Phytoplankton mortality in a changing thermal seascape.

Phaeodactylum tricornutum cell death global warming mortality rate thermal acclimation thermal response tipping points

Journal

Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746

Informations de publication

Date de publication:
10 2021
Historique:
received: 21 04 2021
accepted: 13 06 2021
pubmed: 27 6 2021
medline: 21 10 2021
entrez: 26 6 2021
Statut: ppublish

Résumé

Predicting spatiotemporal distributions of phytoplankton biomass and community composition heavily relies on experimental studies that document how environmental conditions influence population growth rates. In unicellular phytoplankton, the net population growth rate is the difference between the cell division rate and the death rate. Along with predation and disease, phytoplankton mortality arises from abiotic stress. Although the effect of temperature on the net population growth rate is well understood, studies examining thermally induced death rates in phytoplankton are scarce. We investigated how cell division and death rates of the diatom Phaeodactylum tricornutum varied within its thermal tolerance limits (thermal niche), and at temperatures just above its upper thermal tolerance limit. We show that death rates were largely independent of temperature when P. tricornutum was grown within its thermal niche, but increased significantly at temperatures that approached or exceeded its upper thermal tolerance limit. Furthermore, the sensitivity of mortality increased with the duration of exposure to heat stress and was affected by the pre-acclimation temperature. Heat waves can be expected to significantly affect phytoplankton mortality episodically. The increasing frequency of heat waves accompanying global warming can be expected to drive changes in phytoplankton community structure due to interspecific variability of thermal niches with potential implications for food web dynamics and biogeochemical cycles.

Identifiants

pubmed: 34174004
doi: 10.1111/gcb.15772
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

5253-5261

Informations de copyright

© 2021 The Authors. Global Change Biology published by John Wiley & Sons Ltd.

