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


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.

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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.


  1. 1

    Falkowski, P. G. Biogeochemical controls and feedbacks on ocean primary production. Science 281, 200–206 (1998).

    CAS  Article  PubMed  Google Scholar 

  2. 2

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

    CAS  Article  Google Scholar 

  3. 3

    Field, C. B. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

    CAS  Article  PubMed  Google Scholar 

  4. 4

    Falkowski, P. G. The role of phytoplankton photosynthesis in global biogeochemical cycles. Photosynth. Res. 39, 235–258 (1994).

    CAS  Article  PubMed  Google Scholar 

  5. 5

    Bopp, L. et al. Potential impact of climate change on marine export production. Glob. Biogeochem. Cycles 15, 81–99 (2001).

    CAS  Article  Google Scholar 

  6. 6

    López-Urrutia, Á., Martin, E. S., Harris, R. P. & Irigoien, X. Scaling the metabolic balance of the oceans. Proc. Natl Acad. Sci. USA 103, 8739–8744 (2006).

    Article  PubMed  Google Scholar 

  7. 7

    Laufkötter, C. et al. Drivers and uncertainties of future global marine primary production in marine ecosystem models. Biogeosciences 12, 6955–6984 (2015).

    Article  Google Scholar 

  8. 8

    Regaudie-de-Gioux, A. & Duarte, C. M. Compensation irradiance for planktonic community metabolism in the ocean. Glob. Biogeochem. Cycles 24, GB4013 (2010).

    Article  Google Scholar 

  9. 9

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

    Article  Google Scholar 

  10. 10

    Padfield, D., Yvon-Durocher, G., Buckling, A., Jennings, S. & Yvon-Durocher, G. Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton. Ecol. Lett. 19, 133–142 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11

    Listmann, L., LeRoch, M., Schluter, L., Thomas, M. K. & Reusch, T. B. H. Swift thermal reaction norm evolution in a key marine phytoplankton species. Evol. Appl. 9, 1156–1164 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12

    Raven, J. A. & Geider, R. J. Temperature and algal growth. New Phytol. 110, 441–461 (1988).

    CAS  Article  Google Scholar 

  13. 13

    Lawrence, D., Bell, T. & Barraclough, T. G. The effect of immigration on the adaptation of microbial communities to warming. Am. Nat. 187, 236–248 (2016).

    Article  PubMed  Google Scholar 

  14. 14

    Lawrence, D. et al. Species interactions alter evolutionary responses to a novel environment. PLoS Biol. 10, e1001330 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15

    Collins, S. Competition limits adaptation and productivity in a photosynthetic alga at elevated CO2 . Proc. R. Soc. B 278, 247–255 (2010).

    Article  PubMed  Google Scholar 

  16. 16

    Yvon-Durocher, G., Jones, J. I., Trimmer, M., Woodward, G. & Montoya, J. M. Warming alters the metabolic balance of ecosystems. Phil. Trans. R. Soc. B 365, 2117–2126 (2010).

    Article  PubMed  Google Scholar 

  17. 17

    Yvon-Durocher, G. et al. Five years of experimental warming increases the biodiversity and productivity of phytoplankton. PLoS Biol. 13, e1002324 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  18. 18

    Geider, R. J., MacIntyre, H. L. & Kana, T. M. Dynamic model of phytoplankton growth and acclimation: responses of the balanced growth rate and the chlorophyll a:carbon ratio to light, nutrient-limitation and temperature. Mar. Ecol. Prog. Ser. 144, 187–200 (1997).

    Article  Google Scholar 

  19. 19

    Badger, M. R., von Caemmerer, S., Ruuska, S. & Nakano, H. Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Phil. Trans. R. Soc. B 355, 1433–1446 (2000).

    CAS  Article  PubMed  Google Scholar 

  20. 20

    Houille-Vernes, L. & Rappaport, F. Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas . Proc. Natl Acad. Sci. USA 108, 20820–20825 (2011).

    CAS  Article  PubMed  Google Scholar 

  21. 21

    Erickson, E., Wakao, S. & Niyogi, K. K. Light stress and photoprotection in Chlamydomonas reinhardtii . Plant J. 82, 449–465 (2015).

    CAS  Article  PubMed  Google Scholar 

  22. 22

    Atkin, O. K. et al. Global variability in leaf respiration in relation to climate, plant functional types and leaf traits. New Phytol. 206, 614–636 (2015).

    CAS  Article  PubMed  Google Scholar 

  23. 23

    Yvon-Durocher, G., Dossena, M., Trimmer, M., Woodward, G. & Allen, A. P. Temperature and the biogeography of algal stoichiometry. Glob. Ecol. Biogeogr. 24, 562–570 (2015).

    Article  Google Scholar 

  24. 24

    Toseland, A. et al. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat. Clim. Change 3, 979–984 (2013).

    CAS  Article  Google Scholar 

  25. 25

    Berman-Frank, I. & Dubinsky, Z. Balanced growth in aquatic plants: myth or reality? Phytoplankton use the imbalance between carbon assimilation and biomass production to their strategic advantage. BioScience 49, 29–37 (1999).

    Article  Google Scholar 

  26. 26

    Yvon-Durocher, G., Montoya, J. M., Trimmer, M. & Woodward, G. Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems. Glob. Change Biol. 17, 1681–1694 (2011).

    Article  Google Scholar 

  27. 27

    IPCC Climate Change 2014: Synthesis Report (eds Pachauri, R. K. & Meyer, L. A.) (Cambridge Univ. Press, 2014).

    Google Scholar 

  28. 28

    Nakada, T., Shinkawa, H., Ito, T. & Tomita, M. Recharacterization of Chlamydomonas reinhardtii and its relatives with new isolates from Japan. J. Plant Res. 123, 67–78 (2009).

    Article  PubMed  Google Scholar 

  29. 29

    Rambaut, A. FigTree version 1.4.2. (2014);

  30. 30

    Buchanan, R. L., Whiting, R. C. & Damert, W. C. When is simple good enough: a comparison of the Gompertz, Baranyi, and three-phase linear models for fitting bacterial growth curves. Food Microbiol. 14, 313–326 (1997).

    Article  Google Scholar 

  31. 31

    Elzhov, T. V., Mullen, K. M., Spiess, A. N. & Bolker, B. minpack.lm: R interface to the Levenberg-Marquardt nonlinear least-squares algorithm found in MINPACK, plus support for bounds. R package version 1.2-1 (2013);

  32. 32

    Edwards, K. F., Thomas, M. K., Klausmeier, C. A. & Litchman, E. Phytoplankton growth and the interaction of light and temperature: a synthesis at the species and community level. Limnol. Oceanogr. 61, 1232–1244 (2016).

    Article  Google Scholar 

  33. 33

    Eilers, P. H. C. & Peeters, J. C. H. A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol. Model. 42, 199–215 (1988).

    Article  Google Scholar 

  34. 34

    Suggett, D. J., Moore, C. M., Hickman, A. E. & Geider, R. J. Interpretation of fast repetition rate (FRR) fluorescence: signatures of phytoplankton community structure versus physiological state. Mar. Ecol. Prog. Ser. 376, 1–19 (2009).

    Article  Google Scholar 

  35. 35

    Atkinson, D., Ciotti, B. J. & Montagnes, D. J. S. Protists decrease in size linearly with temperature: ca. 2.5% °C−1 . Proc. R. Soc. B 270, 2605–2611 (2003).

    Article  PubMed  Google Scholar 

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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).

Author information




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.

Corresponding authors

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, C., 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).

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