Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

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.

References

  1. Nelson, D. M., Treguer, P., Brzezinski, M. A., Leynaert, A. & Queguiner, B. Production and dissolution of biogenic silica in the ocean: Revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob. Biogeochem. Cycles 9, 359–372 (1995).

    Article  CAS  Google Scholar 

  2. Ducklow, H. W., Steinberg, D. K. & Buesseler, K. O. Upper ocean carbon export and the biological pump. Oceanography 14, 50–58 (2001).

    Article  Google Scholar 

  3. Badger, M. R. et al. The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can. J. Bot. 76, 1052–1071 (1998).

    CAS  Google Scholar 

  4. Giordano, M., Beardall, J. & Raven, J. A. CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 56, 99–131 (2005).

    Article  CAS  Google Scholar 

  5. Reinfelder, J. R. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu. Rev. Mar. Sci. 3, 291–315 (2011).

    Article  Google Scholar 

  6. Berner, R. A. The long-term carbon cycle, fossil fuels and atmospheric composition. Nature 426, 323–326 (2003).

    Article  CAS  Google Scholar 

  7. Sabine, C. L. et al. The oceanic sink for anthropogenic CO2 . Science 305, 367–371 (2004).

    Article  CAS  Google Scholar 

  8. Le Quéré, C. et al. The global carbon budget 1959–2011. Earth Syst. Sci. Data Discuss. 5, 165–185 (2012).

    Article  Google Scholar 

  9. Caldeira, K. & Wickett, M. Anthropogenic carbon and ocean pH. Nature 425, 365 (2003).

    Article  CAS  Google Scholar 

  10. Hopkinson, B. M., Dupont, C. L., Allen, A. E. & Morel, F. M. M. Efficiency of the CO2-concentrating mechanism of diatoms. Proc. Natl Acad. Sci. USA 108, 3830–3837 (2011).

    Article  CAS  Google Scholar 

  11. Moore, J. K., Doney, S. C., Glover, D. M. & Fung, I. Y. Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep-Sea Res. II 49, 463–507 (2002).

    Article  CAS  Google Scholar 

  12. Hennon, G. M. M., Quay, P., Morales, R. L., Swanson, L. M. & Armbrust, E. V. Acclimation conditions modify physiological response of the diatom Thalassiosira pseudonana to elevated CO2 concentrations in a nitrate-limited chemostat. J. Phycol. 253, 243–253 (2014).

    Article  Google Scholar 

  13. Feely, R. A., Sabine, C. L., Hernandez-Ayon, J. M., Ianson, D. & Hales, B. Evidence for upwelling of corrosive ‘acidified’ water onto the continental shelf. Science 320, 1490–1492 (2008).

    Article  CAS  Google Scholar 

  14. Ciais, P. et al. in Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) 465–570 (IPCC, Cambridge Univ. Press, 2013).

    Google Scholar 

  15. Mock, T. et al. Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses. Proc. Natl Acad. Sci. USA 105, 1579–1584 (2008).

    Article  CAS  Google Scholar 

  16. Carvalho, R. N., Bopp, S. K. & Lettieri, T. Transcriptomics responses in marine diatom Thalassiosira pseudonana exposed to the polycyclic aromatic hydrocarbon benzo[a]pyrene. PLoS ONE 6, e26985 (2011).

    Article  CAS  Google Scholar 

  17. Thamatrakoln, K., Korenovska, O., Niheu, A. K. & Bidle, K. D. Whole-genome expression analysis reveals a role for death-related genes in stress acclimation of the diatom Thalassiosira pseudonana. Environ. Microbiol. 14, 67–81 (2012).

    Article  CAS  Google Scholar 

  18. Shrestha, R. P. et al. Whole transcriptome analysis of the silicon response of the diatom Thalassiosira pseudonana. BMC Genomics 13, 499 (2012).

    Article  CAS  Google Scholar 

  19. Ashworth, J. et al. Genome-wide diel growth state transitions in the diatom Thalassiosira pseudonana. Proc. Natl Acad. Sci. USA 110, 7518–7523 (2013).

    Article  CAS  Google Scholar 

  20. Bender, S. J., Durkin, C. A., Berthiaume, C. T., Morales, R. L. & Armbrust, E. V. Transcriptional responses of three model diatoms to nitrate limitation of growth. Front. Mar. Sci. 1, 3 (2014).

