonas communis sp. nov., Nitrosomonas ureae sp. nov., Nitrosomonas aestuarii sp. nov., Nitrosomonas marina sp. nov, Nitrosomonas nitrosa sp. nov., Nitrosomonas eutropha sp. nov., Nitrosomonas oligotropha sp. nov. and Nitrosomonas halophila sp. nov. J. Gen. Microbiol. 137, 1689–1699 (1991).

    Article  CAS  Google Scholar 

  113. Bianchi, M. et al. Nitrification rates, ammonium and nitrate distribution in upper layers of the water column and in sediments of the Indian sector of the Southern Ocean. Deep-Sea Res. II 44, 1017–1032 (1997).

    Article  CAS  Google Scholar 

  114. Horak, R. E. A. et al. Ammonia oxidation kinetics and temperature sensitivity of a natural marine community dominated by Archaea. ISME J. 7, 2023–2033 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Baer, S. E. et al. Effect of temperature on rates of ammonium uptake and nitrification in the western coastal Arctic during winter, spring, and summer. Global Biogeochem. Cyc. 28, 1455–1466 (2014).

    Article  CAS  Google Scholar 

  116. Fenchel, T. & Finlay, B. Oxygen and the spatial structure of microbial communities. Biol. Rev. 83, 553–569 (2008).

    PubMed  Google Scholar 

  117. Bianchi, D., Dunne, J. P., Sarmiento, J. L. & Galbraith, E. D. Data-based estimates of suboxia, denitrification, and N2O production in the ocean and their sensitivities to dissolved O2 . Global Biogeochem. Cyc. 26, GB2009 (2012).

    Article  CAS  Google Scholar 

  118. Robinson, R., Mix, A. & Martinez, P. Southern Ocean control on the extent of denitrification in the southeast Pacific over the last 70 ka. Quat. Sci. Rev. 26, 201–212 (2007).

    Article  Google Scholar 

  119. Stramma, L., Johson, G. C., Sprintall, J. & Mohrholz, V. Extending oxygen-minimum zones in the tropical oceans. Science 320, 655–658 (2008).

    Article  CAS  PubMed  Google Scholar 

  120. Deutsch, C. et al. Climate-forced variability of ocean hypoxia. Science 333, 336–339 (2011).

    Article  CAS  PubMed  Google Scholar 

  121. Horak, R. E. A., Ruef, W., Ward, B. B. & Devol, A. H. Expansion of denitrification and anoxia in the eastern tropical North Pacific from 1972 to 2012. Geophys. Res. Lett. 43, 5252–5260 (2016).

    Article  CAS  Google Scholar 

  122. Kalvelage, T. et al. Oxygen sensitivity of anammox and coupled N-cycle processes in oxygen minimum zones. PLoS ONE 6, e29299 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Kim, H. Review of inorganic nitrogen transformations and effect of global climate change on inorganic nitrogen cycling in ocean ecosystems. Ocean Sci. J. 51, 159 (2016).

    Article  CAS  Google Scholar 

  124. Schmittner, A., Oschlies, A., Matthews, H. D. & Galbraith, E. D. Future changes in climate, ocean circulation, ecosystems, and biogeochemical cycling simulated for a business-as-usual CO2 emission scenario until year 4000 AD. Global Biogeochem. Cyc. 22, GB1013 (2008).

    Article  CAS  Google Scholar 

  125. Frolicher, T. L. et al. Natural variability and anthropogenic trends in oceanic oxygen in a coupled carbon cycle-climate model ensemble. Global Biogeochem. Cyc. 23, GB1003 (2008).

    Google Scholar 

  126. Gnandashian, A., Dunne, J. P. & John, J. Understanding why the volume of suboxic waters does not increase over centuries of global warming in an Earth System Model. Biogeosciences 9, 1159–1172 (2012).

    Article  Google Scholar 

  127. Sunda, W. G. & Cai, W.-J. Eutrophication induced CO2 acidification of subsurface coastal waters: interactive effects of temperature, salinity, and atmospheric pCO2 Environ. Sci. Technol. 46, 10651–10659 (2012).

    Article  CAS  PubMed  Google Scholar 

  128. Ito, T. et al. Acceleration of oxygen decline in the tropical Pacific over the past decades by aerosol pollutants. Nat. Geosci. 9, 409–470 (2016).

    Article  CAS  Google Scholar 

  129. Hughes, J. B. et al. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4, 102–112 (2006).

    Article  CAS  Google Scholar 

  130. Hallegraeff, G. M. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J. Phycol. 46, 220–235 (2010).

    Article  CAS  Google Scholar 

  131. Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).

    Article  Google Scholar 

  132. Sul, W. J. et al. Marine bacteria exhibit a bipolar distribution. Proc. Natl Acad. Sci. USA 110, 2342–2347 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Doblin, M. A. & van Sebille, E. Drift in ocean currents impacts intergenerational microbial exposure to temperature. Proc. Natl Acad. Sci. USA 113, 5700–5705 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Hallegraef, G. M. & Bolch, C. J. Transport of diatom and dinoflagellate resting spores in ships ballast water- implications for plankton biogeography and aquaculture. J. Plankton Res. 14, 1067–1084 (1992).

    Article  Google Scholar 

  135. Doblin, M. A. et al. Transport of the harmful bloom alga Aureococcus anophagefferens by oceangoing ships and coastal boats. Appl. Environ. Microbiol. 70, 6495–6500 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Richardson, A. J. & Schoeman, D. S. Climate impact on plankton ecosystems in the Northeast Atlantic. Science 305, 1609–1612 (2004).

