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Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures

BACKGROUND: Climate change is expected to lead to warming in ocean surface temperatures which will have unequal effects on the rates of photosynthesis and heterotrophy. As a result of this changing metabolic landscape, directional phenotypic evolution will occur, with implications that cascade up to...

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Autores principales: Gonzalez, Logan M., Proulx, Stephen R., Moeller, Holly V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9675069/
https://www.ncbi.nlm.nih.gov/pubmed/36401160
http://dx.doi.org/10.1186/s12862-022-02092-9
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author Gonzalez, Logan M.
Proulx, Stephen R.
Moeller, Holly V.
author_facet Gonzalez, Logan M.
Proulx, Stephen R.
Moeller, Holly V.
author_sort Gonzalez, Logan M.
collection PubMed
description BACKGROUND: Climate change is expected to lead to warming in ocean surface temperatures which will have unequal effects on the rates of photosynthesis and heterotrophy. As a result of this changing metabolic landscape, directional phenotypic evolution will occur, with implications that cascade up to the ecosystem level. While mixotrophic phytoplankton, organisms that combine photosynthesis and heterotrophy to meet their energetic and nutritional needs, are expected to become more heterotrophic with warmer temperatures due to heterotrophy increasing at a faster rate than photosynthesis, it is unclear how evolution will influence how these organisms respond to warmer temperatures. In this study, we used adaptive dynamics to model the consequences of temperature-mediated increases in metabolic rates for the evolution of mixotrophic phytoplankton, focusing specifically on phagotrophic mixotrophs. RESULTS: We find that mixotrophs tend to evolve to become more reliant on phagotrophy as temperatures rise, leading to reduced prey abundance through higher grazing rates. However, if prey abundance becomes too low, evolution favors greater reliance on photosynthesis. These responses depend upon the trade-off that mixotrophs experience between investing in photosynthesis and phagotrophy. Mixotrophs with a convex trade-off maintain mixotrophy over the greatest range of temperatures; evolution in these “generalist” mixotrophs was found to exacerbate carbon cycle impacts, with evolving mixotrophs exhibiting increased sensitivity to rising temperature. CONCLUSIONS: Our results show that mixotrophs may respond more strongly to climate change than predicted by phenotypic plasticity alone due to evolutionary shifts in metabolic investment. However, the type of metabolic trade-off experienced by mixotrophs as well as ecological feedback on prey abundance may ultimately limit the extent of evolutionary change along the heterotrophy-phototrophy spectrum. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-02092-9.
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spelling pubmed-96750692022-11-20 Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures Gonzalez, Logan M. Proulx, Stephen R. Moeller, Holly V. BMC Ecol Evol Research BACKGROUND: Climate change is expected to lead to warming in ocean surface temperatures which will have unequal effects on the rates of photosynthesis and heterotrophy. As a result of this changing metabolic landscape, directional phenotypic evolution will occur, with implications that cascade up to the ecosystem level. While mixotrophic phytoplankton, organisms that combine photosynthesis and heterotrophy to meet their energetic and nutritional needs, are expected to become more heterotrophic with warmer temperatures due to heterotrophy increasing at a faster rate than photosynthesis, it is unclear how evolution will influence how these organisms respond to warmer temperatures. In this study, we used adaptive dynamics to model the consequences of temperature-mediated increases in metabolic rates for the evolution of mixotrophic phytoplankton, focusing specifically on phagotrophic mixotrophs. RESULTS: We find that mixotrophs tend to evolve to become more reliant on phagotrophy as temperatures rise, leading to reduced prey abundance through higher grazing rates. However, if prey abundance becomes too low, evolution favors greater reliance on photosynthesis. These responses depend upon the trade-off that mixotrophs experience between investing in photosynthesis and phagotrophy. Mixotrophs with a convex trade-off maintain mixotrophy over the greatest range of temperatures; evolution in these “generalist” mixotrophs was found to exacerbate carbon cycle impacts, with evolving mixotrophs exhibiting increased sensitivity to rising temperature. CONCLUSIONS: Our results show that mixotrophs may respond more strongly to climate change than predicted by phenotypic plasticity alone due to evolutionary shifts in metabolic investment. However, the type of metabolic trade-off experienced by mixotrophs as well as ecological feedback on prey abundance may ultimately limit the extent of evolutionary change along the heterotrophy-phototrophy spectrum. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-02092-9. BioMed Central 2022-11-18 /pmc/articles/PMC9675069/ /pubmed/36401160 http://dx.doi.org/10.1186/s12862-022-02092-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Gonzalez, Logan M.
Proulx, Stephen R.
Moeller, Holly V.
Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
title Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
title_full Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
title_fullStr Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
title_full_unstemmed Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
title_short Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
title_sort modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9675069/
https://www.ncbi.nlm.nih.gov/pubmed/36401160
http://dx.doi.org/10.1186/s12862-022-02092-9
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