Size evolution in microorganisms masks trade-offs predicted by the growth rate hypothesis

Author:

Gounand Isabelle1234ORCID,Daufresne Tanguy5,Gravel Dominique2ORCID,Bouvier Corinne6,Bouvier Thierry6,Combe Marine17ORCID,Gougat-Barbera Claire1,Poly Franck8,Torres-Barceló Clara1,Mouquet Nicolas16ORCID

Affiliation:

1. Institut des Sciences de l'Evolution de Montpellier, CNRS, IRD, EPHE, Faculté des Sciences de Montpellier, Place Eugène Bataillon, 34095 Montpellier Cedex 05, France

2. Département de Biologie, Université du Québec à Rimouski, Rimouski, Canada

3. Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland

4. Eawag, Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, 8600 Dübendorf, Switzerland

5. INRA -UMR Eco&Sols - Bat 12, 2 Place Viala, 34060 Montpellier cedex 1, France

6. MARBEC (MARine Biodiversity Exploitation and Conservation), UMR IRD-CNRS-UM-IFREMER 9190, Université Montpellier, CC 093, 34095 Montpellier Cedex 5, France

7. UMR MIVEGEC IRD-CNRS-Université de Montpellier, Centre IRD de Montpellier, Montpellier, France

8. Laboratoire d'Ecologie Microbienne, Université de Lyon, Université Lyon 1, CNRS, INRA, UMR CNRS 5557, UMR INRA 1418, Bâtiment Gregor Mendel, 16, rue Raphael Dubois, 69622 Villeurbanne Cedex, France

Abstract

Adaptation to local resource availability depends on responses in growth rate and nutrient acquisition. The growth rate hypothesis (GRH) suggests that growing fast should impair competitive abilities for phosphorus and nitrogen due to high demand for biosynthesis. However, in microorganisms, size influences both growth and uptake rates, which may mask trade-offs and instead generate a positive relationship between these traits (size hypothesis, SH). Here, we evolved a gradient of maximum growth rate ( μ max ) from a single bacterium ancestor to test the relationship among μ max , competitive ability for nutrients and cell size, while controlling for evolutionary history. We found a strong positive correlation between μ max and competitive ability for phosphorus, associated with a trade-off between μ max and cell size: strains selected for high μ max were smaller and better competitors for phosphorus. Our results strongly support the SH, while the trade-offs expected under GRH were not apparent. Beyond plasticity, unicellular populations can respond rapidly to selection pressure through joint evolution of their size and maximum growth rate. Our study stresses that physiological links between these traits tightly shape the evolution of competitive strategies.

Funder

French Ministry of Research and Technology

Centre National de la Recherche Scientifique

Conseil Scientifique de l'Université Montpellier 2

Fonds Québécois de la Recherche sur la Nature et les Technologies

French Consulate

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

Reference59 articles.

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