Review Article | Published:

Microorganisms and ocean global change

Nature Microbiology volume 2, Article number: 17058 (2017) | Download Citation

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

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

  2. 2.

    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).

  3. 3.

    , , & Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar. Ecol. Prog. Ser. 470, 167–189 (2012).

  4. 4.

    , , & A global pattern of thermal adaptation in marine phytoplankton. Science 338, 1085–1088 (2012).

  5. 5.

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

  6. 6.

    & Oceanic sinks for atmospheric CO2. Plant Cell Environ. 22, 741–755 (1999).

  7. 7.

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

  8. 8.

    , & Warming and ocean acidification effects on phytoplankton—from species shifts to size shifts within species in a mesocosm experiment. PLoS ONE (2015).

  9. 9.

    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).

  10. 10.

    & Marine phytoplankton and the changing ocean iron cycle. Nat. Clim. Change 6, 1071–1079 (2016).

  11. 11.

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

  12. 12.

    , , & 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).

  13. 13.

    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).

  14. 14.

    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).

  15. 15.

    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).

  16. 16.

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

  17. 17.

    , & 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).

  18. 18.

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

  19. 19.

    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).

  20. 20.

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

  21. 21.

    & Harmful cyanobacterial blooms: causes, consequences, and controls. Microb. Ecol. 65, 995–1010 (2013).

  22. 22.

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

  23. 23.

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

  24. 24.

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

  25. 25.

    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).

  26. 26.

    , & High CO2 and silicate limitation synergistically increase the toxicity of Pseudo-nitzschia fraudulenta. PLoS ONE 7, e32116 (2012).

  27. 27.

    , & Global change and the future of harmful algal blooms in the ocean. Mar. Ecol. Prog. Ser. 470, 207–233 (2012).

  28. 28.

    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).

  29. 29.

    , , & Reponses of the dinoflagellate Karenia brevis to climate change: pCO2 and sea surface temperatures. Harmful Algae 37, 110–116 (2014).

  30. 30.

    , , , & Impact of elevated pCO2 on paralytic shellfish poisoning toxin content and composition in Alexandrium tamarense. Toxicon 78, 58–67 (2014).

  31. 31.

    & Experimental evolution meets marine phytoplankton. Evolution 67, 1849–1859 (2013).

  32. 32.

    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).

  33. 33.

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

  34. 34.

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

  35. 35.

    & Understanding the responses of ocean biota to a complex matrix of cumulative anthropogenic change. Mar. Ecol. Prog. Ser. 470, 125–135 (2012).

  36. 36.

    & Commentary: lessons learned from ocean acidification research. Nat. Clim. Change 5, 12–14 (2015).

  37. 37.

    & Environmental controls on coccolithophore calcification. Mar. Ecol. Prog. Ser. 470, 137–166 (2012).

  38. 38.

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

  39. 39.

    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).

  40. 40.

    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).

  41. 41.

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

  42. 42.

    , , , & Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6, 2637–2646 (2009).

  43. 43.

    , & Differing responses of three Southern Ocean Emiliania huxleyi ecotypes to changing seawater carbonate chemistry. Mar. Ecol. Prog. Ser. 531, 81–90 (2015).

  44. 44.

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

  45. 45.

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

  46. 46.

    Phytoplankton calcification in a high-CO2 world. Science 320, 336–340 (2008).

  47. 47.

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

  48. 48.

    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).

  49. 49.

    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).

  50. 50.

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

  51. 51.

    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).

  52. 52.

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

  53. 53.

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

  54. 54.

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

  55. 55.

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

  56. 56.

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

  57. 57.

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

  58. 58.

    , & Will ocean acidification affect marine microbes? ISME J. 5, 1–7 (2011).

  59. 59.

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

  60. 60.

    , , & Testing the effect of CO2 concentration on the dynamics of marine heterotrophic bacterioplankton. Limnol. Oceanogr. 51, 1–11 (2006).

  61. 61.

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

  62. 62.

    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).

  63. 63.

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

  64. 64.

    , , & Marine bacterial communities are resistant to elevated carbon dioxide levels. Environ. Microbiol. Rep. 6, 574–582 (2014).

  65. 65.

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

  66. 66.

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

  67. 67.

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

  68. 68.

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

  69. 69.

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

  70. 70.

    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).

  71. 71.

    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).

  72. 72.

    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).

  73. 73.

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

  74. 74.

    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).

  75. 75.

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

  76. 76.

    , , & Experimental warming decreases the average size and nucleic acid content of marine bacterial communities. Front. Microbiol. 7, 730 (2016).

  77. 77.

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

  78. 78.

    , , & Away from darkness: a review on the effects of solar radiation on heterotrophic bacterioplankton activity. Front. Microbiol. 4, 131 (2013).

  79. 79.

    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).

  80. 80.

    , & Emerging patterns of marine nitrogen fixation, Nat. Rev. Microbiol. 9, 499–508 (2011).

  81. 81.

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

  82. 82.

    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).

  83. 83.

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

  84. 84.

    , & Physiological response of Crocosphaera watsonii to enhanced and fluctuating carbon dioxide conditions. PLoS ONE 9, e110660 (2014).

  85. 85.

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

  86. 86.

    , & Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22, 128–145 (2009).

  87. 87.

    , , & Occurrence of nitrogen fixing cyanobacterium Trichodesmium under elevated pCO2 conditions in the Western Bay of Bengal. Int. J. Oceanogr. 2013, 350465 (2013).

  88. 88.

    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).

  89. 89.

