Predicting Optimal Mixotrophic Metabolic Strategies in the Global Ocean

Overview

Journal Sci Adv

Specialties Biology
Science

Date 2024 Dec 13

PMID 39671489

Authors

Holly V Moeller

Kevin M Archibald

Suzana G Leles

Ferdinand Pfab

Affiliations

Soon will be listed here.

Abstract

Mixotrophic protists combine photosynthesis with the ingestion of prey to thrive in resource-limited conditions in the ocean. Yet, how they fine-tune resource investments between their two different metabolic strategies remains unclear. Here, we present a modeling framework (Mixotroph Optimal Contributions to Heterotrophy and Autotrophy) that predicts the optimal (growth-maximizing) investments of carbon and nitrogen as a function of environmental conditions. Our model captures a full spectrum of trophic modes, in which the optimal investments reflect zero-waste solutions (i.e., growth is colimited by carbon and nitrogen) and accurately reproduces experimental results. By fitting the model to data for , we were able to predict metabolic strategies at a global scale. We find that high phagotrophic investment is the dominant strategy across different oceanic biomes, used primarily for nitrogen acquisition. Our results therefore support empirical observations of the importance of mixotrophic grazers to upper ocean bacterivory.

References

Edwards K, Li Q, McBeain K, Schvarcz C, Steward G . Trophic strategies explain the ocean niches of small eukaryotic phytoplankton. Proc Biol Sci. 2023; 290(1991):20222021. PMC: 9874276. DOI: 10.1098/rspb.2022.2021. View

Chakraborty S, Nielsen L, Andersen K . Trophic Strategies of Unicellular Plankton. Am Nat. 2017; 189(4):E77-E90. DOI: 10.1086/690764. View

Ward B, Follows M . Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. Proc Natl Acad Sci U S A. 2016; 113(11):2958-63. PMC: 4801304. DOI: 10.1073/pnas.1517118113. View

Follett C, Dutkiewicz S, Ribalet F, Zakem E, Caron D, Armbrust E . Trophic interactions with heterotrophic bacteria limit the range of . Proc Natl Acad Sci U S A. 2022; 119(2). PMC: 8764666. DOI: 10.1073/pnas.2110993118. View

Gonzalez L, Proulx S, Moeller H . Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures. BMC Ecol Evol. 2022; 22(1):136. PMC: 9675069. DOI: 10.1186/s12862-022-02092-9. View

Berge T, Chakraborty S, Hansen P, Andersen K . Modeling succession of key resource-harvesting traits of mixotrophic plankton. ISME J. 2016; 11(1):212-223. PMC: 5315484. DOI: 10.1038/ismej.2016.92. View

Lie A, Liu Z, Terrado R, Tatters A, Heidelberg K, Caron D . A tale of two mixotrophic chrysophytes: Insights into the metabolisms of two Ochromonas species (Chrysophyceae) through a comparison of gene expression. PLoS One. 2018; 13(2):e0192439. PMC: 5811012. DOI: 10.1371/journal.pone.0192439. View

Sanders R, Porter K, Caron D . Relationship between phototrophy and phagotrophy in the mixotrophic chrysophytePoterioochromonas malhamensis. Microb Ecol. 2013; 19(1):97-109. DOI: 10.1007/BF02015056. View

Wilken S, Choi C, Worden A . Contrasting Mixotrophic Lifestyles Reveal Different Ecological Niches in Two Closely Related Marine Protists. J Phycol. 2019; 56(1):52-67. PMC: 7065223. DOI: 10.1111/jpy.12920. View

10.

Johnson M . Inducible Mixotrophy in the Dinoflagellate Prorocentrum minimum. J Eukaryot Microbiol. 2014; 62(4):431-43. DOI: 10.1111/jeu.12198. View

11.

Faure E, Not F, Benoiston A, Labadie K, Bittner L, Ayata S . Mixotrophic protists display contrasted biogeographies in the global ocean. ISME J. 2019; 13(4):1072-1083. PMC: 6461780. DOI: 10.1038/s41396-018-0340-5. View

12.

Hartmann M, Grob C, Tarran G, Martin A, Burkill P, Scanlan D . Mixotrophic basis of Atlantic oligotrophic ecosystems. Proc Natl Acad Sci U S A. 2012; 109(15):5756-60. PMC: 3326507. DOI: 10.1073/pnas.1118179109. View

13.

Kirchman D, Moran X, Ducklow H . Microbial growth in the polar oceans - role of temperature and potential impact of climate change. Nat Rev Microbiol. 2009; 7(6):451-9. DOI: 10.1038/nrmicro2115. View

14.

Klausmeier C, Litchman E, Daufresne T, Levin S . Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature. 2004; 429(6988):171-4. DOI: 10.1038/nature02454. View

15.

Tittel J, Bissinger V, Zippel B, Gaedke U, Bell E, Lorke A . Mixotrophs combine resource use to outcompete specialists: implications for aquatic food webs. Proc Natl Acad Sci U S A. 2003; 100(22):12776-81. PMC: 240694. DOI: 10.1073/pnas.2130696100. View

16.

Millette N, Gast R, Luo J, Moeller H, Stamieszkin K, Andersen K . Mixoplankton and mixotrophy: future research priorities. J Plankton Res. 2023; 45(4):576-596. PMC: 10361813. DOI: 10.1093/plankt/fbad020. View

17.

Cermak N, Becker J, Knudsen S, Chisholm S, Manalis S, Polz M . Direct single-cell biomass estimates for marine bacteria via Archimedes' principle. ISME J. 2016; 11(3):825-828. PMC: 5322313. DOI: 10.1038/ismej.2016.161. View

18.

Edwards K . Mixotrophy in nanoflagellates across environmental gradients in the ocean. Proc Natl Acad Sci U S A. 2019; 116(13):6211-6220. PMC: 6442547. DOI: 10.1073/pnas.1814860116. View

19.

Mitra A, Flynn K, Tillmann U, Raven J, Caron D, Stoecker D . Defining Planktonic Protist Functional Groups on Mechanisms for Energy and Nutrient Acquisition: Incorporation of Diverse Mixotrophic Strategies. Protist. 2016; 167(2):106-20. DOI: 10.1016/j.protis.2016.01.003. View

20.

Stoecker D, Hansen P, Caron D, Mitra A . Mixotrophy in the Marine Plankton. Ann Rev Mar Sci. 2016; 9:311-335. DOI: 10.1146/annurev-marine-010816-060617. View