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

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          Abstract

          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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          Most cited references57

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          TOWARD A METABOLIC THEORY OF ECOLOGY

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            Climate change impacts on marine ecosystems.

            In marine ecosystems, rising atmospheric CO2 and climate change are associated with concurrent shifts in temperature, circulation, stratification, nutrient input, oxygen content, and ocean acidification, with potentially wide-ranging biological effects. Population-level shifts are occurring because of physiological intolerance to new environments, altered dispersal patterns, and changes in species interactions. Together with local climate-driven invasion and extinction, these processes result in altered community structure and diversity, including possible emergence of novel ecosystems. Impacts are particularly striking for the poles and the tropics, because of the sensitivity of polar ecosystems to sea-ice retreat and poleward species migrations as well as the sensitivity of coral-algal symbiosis to minor increases in temperature. Midlatitude upwelling systems, like the California Current, exhibit strong linkages between climate and species distributions, phenology, and demography. Aggregated effects may modify energy and material flows as well as biogeochemical cycles, eventually impacting the overall ecosystem functioning and services upon which people and societies depend.
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              Primary production of the biosphere: integrating terrestrial and oceanic components

              Integrating conceptually similar models of the growth of marine and terrestrial primary producers yielded an estimated global net primary production (NPP) of 104.9 petagrams of carbon per year, with roughly equal contributions from land and oceans. Approaches based on satellite indices of absorbed solar radiation indicate marked heterogeneity in NPP for both land and oceans, reflecting the influence of physical and ecological processes. The spatial and temporal distributions of ocean NPP are consistent with primary limitation by light, nutrients, and temperature. On land, water limitation imposes additional constraints. On land and ocean, progressive changes in NPP can result in altered carbon storage, although contrasts in mechanisms of carbon storage and rates of organic matter turnover result in a range of relations between carbon storage and changes in NPP.
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                Author and article information

                Contributors
                logan.m.gonzalez@erdc.dren.mil
                Journal
                BMC Ecol Evol
                BMC Ecol Evol
                BMC Ecology and Evolution
                BioMed Central (London )
                2730-7182
                18 November 2022
                18 November 2022
                2022
                : 22
                : 136
                Affiliations
                [1 ]GRID grid.431335.3, ISNI 0000 0004 0582 4666, Biogeochemical Sciences Branch, Cold Regions Research and Engineering Laboratory, , US Army Corps of Engineers, ; Hanover, NH 03755 USA
                [2 ]GRID grid.133342.4, ISNI 0000 0004 1936 9676, Department of Ecology, Evolution, and Marine Biology, , University of California-Santa Barbara, ; Santa Barbara, CA 93106 USA
                Article
                2092
                10.1186/s12862-022-02092-9
                9675069
                36401160
                47fbe2ee-b2e9-4c0b-8a28-43e14dd33351
                © The Author(s) 2022

                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/. The Creative Commons Public Domain Dedication waiver ( http://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.

                History
                : 22 May 2022
                : 7 November 2022
                Funding
                Funded by: National Science Foundation
                Award ID: OCE-1851194
                Award Recipient :
                Funded by: Simons Foundation
                Award ID: 689265
                Award Recipient :
                Funded by: U.S. Army Research Office
                Categories
                Research
                Custom metadata
                © The Author(s) 2022

                mixoplankton,adaptive dynamics,metabolic scaling,carbon cycle,eco-evolutionary feedback

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