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

  90. 90.

    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).

  91. 91.

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

  92. 92.

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

  93. 93.

    , & Cyanobacteria and ultraviolet radiation (UVR) stress: mitigation strategies. Ageing Res. Rev. 9, 79–90 (2010).

  94. 94.

    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).

  95. 95.

    , & Colimitation of the unicellular photosynthetic diazotroph Crocosphaera watsonii by phosphorus, light, and carbon dioxide. Limnol. Oceanogr. 58, 1501–1512 (2013).

  96. 96.

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

  97. 97.

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

  98. 98.

    , , & 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).

  99. 99.

    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).

  100. 100.

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

  101. 101.

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

  102. 102.

    , , & The significance of nitrification for oceanic new production. Nature 447, 999–1002 (2007).

  103. 103.

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

  104. 104.

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

  105. 105.

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

  106. 106.

    , & The inhibition of N2O production by ocean acidification in cold temperate and polar waters. Deep-Sea Res. II 127, 93–101 (2016).

  107. 107.

    , , & Assessing the role of pH in determining water column nitrification rates in a coastal system. Estuar. Coast 34, 1095–1102 (2011).

  108. 108.

    , , & Impacts of ocean acidification on sediment processes in shallow waters of the Arctic Ocean. PLoS ONE 9, e94068 (2014).

  109. 109.

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

  110. 110.

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

  111. 111.

    , , & Acidification alters the composition of ammonia-oxidizing microbial assemblages in marine mesocosms. Mar. Ecol. Prog. Ser. 492, 1–8 (2013).

  112. 112.

    , , , & 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).

  113. 113.

    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).

  114. 114.

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

  115. 115.

    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).

  116. 116.

    & Biol. Rev. 83, 553–569 (2008).

  117. 117.

    , , & Data-based estimates of suboxia, denitrification, and N2O production in the ocean and their sensitivities to dissolved O2. Global Biogeochem. Cyc. 26, GB2009 (2012).

  118. 118.

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

  119. 119.

    , , & Extending oxygen-minimum zones in the tropical oceans. Science 320, 655–658 (2008).

  120. 120.

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

  121. 121.

    , , & Expansion of denitrification and anoxia in the eastern tropical North Pacific from 1972 to 2012. Geophys. Res. Lett. 43, 5252–5260 (2016).

  122. 122.

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

  123. 123.

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

  124. 124.

    , , & 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).

  125. 125.

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

  126. 126.

    , & 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).

  127. 127.

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

  128. 128.

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

  129. 129.

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

  130. 130.

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

  131. 131.

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

  132. 132.

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

  133. 133.

    & Drift in ocean currents impacts intergenerational microbial exposure to temperature. Proc. Natl Acad. Sci. USA 113, 5700–5705 (2016).

  134. 134.

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

  135. 135.

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

  136. 136.

    & Climate impact on plankton ecosystems in the Northeast Atlantic. Science 305, 1609–1612 (2004).

  137. 137.

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

  138. 138.

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

  139. 139.

    , & Physiological constraints on the global distribution of Trichodesmium- effect of temperature on diazotrophy. Biogeosciences 4, 53–61 (2007).

  140. 140.

    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).

  141. 141.

    , , & Phytoplankton adapt to changing ocean environments. Proc. Natl Acad. Sci. USA 112, 5762–5766 (2015).

  142. 142.

    , , & Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities. Proc. Natl Acad. Sci. USA 113, 2964–2969 (2016).

  143. 143.

    & Trait-based community ecology of phytoplankton. Annu. Rev. Ecol. Evol. Syst. 39, 615–639 (2008).

  144. 144.

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

  145. 145.

    , & Evolutionary potential of marine phytoplankton under ocean acidification. Evol. Appl. 7, 140–155 (2014).

  146. 146.

    , , & Diatom phytoplankton response to Holocene climate change in the Subpolar North Atlantic. Glob. Planet. Change 79, 214–225 (2011).

  147. 147.

    et al. Coccolithophore calcification response to past ocean acidification and climate change. Nat. Commun. 5, 5363 (2014)

  148. 148.

    , & Long-term evolutionary and ecological responses of calcifying phytoplankton to changes in atmospheric CO2. Glob. Change Biol. 18, 3504–3516 (2012).

  149. 149.

    , , & The response of calcifying plankton to climate change in the Pliocene. Biogeosciences 10, 6131–6139 (2013).

  150. 150.

    , & Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 5, 346–351 (2012).

  151. 151.

    , , & Functional genetic divergence in high CO2 adapted Emiliania huxleyi populations. Evolution 67, 1892–1900 (2012).

  152. 152.

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

  153. 153.

    & Plasticity predicts evolution in a marine alga. Proc. Biol. Sci. 281, 20141486 (2014).

  154. 154.

    , & Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton. ISME J. 10, 75–84 (2016).

  155. 155.

    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).

  156. 156.

    , , & Iron deficiency increases growth and nitrogen fixation rates of phosphorus-deficient marine cyanobacteria. ISME J. 9, 238–245 (2015).

  157. 157.

    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).

  158. 158.

    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).

  159. 159.

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

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

Affiliations

  1. Marine and Environmental Biology, University of Southern California, Los Angeles, California 90089, USA.

    • David A. Hutchins
    •  & Feixue Fu

Authors

  1. Search for David A. Hutchins in:

  2. Search for Feixue Fu in:

Contributions

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

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to David A. Hutchins.

About this article

Publication history

Received

Accepted

Published

DOI

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

Further reading