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Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis

Nature Ecology & Evolution volume 1, Article number: 0094 (2017) Cite this article

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Abstract

Phytoplankton photosynthesis is a critical flux in the carbon cycle, accounting for approximately 40% of the carbon dioxide fixed globally on an annual basis and fuelling the productivity of aquatic food webs. However, rapid evolutionary responses of phytoplankton to warming remain largely unexplored, particularly outside the laboratory, where multiple selection pressures can modify adaptation to environmental change. Here, we use a decade-long experiment in outdoor mesocosms to investigate mechanisms of adaptation to warming (+4 °C above ambient temperature) in the green alga Chlamydomonas reinhardtii, in naturally assembled communities. Isolates from warmed mesocosms had higher optimal growth temperatures than their counterparts from ambient treatments. Consequently, warm-adapted isolates were stronger competitors at elevated temperature and experienced a decline in competitive fitness in ambient conditions, indicating adaptation to local thermal regimes. Higher competitive fitness in the warmed isolates was linked to greater photosynthetic capacity and reduced susceptibility to photoinhibition. These findings suggest that adaptive responses to warming in phytoplankton could help to mitigate projected declines in aquatic net primary production by increasing rates of cellular net photosynthesis.

The formation of organic carbon by phytoplankton (net primary production, NPP) is a key flux in the carbon cycle1,2, contributing to nearly half of the carbon dioxide fixed globally on an annual basis3,4. There are currently major concerns that global warming will reduce aquatic NPP, due to increased nutrient limitation5, and because rates of respiration and zooplankton grazing tend to be more sensitive to rising temperatures than those of photosynthesis6–8. These projections, however, do not account for the capacity for phytoplankton to adapt rapidly to environmental change. Although ample evidence for rapid evolutionary responses in phytoplankton to warming exists9–11, our current understanding is based on highly simplified laboratory experiments, where populations are allowed to adapt free from natural enemies or competitors and where individual abiotic variables are manipulated in isolation. Consequently, we lack understanding of the mechanisms that govern evolutionary responses of phytoplankton to warming in sufficient detail and under a realistic ecological context, to capture the dynamics of thermal adaptation in models of aquatic biogeochemistry5–8.

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Figure 1: Patterns of local thermal adaptation.
Figure 2: Competitive fitness of the warmed relative to the ambient isolates at 16 and 34 °C.
Figure 3: Differences in photochemical traits between the warmed and ambient isolates.
Figure 4: Shifts in metabolic traits between warmed and ambient isolates.
Figure 5: Higher rates of NP are linked to greater competitive fitness in the warm-adapted isolates.

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Acknowledgements

This study was supported by a grant from the Leverhulme Trust (RPG-2013-335) awarded to G.Y.-D, A.B. and N.S., and an NERC grant awarded to S.P. and G.Y.-D. (NE/M003205/1).

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Authors and Affiliations

  1. Environment and Sustainability Institute, University of Exeter,

    C.-Elisa Schaum, Samuel Barton, Elvire Bestion, Angus Buckling, Paula Lopez & Gabriel Yvon-Durocher

  2. Penryn Campus,, Penryn, TR10 9EZ, Cornwall, UK

    C.-Elisa Schaum, Samuel Barton, Elvire Bestion, Angus Buckling, Paula Lopez & Gabriel Yvon-Durocher

  3. Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK

    Bernardo Garcia-Carreras & Samraat Pawar

  4. Biosciences, Daphne du Maurier Building, University of Exeter, Penryn Campus, Penryn, TR10 9FE, Cornwall, UK

    Chris Lowe

  5. School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, UK

    Nicholas Smirnoff

  6. Geoffrey Pope Building, University of Exeter, Exeter EX4 4QD, UK

    Mark Trimmer

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  1. C.-Elisa Schaum
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Contributions

G.Y.-D. conceived the study. C.-E.S. and G.Y.-D. designed the experimental work, and P.L., C.-E.S., S.B. and E.B. conducted the experiment. C.-E.S. and G.Y.-D. analysed the data. M.T. maintains the experimental mesocosms. C.-E.S. and G.Y.-D. wrote the manuscript and all authors contributed to revisions.

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Correspondence to C.-Elisa Schaum or Gabriel Yvon-Durocher.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1–5, Supplementary Tables 1–5. (PDF 2229 kb)

Supplementary Data 1

Data used for Figures 1–5. (XLSX 33 kb)

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Schaum, CE., Barton, S., Bestion, E. et al. Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis. Nat Ecol Evol 1, 0094 (2017). https://doi.org/10.1038/s41559-017-0094

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