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.

  • Article
  • Published:

Acidification diminishes diatom silica production in the Southern Ocean

Abstract

Diatoms, large bloom-forming marine microorganisms, build frustules out of silicate, which ballasts the cells and aids their export to the deep ocean. This unique physiology forges an important link between the marine silicon and carbon cycles. However, the effect of ocean acidification on the silicification of diatoms is unclear. Here we show that diatom silicification strongly diminishes with increased acidity in a natural Antarctic community. Analyses of single cells from within the community reveal that the effect of reduced pH on silicification differs among taxa, with several species having significantly reduced silica incorporation at CO2 levels equivalent to those projected for 2100. These findings suggest that, before the end of this century, ocean acidification may influence the carbon and silicon cycle by both altering the composition of the diatom assemblages and reducing cell ballasting, which will probably alter vertical flux of these elements to the deep ocean.

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

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Silicification and diatom community composition on day 12.
Fig. 2: Single-celled silicification with [H+].
Fig. 3: Silicification as a function of growth, cell surface area and abundance.
Fig. 4: Diatom response to [H+].

Similar content being viewed by others

Data availability

The data that support these findings are available from the Australian Antarctic Data Centre (https://doi.org/10.26179/5c3e745a9b071)69.

References

  1. Khatiwala, S., Primeau, F. & Hall, T. Reconstruction of the history of anthropogenic CO2 concentrations in the ocean. Nature 462, 346–349 (2009).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).

    Article  CAS  Google Scholar 

  4. Riebesell, U. et al. Reduced calcification in marine plankton in response to increased atmospheric CO2. Nature 407, 634–637 (2000).

    Google Scholar 

  5. Fabry, V. J. Marine calcifiers in a high-CO2 ocean. Science 320, 1020–1022 (2008).

    Article  CAS  Google Scholar 

  6. Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. Ocean acidification: the other CO2 problem. Annu. Rev. Mar. Sci. 1, 169–192 (2009).

    Article  Google Scholar 

  7. Levitan, I. et al. Elevated CO2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob. Change Biol. 13, 1–8 (2007).

    Article  Google Scholar 

  8. Tortell, P. et al. CO2 sensitivity of Southern Ocean phytoplankton. Geophys. Res. Lett. 35, L04605 (2008).

    Article  Google Scholar 

  9. Wu, Y., Gao, K. & Riebesell, U. CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7, 2915–2923 (2010).

    Article  CAS  Google Scholar 

  10. Schaum, E., Rost, B., Millar, A. J. & Collins, S. Variation in plastic responses of a globally distributed picoplankton species to ocean acidification. Nat. Clim. Change 3, 298–302 (2013).

    Article  CAS  Google Scholar 

  11. Wu, Y., Campbell, D. A., Irwin, A. J., Suggett, D. J. & Finkel, Z. V. Ocean acidification enhances the growth rate of larger diatoms. Limnol. Oceanogr. 59, 1027–1034 (2014).

    Article  CAS  Google Scholar 

  12. Dutkiewicz, S. et al. Impact of ocean acidification on the structure of future phytoplankton communities. Nat. Clim. Change 5, 1002–1006 (2015).

    Article  CAS  Google Scholar 

  13. Mackey, K. R. M., Morris, J. J., Morel, F. M. M. & Kranz, S. A. Response of photosynthesis to ocean acidification. Oceanography 28, 74–91 (2015).

    Article  Google Scholar 

  14. Riebesell, U., Gattuso, J.-P., Thingstad, T. F. & Meddleburg, J. J. Arctic ocean acidification: pelagic ecosystem and biogeochemical responses during a mesocosm study. Biogeosciences 10, 5619–5626 (2013).

    Article  Google Scholar 

  15. Sala, M. M. et al. Contrasting effects of ocean acidification on the microbial food web under different trophic conditions. ICES J. Mar. Sci. 73, 670–679 (2015).

    Article  Google Scholar 

  16. Burkhardt, S., Riebesell, U. & Zondervan, I. Effects of growth rate, CO2 concentration, and cell size on the stable carbon isotope fractionation in marine phytoplankton. Geochim. Cosmochim. Acta 63, 3729–3741 (1999).

    Article  CAS  Google Scholar 

  17. Tortell, P. D., DiTullio, G., Sigman, D. M. & Morel, F. M. M. CO2 effects on taxonomic composition and nutrient utilization in an equatorial Pacific phytoplankton assemblage. Mar. Ecol. Prog. Ser. 236, 37–43 (2002).

    Article  Google Scholar 

  18. 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 

  19. Martin-Jezequel, V., Hildebrand, M. & Brzezinski, M. A. Silicon metabolism in diatoms: implications for growth. J. Phycol. 36, 821–840 (2000).

    Article  CAS  Google Scholar 

  20. Smetacek, V. Diatoms and the ocean carbon cycle. Protist 150, 25–32 (1999).

    Article  CAS  Google Scholar 

  21. Hamm, C. E. et al. Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421, 841–843 (2003).

    Article  CAS  Google Scholar 

  22. Buesseler, K. O. The decoupling of production and particle export in the surface ocean. Glob. Biogeochem. Cycles 12, 297–310 (1998).

    Article  CAS  Google Scholar 

  23. Dugdale, R. C. & Wilkerson, F. P. Silicate regulation of new production in the equatorial Pacific upwelling. Nature 391, 270–273 (1998).

    Article  CAS  Google Scholar 

  24. Agusti, S. et al. Ubiquitous healthy diatoms in the deep sea confirm deep carbon injection by the biological pump. Nat. Commun. 6, 7608 (2015).

    Article  CAS  Google Scholar 

  25. Tréguer, P. et al. Influence of diatom diversity on the ocean biological carbon pump. Nat. Geosci. 11, 27–37 (2018).

    Article  Google Scholar 

  26. Baines, S. B., Twining, B. S., Brzezinski, M. A., Nelson, D. M. & Fisher, N. S. Causes and biogeochemical implications of regional differences in silicification of marine diatoms. Glob. Biogeochem. Cycles 24, GB4031 (2010).

    Article  Google Scholar 

  27. Bach, L. T. et al. Effects of elevated CO2 on a natural diatom community in the subtropical NE Atlantic. Front. Mar. Sci. https://doi.org/10.3389/fmars.2019.00075 (2019).

  28. Tatters, A. O. et al. Short- and long-term conditioning of a temperate marine diatom community to acidification and warming. Phil. Trans. R. Soc. B 368, 20120437 (2013).

    Article  Google Scholar 

  29. Davidson, A. T. et al. Enhanced CO2 concentrations change the structure of Antarctic marine microbial communities. Mar. Ecol. Prog. Ser. 552, 93–113 (2016).

    Article  CAS  Google Scholar 

  30. Schulz, K. G. et al. Phytoplankton blooms at increasing levels of atmospheric carbon dioxide: experimental evidence for negative effects on prymnesiophytes and positive on small picoeukaryotes. Front. Mar. Sci. 4, 64 (2017).

    Article  Google Scholar 

  31. Hancock, A. M. et al. Ocean acidification changes the structure of an Antarctic coastal protistan community. Biogeosci. Discuss. 15, 2393–2410 (2018).

    Article  CAS  Google Scholar 

  32. Riebesell, U. & Tortell, P. D. in Ocean Acidification (eds Gattuso, J.-P. & Hansson, L.) 99–121 (Oxford Univ. Press, 2011).

  33. Deppeler, S. et al. Ocean acidification of a coastal Antarctic marine microbial community reveals a critical threshold for CO2 tolerance in phytoplankton productivity. Biogeosciences 15, 209 (2018).

    Article  CAS  Google Scholar 

  34. Westwood, K. et al. Ocean acidification impacts primary and bacterial production in Antarctic coastal waters during austral summer. J. Exp. Mar. Biol. Ecol. 498, 46–60 (2018).

    Article  CAS  Google Scholar 

  35. Milligan, A. J. & Morel, F. M. A proton buffering role for silica in diatoms. Science 297, 1848–1850 (2002).

    Article  CAS  Google Scholar 

  36. Hervé, V. et al. Multiparametric analyses reveal the pH-dependence of silicon biomineralization in diatoms. PLoS ONE 7, e46722 (2012).

    Article  Google Scholar 

  37. Milligan, A. J., Varela, D. E., Brzezinski, M. A. & Morel, F. M. M. Dynamics of silicon metabolism and silicon isotopic discrimination in a marine diatom as a function of \(p_{\mathrm {CO}_2}\). Limnol. Oceanogr. 49, 322–329 (2004).

    Article  CAS  Google Scholar 

  38. Sugie, K. & Yoshimura, T. Effects of high CO2 levels on the ecophysiology of the diatom Thalassiosira weissflogii differ depending on the iron nutritional status. ICES J. Mar. Sci. 73, 680–692 (2016).

    Article  Google Scholar 

  39. Riebesell, U. & Gattuso, J.-P. Lessons learned from ocean acidification research. Nat. Clim. Change 5, 12–14 (2015).

    Article  CAS  Google Scholar 

  40. Havenhand, J., Dupont, S. & Quinn, G. P. in Guide to Best Practices for Ocean Acidification Research and Data Reporting (eds Riebesell, U. et al.) 67–80 (Publications Office of the European Union, 2010).

  41. Roden, N. P., Shadwick, E. H., Tilbrook, B. & Trull, T. W. Annual cycle of carbonate chemistry and decadal change in coastal Prydz Bay, East Antarctica. Mar. Chem. 155, 135–147 (2013).

    Article  CAS  Google Scholar 

  42. Dutkiewicz, S., Scott, J. R. & Follows, M. J. Winners and losers: ecological and biogeochemical changes in a warming ocean. Glob. Biogeochem. Cycles 27, 463–477 (2013).

    Article  CAS  Google Scholar 

  43. Miklasz, K. A. & Denny, M. W. Diatom sinking speeds: improved predictions and insight from a modified Stoke’s law. Limnol. Oceanogr. 55, 2513–2525 (2010).

    Article  Google Scholar 

  44. McNair, H. M., Brzezinski, M. A., Till, C. P. & Krause, J. W. Taxon‐specific contributions to silica production in natural diatom assemblages. Limnol. Oceanogr. 63, 1056–1075 (2018).

    Article  CAS  Google Scholar 

  45. Shi, D., Xu, Y., Hopkinson, B. M. & Morel, F. M. M. Effect of ocean acidification on iron availability to marine phytoplankton. Science 327, 676–679 (2010).

    Article  CAS  Google Scholar 

  46. Villareal, T. A., Altabet, M. A. & Culver-Rymsza, K. Nitrogen transport by vertically migrating diatom mats in the North Pacific Ocean. Nature 363, 709–712 (1993).

    Article  CAS  Google Scholar 

  47. Durkin, C. A. et al. Frustule-related gene transcription and the influence of diatom community composition on silica precipitation in an iron-limited environment. Limnol. Oceanogr. 57, 1619–1633 (2012).

    Article  CAS  Google Scholar 

  48. McNeil, B. & Matear, R. Southern Ocean acidification: a tipping point at 450-ppm atmospheric CO2. Proc. Natl Acad. Sci. USA 105, 18860–18864 (2008).

    Article  CAS  Google Scholar 

  49. Assmy, P. et al. Thick-shelled, grazer-protected diatoms decouple ocean carbon and silicon cycles in the iron-limited Antarctic Circumpolar Current. Proc. Natl Acad. Sci. USA 110, 20633–20638 (2013).

    Article  CAS  Google Scholar 

  50. Kang, S. & Fryxell, G. Fragilariopsis cylindrus (Grunow) Krieger: the most abundant diatom in water column assemblages of Antarctic marginal ice-edge zones. Polar Biol. 12, 609–627 (1992).

    Article  Google Scholar 

  51. Matsumoto, K., Sarmiento, J. L. & Brzezinski, M. A. Silicic acid leakage from the Southern Ocean: a possible explanation for glacial atmospheric \(p_{\mathrm {CO}_2}\). Glob. Biogeochem. Cycles 16, 5–1 (2002).

    Article  Google Scholar 

  52. Boyd, P. W. Physiology and iron modulate diverse responses of diatoms to a warming Southern Ocean. Nat. Clim. Change 9, 148–152 (2019).

    Article  CAS  Google Scholar 

  53. Boyd, P. W., Lennartz, S. T., Glover, D. M. & Doney, S. C. Biological ramifications of climate-change-mediated oceanic multi-stressors. Nat. Clim. Change 5, 71–79 (2014).

    Article  Google Scholar 

  54. Petrou, K. et al. Southern Ocean phytoplankton physiology in a changing climate. J. Plant Physiol. 203, 135–150 (2016).

    Article  CAS  Google Scholar 

  55. Boyd, P. W. et al. Physiological responses of a Southern Ocean diatom to complex future ocean conditions. Nat. Clim. Change 6, 207–213 (2016).

    Article  Google Scholar 

  56. Deppeler, S. L. & Davidson, A. T. Southern Ocean phytoplankton in a changing climate. Front. Mar. Sci. 4, 40 (2017).

    Article  Google Scholar 

  57. Dickson, A. G., Sabine, C. L. & Christian, J. R. Guide to Best Practices for Ocean CO 2 Measurements (PICES Special Publication, North Pacific Marine Science Organization, 2007).

  58. Dickson, A. G. Standards for ocean measurements. Oceanography 23, 34–47 (2010).

    Article  Google Scholar 

  59. Leblanc, K. & Hutchins, D. A. New applications of a biogenic silica deposition fluorophore in the study of oceanic diatoms. Limnol. Oceanogr. Methods 3, 462–476 (2005).

    Article  CAS  Google Scholar 

  60. Shimizu, K., Del Amo, Y., Brzezinski, M. A., Stucky, G. D. & Morse, D. E. A novel fluorescent silica tracer for biological silicification studies. Chem. Biol. 8, 1051–1060 (2001).

    Article  CAS  Google Scholar 

  61. McNair, H. M., Brzezinski, M. A. & Krause, J. W. Quantifying diatom silicification with the fluorescent dye, PDMPO. Limnol. Oceanogr. Methods 13, 587–599 (2015).

    Article  CAS  Google Scholar 

  62. Baker, K. G. et al. Thermal performance curves of functional traits aid understanding of thermally induced changes in diatom-mediated biogeochemical fluxes. Front. Mar. Sci. 3, 44 (2016).

    Article  Google Scholar 

  63. Parambath, M. et al. The nature of the silicaphilic fluorescence of PDMPO. Phys. Chem. Chem. Phys. 18, 5938–5948 (2016).

    Article  CAS  Google Scholar 

  64. Strickland, J. D. H. & Parsons, T. R. A Practical Handbook of Seawater Analysis (Fisheries Research Board of Canada, 1968).

  65. Nelson, D. M. et al. Particulate matter and nutrient distributions in the ice-edge zone of the Weddell Sea: relationship to hydrography during late summer. Deep Sea Res. Pt A 36, 191–209 (1989).

    Article  CAS  Google Scholar 

  66. Schneider, C. A., Raspnad, W. S. & Eliceiri, K. W. NIH image to imageJ: 25 years of image analysis. Nat. Methods 9, 671–679 (2012).

    Article  CAS  Google Scholar 

  67. Kreyling, J. et al. To replicate, or not to replicate—that is the question: how to tackle nonlinear responses in ecological experiments. Ecol. Lett. 21, 1629–1638 (2018).

    Article  Google Scholar 

  68. Cottingham, K. L., Lennon, J. T. & Brown, B. L. Knowing when to draw the line: designing more informative ecological experiments. Front. Ecol. Environ. 3, 145–152 (2005).

    Article  Google Scholar 

  69. Petrou, K. Antarctic Diatom Silicification Diminishes Under Ocean Acidification (Australian Antarctic Data Centre, 2019); https://doi.org/10.26179/5c3e745a9b071.

Download references

Acknowledgements

The work was supported by Australian Antarctic Science project AAS 4026 from the Australian Antarctic Division (AAD); samples were imported under permit no. IP13019928. We are grateful to AAD technical support for their assistance and support in designing and equipping the mesocosm facility and to the Davis Station expeditioners in the summer of 2014/2015.

Author information

Authors and Affiliations

Authors

Contributions

K.P. conceptualized the study. K.P., K.G.B., D.A.N., A.M.H., K.G.S. and A.T.D. carried out the investigations. K.P. and K.G.B. developed the methodology. K.P. and D.A.N. conducted the formal analysis and visualization. K.P. prepared the original draft. K.P., K.G.B., D.A.N., A.M.H., K.G.S. and A.T.D. reviewed and edited it. K.P. and A.T.D. obtained the funding and provided resources.

Corresponding author

Correspondence to Katherina Petrou.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information: Nature Climate Change thanks Phillipp Assmy, Paul Treguer and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–5, Tables 1–6 and references.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Petrou, K., Baker, K.G., Nielsen, D.A. et al. Acidification diminishes diatom silica production in the Southern Ocean. Nat. Clim. Chang. 9, 781–786 (2019). https://doi.org/10.1038/s41558-019-0557-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41558-019-0557-y

This article is cited by

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

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