The cost of adaptability: resource availability constrains functional stability under pulsed disturbances

Author:

Rain-Franco Angel12ORCID,Peter Hannes3ORCID,Pavan de Moraes Guilherme124,Beier Sara12ORCID

Affiliation:

1. UMR 7621 Laboratoire d’Océanographie Microbienne, Observatoire Océanologique de Banyuls-sur-Mer, Sorbonne Université, Banyuls-sur-Mer, France

2. Department of Biological Oceanography, Leibniz Institute for Baltic Sea Research Warnemünde, Rostock, Germany

3. River Ecosystems Laboratory, Ecole Polytechnique Federale de Lausanne, Lausanne, Switzerland

4. Department of Botany, Graduate Program in Ecology and Natural Resources (PPGERN), Laboratory of Phycology, Universidade Federal de São Carlos, São Carlos, Brazil

Abstract

ABSTRACT Global change exposes ecosystems to changes in the frequency, magnitude, and concomitancy of disturbances, which impact the composition and functioning of these systems. Here, we experimentally evaluate the effects of salinity disturbances and eutrophication on bacterial communities from coastal ecosystems. The functional stability of these communities is critically important for maintaining water quality, productivity, and ecosystem services, such as fishery yields. Microbial functional stability can be maintained via resistance and resilience, which are reflected in genomic traits such as genome size and codon usage bias and may be linked to metabolic costs. However, little is known about the mechanisms that select these traits under varying nutrient regimes. To study the impact of pulsed disturbances on community assembly and functioning depending on metabolic costs, we performed a 41-day pulse disturbance experiment across two levels of resource availability. Our setup triggered stochastic community re-assembly processes in all treatments. In contrast, we observed consistent and resource availability-dependent patterns of superordinate community functioning and structural patterns, such as functional resistance in response to disturbances, genomic trait distributions, and species diversity. Predicted genomic traits reflected the selection for taxa possessing resistant- and resilience-related traits, particularly under high nutrient availability. Our findings are a step toward unraveling the compositional and genomic underpinnings of functional resistance in microbial communities after exposure to consecutive pulse disturbances. Our work demonstrates how resource availability alleviates metabolic constraints on resistance and resilience, and this has important consequences for predicting water quality and ecosystem productivity of environments exposed to global change. IMPORTANCE Understanding the communities’ responses to disturbances is a prerequisite to predicting ecosystem dynamics and, thus, highly relevant considering global change. Microbial communities play key roles in numerous ecosystem functions and services, and the large diversity, rapid growth, and phenotypic plasticity of microorganisms are thought to allow high resistance and resilience. While potential metabolic costs associated with adaptations to fluctuating environments have been debated, little evidence supports trade-offs between resource availability, resistance, and resilience. Here, we experimentally assessed the compositional and functional responses of an aquatic microbial model community to disturbances and systematically manipulated resource availability. Our results demonstrate that the capacity to tolerate environmental fluctuations is constrained by resource availability and reflected in the selection of genomic traits.

Funder

Agencia Nacional de Investigación y Desarrollo

Coordination for the improvement of higher education personnel

Deutsche Forschungsgemeinschaft

German Network for Bioinformatics Infrastructure

Publisher

American Society for Microbiology

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