Références

Agustí, S., & Duarte, C. M. (2000). Experimental induction of a large phytoplankton bloom in Antarctic coastal waters. Marine Ecology Progress Series, 206, 73-85. https://doi.org/10.3354/meps206073
Agustí, S., Satta, M. P., Mura, M. P., & Benavent, E. (1998). Dissolved esterase activity as a tracer of phytoplankton lysis: Evidence of high phytoplankton lysis rates in the northwestern Mediterranean. Limnology and Oceanography, 43(8), 1836-1849. https://doi.org/10.4319/lo.1998.43.8.1836
Angilletta, Jr., M. J., Wilson, R. S., Navas, C. A., & James, R. S. (2003). Tradeoffs and the evolution of thermal reaction norms. Trends in Ecology & Evolution, 18, 234-240. https://doi.org/10.1016/S0169-5347(03)00087-9
Baker, K. G., Radford, D. T., Evenhuis, C., Kuzhiumparam, U., Ralph, P. J., & Doblin, M. A. (2018). Thermal niche evolution of functional traits in a tropical marine phototroph. Journal of Phycology, 54, 799-810. https://doi.org/10.1111/jpy.12759
Berges, J. A., & Falkowski, P. G. (1998). Physiological stress and cell death in marine phytoplankton: Induction of proteases in response to nitrogen or light limitation. Limnology and Oceanography, 43, 129-135. https://doi.org/10.4319/lo.1998.43.1.0129
Berges, J. A., Franklin, D. J., & Harrison, P. J. (2001). Evolution of an artificial seawater medium: Improvements in enriched seawater, artificial water over the last two decades. Journal of Phycology, 37, 1138-1145. https://doi.org/10.1046/j.1529-8817.2001.01052.x
Bouchard, J. N., & Yamasaki, H. (2008). Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: A possible linkage between nitric oxide and the coral bleaching phenomenon. Plant and Cell Physiology, 49, 641-652. https://doi.org/10.1093/pcp/pcn037
Brussaard, C. P., Noordeloos, A. A., & Riegman, R. (1997). Autolysis kinetics of the marine diatom Ditylum brightwellii (Bacillariophyceae) under nitrogen and phosphorus limitation and starvation. Journal of Phycology, 33(6), 980-987. https://doi.org/10.1111/j.0022-3646.1997.00980.x
Buerger, P., Alvarez-Roa, C., Coppin, C. W., Pearce, S. L., Chakravarti, L. J., Oakeshott, J. G., Edwards, O. R., & Van Oppen, M. J. H. (2020). Heat-evolved microalgal symbionts increase coral bleaching tolerance. Science Advances, 6, 1. https://doi.org/10.1126/sciadv.aba2498
Dunn, S. R., Thomason, J. C., Le Tissier, M. D. A., & Bythell, J. C. (2004). Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell Death & Differentiation, 11, 1213-1222. https://doi.org/10.1038/sj.cdd.4401484
Follows, M. J., Dutkiewicz, S., Grant, S., & Chisholm, S. W. (2007). Emergent biogeography of microbial communities in a model ocean. Science, 315, 1843-1846. https://doi.org/10.1126/science.1138544
Franklin, D. J., Hoegh-Guldberg, O., Jones, R. J., & Berges, J. A. (2004). Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Marine Ecology Progress Series, 272, 117-130. https://doi.org/10.3354/meps272117
Frölicher, T. L., Fischer, E. M., & Gruber, N. (2018). Marine heatwaves under global warming. Nature, 560, 360-364. https://doi.org/10.1038/s41586-018-0383-9
Gibor, A. (1956). The culture of brine algae. The Biological Bulletin, 111, 223-229. https://doi.org/10.2307/1539013
Guillard, R. R., & Ryther, J. H. (1962). Studies of marine planktonic diatoms. I. Cyclothella nana Hustedt and Detonula confervacea Gran. Canadian Journal of Microbiology, 8(2), 229-239. https://doi.org/10.1139/m62-029
Harrison, P. J., Waters, R. E., & Taylor, F. J. R. (1980). A broad spectrum artificial sea water medium for coastal and open ocean phytoplankton. Journal of Phycology, 16, 28-35. https://doi.org/10.1111/j.0022-3646.1980.00028.x
Jiménez, C., Capasso, J. M., Edelstein, C. L., Rivard, C. J., Lucia, S., Breusegem, S., Berl, T., & Segovia, M. (2009). Different ways to die: Cell death modes of the unicellular chlorophyte Dunaliella viridis exposed to various environmental stresses are mediated by the caspase-like activity DEVDase. Journal of Experimental Botany, 60, 815-828. https://doi.org/10.1093/jxb/ern330
Keller, M. D., Selvin, R. C., Claus, W., & Guillard, R. R. L. (1987). Media for the culture of oceanic ultraphytoplankton. Journal of Phycology, 23, 633-638. https://doi.org/10.1111/j.1529-8817.1987.tb04217.x
Low-Décarie, E., Boatman, T. G., Bennett, N., Passfield, W., Gavalás-Olea, A., Siegel, P., & Geider, R. J. (2017). Predictions of response to temperature are contingent on model choice and data quality. Ecology and Evolution, 7, 10467-10481. https://doi.org/10.1002/ece3.3576
Luhring, T. M., & DeLong, J. P. (2017). Scaling from metabolism to population growth rate to understand how acclimation temperature alters thermal performance. Integrative and Comparative Biology, 57, 103-111. https://doi.org/10.1093/icb/icx041
Marbà, N., Duarte, C. M., & Agustí, S. (2007). Allometric scaling of plant life history. Proceedings of the National Academy of Sciences, 104(40), 15777-15780. https://doi.org/10.1073/pnas.0703476104
McCoy, M. W., & Gillooly, J. F. (2008). Predicting natural mortality rates of plants and animals. Ecology Letters, 11, 710-716. https://doi.org/10.1111/j.1461-0248.2008.01190.x
Montagnes, D. J. S., Morgan, G., Bissinger, J. E., Atkinson, D., & Weisse, T. (2008). Short-term temperature change may impact freshwater carbon flux: A microbial perspective. Global Change Biology, 14, 2823-2838. https://doi.org/10.1111/j.1365-2486.2008.01700.x
Muggeo, V. M. R. (2015). Regression models with breakpoints/changepoints estimation. R package version 0.5-1.4.
