Biodiversity of marine microbes is safeguarded by phenotypic heterogeneity in ecological traits

RESEARCH ARTICLE Biodiversity of marine microbes is safeguarded by phenotypic heterogeneity in ecological traits Susanne Menden-Deuer1, Julie RowlettID2*, Medet Nursultanov3, Sinead Collins4, Tatiana Rynearson1 1 Graduate School of Oceanography, University of Rhode Island, Narragansett Bay Campus, Narragansett, RI, United States of America, 2 Mathematical Sciences, Chalmers University and the University of Gothenburg, Gothenburg, Sweden, 3 School of Mathematics and Statistics, University of Sydney, Camperdown, Australia, 4 Biological Sciences, Ashworth Laboratories, University of Edinburgh, Edinburgh, United Kingdom * julie.rowlett@chalmers.se Abstract Why, contrary to theoretical predictions, do marine microbe communities harbor tremen- dous phenotypic heterogeneity? How can so many marine microbe species competing in the same niche coexist? We discovered a unifying explanation for both phenomena by investigating a non-cooperative game that interpolates between individual-level competi- tions and species-level outcomes. We identified all equilibrium strategies of the game. These strategies represent the probability distribution of competitive abilities (e.g. traits) and are characterized by maximal phenotypic heterogeneity. They are also neutral towards each other in the sense that an unlimited number of species can co-exist while competing according to the equilibrium strategies. Whereas prior theory predicts that natural selection would minimize trait variation around an optimum value, here we obtained a mathematical

proof that species with maximally variable traits are those that endure. This discrepancy may reflect a disparity between predictions from models developed for larger organisms in contrast to our microbe-centric model. Rigorous mathematics proves that phenotypic het- erogeneity is itself a mechanistic underpinning of microbial diversity. This discovery has fun- damental ramifications for microbial ecology and may represent an adaptive reservoir sheltering biodiversity in changing environmental conditions. Introduction Marine planktonic microbes make Earth habitable by collectively generating as much organic matter and oxygen as all terrestrial plants combined [1]. The ecological, biogeochemical and economical importance of marine microbes is rooted in their vast species and metabolic diver- sity [1, 2]. Recent estimates of marine microbial species diversity exceed 200,000 species in the plankton [3, 4]. At all levels of taxonomy, from species to intra-strain comparisons, there exists a tremendous and theoretically inexplicable variability in genetic, physiological, behavioral PLOS ONE PLOS ONE | https://doi.org/10.1371/journal.pone.0254799 August 4, 2021 1 / 18 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Menden-Deuer S, Rowlett J, Nursultanov M, Collins S, Rynearson T (2021) Biodiversity of marine microbes is safeguarded by phenotypic heterogeneity in ecological traits. PLoS ONE 16(8): e0254799. https://doi.org/10.1371/journal. pone.0254799 Editor: Andrea Belgrano, Swedish University of

Agricultural Sciences and Swedish Institute for the Marine Environment, University of Gothenburg, SWEDEN Received: January 17, 2021 Accepted: July 5, 2021 Published: August 4, 2021 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0254799 Copyright: © 2021 Menden-Deuer et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.