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Diatom acclimation to elevated CO2 via cAMP signalling and coordinated gene expression

Nature Climate Change volume 5, pages 761–765 (2015)Cite this article

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Abstract

Diatoms are responsible for ∼40% of marine primary productivity1, fuelling the oceanic carbon cycle and contributing to natural carbon sequestration in the deep ocean2. Diatoms rely on energetically expensive carbon concentrating mechanisms (CCMs) to fix carbon efficiently at modern levels of CO2 (refs 3, 4, 5). How diatoms may respond over the short and long term to rising atmospheric CO2 remains an open question. Here we use nitrate-limited chemostats to show that the model diatom Thalassiosira pseudonana rapidly responds to increasing CO2 by differentially expressing gene clusters that regulate transcription and chromosome folding, and subsequently reduces transcription of photosynthesis and respiration gene clusters under steady-state elevated CO2. These results suggest that exposure to elevated CO2 first causes a shift in regulation, and then a metabolic rearrangement. Genes in one CO2-responsive cluster included CCM and photorespiration genes that share a putative cAMP-responsive cis-regulatory sequence, implying these genes are co-regulated in response to CO2, with cAMP as an intermediate messenger. We verified cAMP-induced downregulation of CCM gene δ-CA3 in nutrient-replete diatom cultures by inhibiting the hydrolysis of cAMP. These results indicate an important role for cAMP in downregulating CCM and photorespiration genes under elevated CO2 and provide insights into mechanisms of diatom acclimation in response to climate change.

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Figure 1: Gene set enrichment in transition and steady-state nitrate-limited cultures.
Figure 2: Clusters of co-expressed genes versus CO2 in transition and steady-state experiments.
Figure 3: cAMP and CO2 dependence of gene expression in nutrient-replete cultures.
Figure 4: Model of cell signalling and metabolite fluxes in T. pseudonana after acclimation to high CO2.

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Acknowledgements

National Science Foundation (Grants OCB-0928561 and MCB-1316206 to M.V.O. and N.S.B.; OCE-0927238 to E.V.A.), Gordon and Betty Moore Foundation (Grant 537.01 to E.V.A.). We thank S. Amin for comments on the manuscript and B. Durham for advice on RT-qPCR.

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Authors and Affiliations

  1. School of Oceanography, University of Washington, Seattle, Washington 98105, USA

    Gwenn M. M. Hennon, Ryan D. Groussman, Chris Berthiaume, Rhonda L. Morales & E. V. Armbrust

  2. Institute for Systems Biology, Seattle, Washington 98109, USA

    Justin Ashworth, Nitin S. Baliga & Mónica V. Orellana

  3. Polar Science Center, University of Washington, Seattle, Washington 98105, USA

    Mónica V. Orellana

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  1. Gwenn M. M. Hennon
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  8. E. V. Armbrust
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Contributions

G.M.M.H., R.L.M. and R.D.G. carried ot RNA sample preparation, sequencing and RT-qPCR. G.M.M.H., J.A. and C.B carried out bioinformatics and statistics. G.M.M.H., J.A., M.V.O., N.S.B. and E.V.A. carried out experimental design. The manuscript was prepared by G.M.M.H., J.A., R.D.G. and E.V.A. All authors contributed to discussion of results and comments on the manuscript.

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Correspondence to Gwenn M. M. Hennon or E. V. Armbrust.

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Hennon, G., Ashworth, J., Groussman, R. et al. Diatom acclimation to elevated CO2 via cAMP signalling and coordinated gene expression. Nature Clim Change 5, 761–765 (2015). https://doi.org/10.1038/nclimate2683

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