Nguyen, H. M., Kim, M., Ralph, P. J., Marín-Guirao, L., Pernice, M., & Procaccini, G. (2020). Stress memory in seagrasses: First insight into the effects of thermal priming and the role of epigenetic modifications. Frontiers in Plant Science, 11, 494. https://doi.org/10.3389/fpls.2020.00494
Padfield, D., Yvon-Durocher, G., Buckling, A., Jennings, S., & Yvon-Durocher, G. (2016). Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton. Ecology Letters, 19, 133-142. https://doi.org/10.1111/ele.12545
Peperzak, L., & Brussaard, C. P. (2011). Flow cytometric applicability of fluorescent vitality probes on phytoplankton. Journal of Phycology, 47(3), 692-702. https://doi.org/10.1111/j.1529-8817.2011.00991.x
Remy, M., Hillebrand, H., & Flöder, S. (2017). Stability of marine phytoplankton communities facing stress related to global change: Interactive effects of heat waves and turbidity. Journal of Experimental Marine Biology and Ecology, 497, 219-229. https://doi.org/10.1016/j.jembe.2017.10.002
Rezende, E. L., Castañeda, L. E., & Santos, M. (2014). Tolerance landscapes in thermal ecology. Functional Ecology, 28, 799-809. https://doi.org/10.1111/1365-2435.12268
Ruthrof, K. X., Breshears, D. D., Fontaine, J. B., Froend, R. H., Matusick, G., Kala, J., Miller, B. P., Mitchell, P. J., Wilson, S. K., van Keulen, M., Enright, N. J., Law, D. J., Wernberg, T., & Hardy, G. E. S. J. (2018). Subcontinental heat wave triggers terrestrial and marine, multi-taxa responses. Scientific Reports, 8, 1-9. https://doi.org/10.1038/s41598-018-31236-5
Samuels, T., Rynearson, T. A., & Collins, S. (2021). Surviving heatwaves: Thermal experience predicts life and death in a Southern Ocean diatom. Frontiers in Marine Science, 8, 9. https://doi.org/10.3389/fmars.2021.600343
Schulte, P. M., Healy, T. M., & Fangue, N. A. (2011). Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integrative and Comparative Biology, 51, 691-702. https://doi.org/10.1093/icb/icr097
Serra-Maia, R., Bernard, O., Gonçalves, A., Bensalem, S., & Lopes, F. (2016). Influence of temperature on Chlorella vulgaris growth and mortality rates in a photobioreactor. Algal Research, 18, 352-359. https://doi.org/10.1016/j.algal.2016.06.016
Siegel, P., Baker, K. G., Low-Décarie, E., & Geider, R. J. (2020). High predictability of direct competition between marine diatoms under different temperatures and nutrient states. Ecology and Evolution, 10, 7276-7290. https://doi.org/10.1002/ece3.6453
Siegle, M. R., Taylor, E. B., & O'Connor, M. I. (2018). Prior heat accumulation reduces survival during subsequent experimental heat waves. Journal of Experimental Marine Biology and Ecology, 501, 109-117. https://doi.org/10.1016/j.jembe.2018.01.012
Stillman, J. H., & Tagmount, A. (2009). Seasonal and latitudinal acclimatization of cardiac transcriptome responses to thermal stress in porcelain crabs, Petrolisthes cinctipes. Molecular Ecology, 18, 4206-4226. https://doi.org/10.1111/j.1365-294X.2009.04354.x
Takahashi, S., Yoshioka-Nishimura, M., Nanba, D., & Badger, M. R. (2013). Thermal acclimation of the symbiotic alga Symbiodinium spp. alleviates photobleaching under heat stress. Plant Physiology, 161, 477-485. https://doi.org/10.1104/pp.112.207480
Thomas, M. K., Aranguren-Gassis, M., Kremer, C. T., Gould, M. R., Anderson, K., Klausmeier, C. A., & Litchman, E. (2017). Temperature-nutrient interactions exacerbate sensitivity to warming in phytoplankton. Global Change Biology, 23, 3269-3280. https://doi.org/10.1111/gcb.13641
Timmermans, K. R., Veldhuis, M. J., & Brussaard, C. P. (2007). Cell death in three marine diatom species in response to different irradiance levels, silicate, or iron concentrations. Aquatic Microbial Ecology, 46(3), 253-261. https://doi.org/10.3354/ame046253
Toms, J. D., & Lesperance, M. L. (2003). Piecewise regression: A tool for identifying ecological thresholds. Ecology, 84, 2034-2041. https://doi.org/10.1890/02-0472
Veldhuis, M., Kraay, G., & Timmermans, K. (2001). Cell death in phytoplankton: Correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth. European Journal of Phycology, 36, 167-177. https://doi.org/10.1017/S0967026201003110
Vona, V., Di Martino Rigano, V., Lobosco, O., Carfagna, S., Esposito, S., & Rigano, C. (2004). Temperature responses of growth, photosynthesis, respiration and NADH: Nitrate reductase in cryophilic and mesophilic algae. New Phytologist, 163, 325-331. https://doi.org/10.1111/j.1365-3040.2006.01523.x
Wickham, H. (2019). modelr: Modelling functions that work with the pipe. R package version 0.1, 4.
Wood, A. M., Everroad, R. C., & Wingard, L. M. (2005). Measuring growth rates in microalgal cultures. In R. A. Anderson (Ed.), Algal culturing techniques (pp. 269-288). Elsevier Academic Press.
Zhang, W. Y., Storey, K. B., & Dong, Y. W. (2021). Synchronization of seasonal acclimatization and short-term heat hardening improves physiological resilience in a changing climate. Functional Ecology, 35, 686-695. https://doi.org/10.1111/1365-2435.13768
Zhao, Y., Tang, X., Qu, F., Lv, M., Liu, Q., Li, J., Li, L., Zhang, B., & Zhao, Y. (2020). ROS-mediated programmed cell death (PCD) of Thalassiosira pseudonana under the stress of BDE-47. Environmental Pollution, 262. https://doi.org/10.1016/j.envpol.2020.114342
Zuppini, A., Andreoli, C., & Baldan, B. (2007). Heat stress: An inducer of programmed cell death in Chlorella saccharophila. Plant and Cell Physiology, 48, 1000-1009. https://doi.org/10.1093/pcp/pcm070

Auteurs

Kirralee G Baker (KG)

School of Life Sciences, University of Essex, Colchester, UK.

Richard J Geider (RJ)

School of Life Sciences, University of Essex, Colchester, UK.

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