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The impact of temperature on marine phytoplankton resource allocation and metabolism

Abstract

Marine phytoplankton are responsible for 50% of the CO2 that is fixed annually worldwide, and contribute massively to other biogeochemical cycles in the oceans1. Their contribution depends significantly on the interplay between dynamic environmental conditions and the metabolic responses that underpin resource allocation and hence biogeochemical cycling in the oceans. However, these complex environment–biome interactions have not been studied on a larger scale. Here we use a set of integrative approaches that combine metatranscriptomes, biochemical data, cellular physiology and emergent phytoplankton growth strategies in a global ecosystems model, to show that temperature significantly affects eukaryotic phytoplankton metabolism with consequences for biogeochemical cycling under global warming. In particular, the rate of protein synthesis strongly increases under high temperatures even though the numbers of ribosomes and their associated rRNAs decreases. Thus, at higher temperatures, eukaryotic phytoplankton seem to require a lower density of ribosomes to produce the required amounts of cellular protein. The reduction of phosphate-rich ribosomes2 in warmer oceans will tend to produce higher organismal nitrogen (N) to phosphate (P) ratios, in turn increasing demand for N with consequences for the marine carbon cycle due to shifts towards N-limitation. Our integrative approach suggests that temperature plays a previously unrecognized, critical role in resource allocation and marine phytoplankton stoichiometry, with implications for the biogeochemical cycles that they drive.

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Figure 1: Sampling sites for eukaryotic phytoplankton metatranscriptomes and sequence distribution.
Figure 2: Heatmaps for algal groups and biological processes.
Figure 3: The impact of temperature on translation.
Figure 4: Phytoplankton cell model and N:P ratios.

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Acknowledgements

Sequencing of ANT, EPAC and NPAC was funded by a Natural Environment Research Council (NERC) grant (MGF (NBAF) grant 197) and a 454 Life Sciences grant (Roche, 10Gb grant) awarded to T.M. and K.V. K.V. acknowledges the DFG for funding. Sequencing of ARC and NATL was funded by the EU FP7 project ‘Arctic Tipping Points’ awarded to G.A.P. We thank The Genome Analysis Centre (TGAC) in Norwich and Melanie Febrer for facilitating the work with 454 Life Sciences (Roche) in the US and UK. S.J.D., J.R.C. and T.M.L. acknowledge the Leverhulme Trust (F/00 204/AP) for funding. The PhD studentship of A.T. was funded by the Earth and Life Systems Alliance (ELSA) in Norwich. A.K. and T.M. acknowledge the Leverhulme Trust (F/00204/AU) for funding. Part of the bioinformatic analysis was performed on the High Performance Computing Cluster supported by the Research and Specialist Computing Support service at the University of East Anglia. We thank S. Moxon for his patient support, discussions and suggestions. We thank W. Guo and A. Marchetti for providing us with samples from EPAC and M. Parker, E. V. Armbrust, and the ‘Sorcerer II’ crew (JCVI) for assistance with sampling of NPAC. G.A.P. acknowledges A. Ramos, E. Serrão and the crew of R/V Jan Mayen, University Tromso, Norway for assistance with sampling of ARC and NATL.

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Metatranscriptome sample preparation: T.M., G.A.P., K.V. and C.U.; Bioinformatics: A.T. and V.M.; Western blots: A.K.; Quantitative PCR: J.S.; Growth experiments: A.K., J.S. and T.M.; Modelling: S.J.D., J.R.C., T.M.L.; T.M. designed the study and wrote the manuscript with help from S.J.D. and T.M.L. All authors discussed the results and commented on the manuscript.

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Correspondence to T. Mock.

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Toseland, A., Daines, S., Clark, J. et al. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nature Clim Change 3, 979–984 (2013). https://doi.org/10.1038/nclimate1989

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