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Microbial population dynamics decouple nutrient affinity from environmental concentration

View ORCID ProfileJustus Wilhelm Fink, View ORCID ProfileNoelle A. Held, View ORCID ProfileMichael Manhart
doi: https://doi.org/10.1101/2022.05.04.490627
Justus Wilhelm Fink
1Institute of Integrative Biology, Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland
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  • For correspondence: justus.fink@env.ethz.ch
Noelle A. Held
2Institute of Biogeochemistry and Pollutant Dynamics, Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland
3Department of Environmental Microbiology, Swiss Federal Institute of Aquatic Science and Technology (Eawag), Dübendorf, Switzerland
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Michael Manhart
1Institute of Integrative Biology, Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland
3Department of Environmental Microbiology, Swiss Federal Institute of Aquatic Science and Technology (Eawag), Dübendorf, Switzerland
4Center for Advanced Biotechnology and Medicine and Department of Biochemistry and Molecular Biology, Robert Wood Johnson Medical School, Rutgers University, Piscataway, NJ, USA
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Abstract

How the growth rate of a microbial population depends on the availability of chemical nutrients and other resources in the environment is a fundamental question in microbiology. Models of this dependence, such as the well-known Monod model, are characterized by a threshold concentration (or affinity) of the resource, above which the population can grow near its maximum rate. Even though this concept is a core element of microbiological and ecological modeling, there is little empirical and theoretical evidence for the evolved diversity of these thresholds. In particular, does resource scarcity drive populations to evolve commensurately lower thresholds? To address this question, we perform the largest-to-date meta-analysis of resource threshold data across a wide range of organisms and resources, substantially expanding previous surveys. We find that the thresholds vary across orders of magnitude, even for the same organism and resource. To explain this variation, we develop an evolutionary model to show that demographic fluctuations (genetic drift) can constrain the adaptation of resource thresholds. We find that this effect fundamentally differs depending on the type of population dynamics: populations undergoing periodic bottlenecks of fixed size will adapt their thresholds in proportion to the environmental resource concentration, but populations undergoing periodic dilutions of fixed size will evolve thresholds that are largely decoupled from the environmental concentration. Our model not only provides testable predictions for laboratory evolution experiments, but it also reveals how an evolved resource threshold may not reflect the organism’s environment. In particular, this explains how organisms in nutrient-rich environments can still evolve facultative growth at low resource concentrations. Altogether our results demonstrate the critical role of population dynamics in shaping fundamental ecological traits.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted May 04, 2022.
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Microbial population dynamics decouple nutrient affinity from environmental concentration
Justus Wilhelm Fink, Noelle A. Held, Michael Manhart
bioRxiv 2022.05.04.490627; doi: https://doi.org/10.1101/2022.05.04.490627
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Microbial population dynamics decouple nutrient affinity from environmental concentration
Justus Wilhelm Fink, Noelle A. Held, Michael Manhart
bioRxiv 2022.05.04.490627; doi: https://doi.org/10.1101/2022.05.04.490627

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