    Article  CAS  PubMed  Google Scholar 

  137. Winter, A. et al. Poleward expansion of the coccolithophore Emiliania huxleyi. J. Plankton Res. 36, 316–325 (2014).

    Article  CAS  Google Scholar 

  138. Flombaum, P. et al. Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proc. Natl Acad. Sci. USA 110, 9824–9829 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Breitbarth, E., Oschlies, A. & LaRoche, L. Physiological constraints on the global distribution of Trichodesmium- effect of temperature on diazotrophy. Biogeosciences 4, 53–61 (2007).

    Article  CAS  Google Scholar 

  140. Boyd, P. W. et al. Marine phytoplankton temperature versus growth responses from polar to tropical waters – outcome of a scientific community-wide study. PLoS ONE 8, e63091 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Irwin, A. J., Finkel, Z. V., Müller-Karger, F. E. & Ghinaglia, L. T. Phytoplankton adapt to changing ocean environments. Proc. Natl Acad. Sci. USA 112, 5762–5766 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Barton, A. D., Irwin, A. J., Finkel, Z. V. & Stock, C. A. Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities. Proc. Natl Acad. Sci. USA 113, 2964–2969 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Litchman, E. & Klausmeier, C. A. Trait-based community ecology of phytoplankton. Annu. Rev. Ecol. Evol. Syst. 39, 615–639 (2008).

    Article  Google Scholar 

  144. Barton, A. D. et al. The biogeography of marine plankton traits. Ecol. Lett. 16, 522–534 (2013).

    Article  PubMed  Google Scholar 

  145. Collins, S., Rost, B. & Rynearson, T. A. Evolutionary potential of marine phytoplankton under ocean acidification. Evol. Appl. 7, 140–155 (2014).

    Article  CAS  PubMed  Google Scholar 

  146. Miller, K. R., Chapman, M. R., Andrews, J. E. & Koç, N. Diatom phytoplankton response to Holocene climate change in the Subpolar North Atlantic. Glob. Planet. Change 79, 214–225 (2011).

    Article  Google Scholar 

  147. O’Dea, S. A. et al. Coccolithophore calcification response to past ocean acidification and climate change. Nat. Commun. 5, 5363 (2014)

    Article  PubMed  Google Scholar 

  148. Hannisdal, B., Henderiks, J. & Liow, L. H. Long-term evolutionary and ecological responses of calcifying phytoplankton to changes in atmospheric CO2 . Glob. Change Biol. 18, 3504–3516 (2012).

    Article  Google Scholar 

  149. Davis, C. V., Badger, M. P. S., Bown, P. R. & Schmidt, D. N. The response of calcifying plankton to climate change in the Pliocene. Biogeosciences 10, 6131–6139 (2013).

    Article  CAS  Google Scholar 

  150. Lohbeck, K. T., Riebesell, U. & Reusch, T. B. H. Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 5, 346–351 (2012).

    Article  CAS  Google Scholar 

  151. Lohbeck, K. T., Riebesell, U., Collins, S. & Reusch, T. B. H. Functional genetic divergence in high CO2 adapted Emiliania huxleyi populations. Evolution 67, 1892–1900 (2012).

    Article  PubMed  Google Scholar 

  152. Schlüter, L. et al. Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat. Clim. Change 4, 1024–1030 (2014).

    Article  CAS  Google Scholar 

  153. Schaum, C. E. & Collins, S. Plasticity predicts evolution in a marine alga. Proc. Biol. Sci. 281, 20141486 (2014).

    PubMed  PubMed Central  Google Scholar 

  154. Schaum, C. E., Rost, B. & Collins, S. Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton. ISME J. 10, 75–84 (2016).

    Article  CAS  PubMed  Google Scholar 

  155. Walworth, N. G. et al. Molecular and physiological evidence of genetic assimilation to high CO2 in the marine nitrogen fixer Trichodesmium. Proc. Natl Acad. Sci. USA 113, E7367–E7374 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Garcia, N. S., Fu, F.-X., Sedwick, P. N. & Hutchins, D. A. Iron deficiency increases growth and nitrogen fixation rates of phosphorus-deficient marine cyanobacteria. ISME J. 9, 238–245 (2015).

    Article  CAS  PubMed  Google Scholar 

  157. Tatters, A. O. et al. Short- and long-term conditioning of a temperate marine diatom community to acidification and warming. Phil. Trans. R. Soc. B 368, 20120437 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  158. Tatters, A. O. et al. Short- versus long-term responses to changing CO2 in a coastal dinoflagellate bloom: Implications for interspecific competitive interactions and community structure. Evolution 67, 1879–1891 (2013).

    Article  PubMed  Google Scholar 

  159. Scheinin, M. et al. Experimental evolution gone wild. J. R. Soc. Interface 12, 20150056 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Support was provided by US National Science Foundation grants OCE 1260490, OCE 1538525, and OCE 1657757 to D.A.H. and F.F. Thanks to J. Brown and the Wrigley Institute of Environmental Sciences for assistance with graphics.

Author information

Authors and Affiliations

Authors

Contributions

D.A.H. developed much of the material presented and wrote the paper, with major contributions from F.F.

Corresponding author

Correspondence to David A. Hutchins.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hutchins, D., Fu, F. Microorganisms and ocean global change. Nat Microbiol 2, 17058 (2017). https://doi.org/10.1038/nmicrobiol.2017.58

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nmicrobiol.2017.58

  • Springer Nature Limited

This article is cited by

Navigation