    Article  Google Scholar 

  21. Samukawa, M., Shen, C., Hopkinson, B. M. & Matsuda, Y. Localization of putative carbonic anhydrases in the marine diatom, Thalassiosira pseudonana. Photosynth. Res. 121, 235–249 (2014).

    Article  CAS  Google Scholar 

  22. Xu, Y., Feng, L., Jeffrey, P. D., Shi, Y. & Morel, F. M. M. Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452, 56–61 (2008).

    Article  CAS  Google Scholar 

  23. Ohno, N. et al. CO2-cAMP-responsive cis-elements targeted by a transcription factor with CREB/ATF-like basic zipper domain in the marine diatom Phaeodactylum tricornutum. Plant Physiol. 158, 499–513 (2012).

    Article  CAS  Google Scholar 

  24. Rayko, E., Maumus, F., Maheswari, U., Jabbari, K. & Bowler, C. Transcription factor families inferred from genome sequences of photosynthetic stramenopiles. New Phytol. 188, 52–66 (2010).

    Article  CAS  Google Scholar 

  25. Krishna, S., Andersson, A. M. C., Semsey, S. & Sneppen, K. Structure and function of negative feedback loops at the interface of genetic and metabolic networks. Nucleic Acids Res. 34, 2455–2462 (2006).

    Article  CAS  Google Scholar 

  26. Matsuda, Y., Nakajima, K. & Tachibana, M. Recent progresses on the genetic basis of the regulation of CO2 acquisition systems in response to CO2 concentration. Photosynth. Res. 109, 191–203 (2011).

    Article  CAS  Google Scholar 

  27. Hammer, A., Hodgson, D. R. W. & Cann, M. J. Regulation of prokaryotic adenylyl cyclases by CO2 . Biochem. J. 396, 215–218 (2006).

    Article  CAS  Google Scholar 

  28. Dickson, V. K., Pedi, L. & Long, S. B. Structure and insights into the function of a Ca2+-activated Cl channel. Nature 516, 213–218 (2014).

    Article  CAS  Google Scholar 

  29. Qu, Z. & Hartzell, H. Bestrophin Cl channels are highly permeable to HCO3. Am. J. Cell Physiol. 294, 1371–1377 (2008).

    Article  Google Scholar 

  30. Nakajima, K., Tanaka, A. & Matsuda, Y. SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater. Proc. Natl Acad. Sci. USA 110, 1767–1772 (2013).

    Article  CAS  Google Scholar 

  31. Lewis, E. & Wallace, D. Program Developed for CO2 System Calculations (Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, 1998); http://cdiac.ornl.gov/oceans/co2rprt.html

    Book  Google Scholar 

  32. Harada, H., Nakajima, K., Sakaue, K. & Matsuda, Y. CO2 sensing at ocean surface mediated by cAMP in a marine diatom. Plant Physiol. 142, 1318–1328 (2006).

    Article  CAS  Google Scholar 

  33. Robinson, M. D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25 (2010).

    Article  Google Scholar 

  34. Mullner, D. Dastcluster: Fast hierarchical, agglomerative clustering routines for R and Python. J. Stat. Softw. 53, 1–18 (2013).

    Article  Google Scholar 

  35. Reiss, D. J., Baliga, N. S. & Bonneau, R. Integrated biclustering of heterogeneous genome-wide datasets for the inference of global regulatory networks. BMC Bioinform. 7, 280 (2006).

    Article  Google Scholar 

  36. Bailey, T. & Elkan, C. Fitting a Mixture Model by Expectation Maximization to Discover Motifs in Biopolymers (Univ. California, 1994); http://biofactory.org/sites/default/files/presentations/motif.pdf

    Google Scholar 

  37. Gupta, S., Stamatoyannopoulos, J. A., Bailey, T. L. & Noble, W. S. Quantifying similarity between motifs. Genome Biol. 8, R24 (2007).

    Article  Google Scholar 

  38. Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7 (2011).

    Article  CAS  Google Scholar 

  39. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

    Article  CAS  Google Scholar 

  40. Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. & Barton, G. J. Jalview Version 2-A multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009).

    Article  CAS  Google Scholar 

  41. Crawfurd, K. J., Raven, J. A., Wheeler, G. L., Baxter, E. J. & Joint, I. The response of Thalassiosira pseudonana to long-term exposure to increased CO2 and decreased pH. PLoS ONE 6, 1–9 (2011).

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

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.

Corresponding authors

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

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate2683

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing