Ocean acidification is changing the productivity and composition of phytoplankton communities at the base of the aquatic food web. Now a study shows that acidification impairs the swimming ability of flagellated microalgae, suggesting that their capacity to survive is threatened in a high CO2 world.
Phytoplankton play a key role in aquatic ecosystems: they are responsible for about half of global carbon fixation, they form the base of the aquatic food web and they drive biogeochemical cycles1. For these microscopic phytoplankton, the ability to move can be a key trait for surviving in a vast water mass. Swimming allows phytoplankton to move towards favourable and away from harmful conditions, thereby increasing their fitness2,3. Many phytoplankton species can swim, and most of them rely on flagellae to do so. Anthropogenic CO2 emissions have increased dissolved CO2 concentrations, thereby lowering the pH of the surface ocean: a process that is commonly known as ocean acidification4. Ocean acidification is changing biogeochemical cycles, productivity and biodiversity on a global scale4, and can impact key traits of important marine organisms, such as the swimming ability of phytoplankton. Writing in Nature Climate Change, Yitao Wang and co-authors5 show that CO2-induced acidification inhibits the motility of flagellated phytoplankton (Fig. 1), which could lead to dramatic shifts in phytoplankton community composition.
Predicting how phytoplankton communities will change in response to ocean acidification is difficult yet important, because changes in community composition can lead to changes in ecosystem functioning and biogeochemical cycling4,6. Phytoplankton species composition naturally varies over time and space, and is governed by a myriad of factors (for example, nutrient availability, temperature, predation pressure and pollution), which makes extrapolating results obtained from a single lab strain or even a single community towards global patterns almost impossible. A first, simplifying step towards predicting how ocean acidification may change phytoplankton assemblages is to investigate how acidification affects important functional traits. One of the traits that has been studied extensively in various marine species in response to ocean acidification is the ability to calcify. Ocean acidification lowers the availability of calcium carbonate, a key resource for calcifying organisms that use calcium carbonate to build structural and protective shells, scales and skeletons7. Ocean acidification decreases calcification rates in many calcifying phytoplankton8, which, in turn, affects their survival in a high CO2 world. Another key trait of many phytoplankton species is the ability to swim. Swimming enhances survival because it allows phytoplankton to move towards optimal light intensities at the water surface or towards high nutrient concentrations deep in the water column2,9. Swimming also gives species the opportunity to actively avoid damaging high light intensities and escape predators3,9.
The flagellar movement that provides motility is driven by pH gradients, and intracellular pH gradients can be affected by a decrease in external pH10,11. It is therefore likely that flagellar movement is sensitive to pH. Short exposure to changes in pH have indeed been shown to affect the motility and swimming behaviour of flagellated phytoplankton12. An important aspect to consider when studying microorganisms with generation times of hours to days, is that they can evolve in response to changing conditions at timescales of weeks to months. Therefore, to be able to assess the impact of ocean acidification on phytoplankton communities, it is imperative to take evolution over longer timescales into account, to find out which traits will evolve and how these traits will change13. To date, the impact of CO2-induced acidification on algal motility, particularly after long-term acclimation, has not yet been investigated.
To fill this gap in knowledge, Yitao Wang and co-authors examined how CO2-induced acidification changes flagellar motility, and which molecular mechanisms underpin these changes5. Three typical flagellated phytoplankton from different taxa representing freshwater, estuarine and Antarctic marine habitats were grown at a range of atmospheric CO2 concentrations for five years. Long-term acclimation to elevated CO2 concentrations reduced both the instantaneous and average velocity of all three flagellated species under laboratory and field conditions, indicating that organisms will require more time to reach optimal conditions in the water column and will be worse at escaping predators. Long-term acclimation also decreased the ability to move towards favourable, and away from damaging light intensities. Furthermore, CO2-induced acidification caused more individuals to lose their flagella and slowed down restoration of motility. All of these factors will likely decrease growth and survival of flagellated phytoplankton.
To identify which molecular mechanisms underpin the observed reduction in motility, the authors studied the gene expression of flagella bending genes in the Antarctic species Microglena. The transcriptome data showed that long-term acclimation to CO2-induced acidification resulted in downregulation of genes that promoted flagellar motion, while genes that suppress flagellar movement and genes that induce deflagellation were upregulated. Despite the fact that flagellar movement relies on pH gradients10, the impact of pH on the expression of flagellar bending genes had thus far only been studied in the bacterium Escherischia coli14. Interestingly, in contrast to the findings of Wang et al.5, flagellar bending genes in E. coli were repressed after short-time exposure to elevated pH.
The work of Wang and co-authors is an outstanding first step towards understanding how a key trait, such as the ability to swim, will change in response to increasing levels of CO2. The results strongly suggest that CO2-induced acidification will disadvantage flagellated phytoplankton. However, before these results can be extrapolated to the global scale or even the ecosystem level, many questions remain. One key question is how different aspects of climate change will interact to impact flagellated phytoplankton. The authors provide an example by pointing out that warmer Antarctic waters will melt sea ice, thereby exposing Microglena sp. to much higher light intensities. This will increase the distance that cells have to travel to find their optimal light intensity5, which will be an additional challenge for organisms whose swimming ability is already impaired by CO2-induced acidification. Another key question that has yet to be addressed is how flagellated phytoplankton will adapt to CO2-induced acidification in a complex three-dimensional natural environment with selective pressures that are very different from those in a laboratory flask. In a complex environment, the selective pressures that favour swimming may be much stronger. The fact that flagellated species comprise an important component of phytoplankton communities in acidic environments15 provides hopeful clues that flagellated phytoplankton may be able to adapt to, and survive at, elevated CO2 concentrations.
Falkowski, P. G., Fenchel, T. & Delong, E. F. Science 320, 1034–1039 (2008).
Hall, N. S. & Paerl, H. W. Mar. Ecol. Prog. Ser. 425, 7–21 (2011).
Waisbord, N. & Guasto, J. S. Nat. Phys. 14, 1157–1162 (2018).
Gattuso, J. P. et al. Science 349, aac4722 (2015).
Wang, Y. et al. Nat. Clim. Change https://doi.org/10.1038/s41558-020-0776-2 (2020).
Eggers, S. L. et al. Glob. Change Biol. 20, 713–723 (2014).
Orr, J. C. et al. Nature 437, 681–686 (2005).
Hofmann, G. E. et al. Annu. Rev. Ecol. Evol. Syst. 41, 127–147 (2010).
Sineshchekov, O. A., Jung, K. H. & Spudich, J. L. Proc. Natl Acad. Sci. USA 99, 8689–8694 (2002).
Blair, D. F. FEBS Lett. 545, 86–95 (2003).
Suffrian, K., Schulz, K. G., Gutowska, M. A., Riebesell, U. & Bleich, M. New Phytol. 190, 595–608 (2011).
Kim, H., Spivack, A. J. & Menden-Deuer, S. Harmful Algae 26, 1–11 (2013).
Collins, S., Boyd, P. W. & Doblin, M. A. Annu. Rev. Mar. Sci. 12, 181–208 (2019).
Maurer, L. M., Yohannes, E., Bondurant, S. S., Radmacher, M. & Slonczewski, J. L. J. Bacteriol. 187, 304–319 (2005).
Nixdorf, B., Mischke, U. & Leβmann, D. Hydrobiologia 369, 315–327 (1998).
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Verspagen, J.M.H. Acidification slows algal movement. Nat. Clim. Chang. 10, 497–498 (2020). https://doi.org/10.1038/s41558-020-0799-8