Experimental Evolution in Plant-Microbe Systems: A Tool for Deciphering the Functioning and Evolution of Plant-Associated Microbial Communities

Abstract

In natural environments, microbial communities must constantly adapt to stressful environmental conditions. The genetic and phenotypic mechanisms underlying the adaptive response of microbial communities to new (and often complex) environments can be tackled with a combination of experimental evolution and next generation sequencing. This combination allows to analyse the real-time evolution of microbial populations in response to imposed environmental factors or during the interaction with a host, by screening for phenotypic and genotypic changes over a multitude of identical experimental cycles. Experimental evolution (EE) coupled with comparative genomics has indeed facilitated the monitoring of bacterial genetic evolution and the understanding of adaptive evolution processes. Basically, EE studies had long been done on single strains, allowing to reveal the dynamics and genetic targets of natural selection and to uncover the correlation between genetic and phenotypic adaptive changes. However, species are always evolving in relation with other species and have to adapt not only to the environment itself but also to the biotic environment dynamically shaped by the other species. Nowadays, there is a growing interest to apply EE on microbial communities evolving under natural environments. In this paper, we provide a non-exhaustive review of microbial EE studies done with systems of increasing complexity (from single species, to synthetic communities and natural communities) and with a particular focus on studies between plants and plant-associated microorganisms. We highlight some of the mechanisms controlling the functioning of microbial species and their adaptive responses to environment changes and emphasize the importance of considering bacterial communities and complex environments in EE studies.

Metagenomic Analyses of the Soybean Root Mycobiome and Microbiome Reveal Signatures of the Healthy and Diseased Plants Affected by Taproot Decline

“…Nevertheless, the predictions advanced by our work require future testing in natural and synthetic biomes. Understanding the principles underlying complex multi-species assemblages and the factors determining their stability and dynamics lays the foundation of sustainable agriculture [ 78 , 79 ].…”

Evolution of manipulative microbial behaviors in the rhizosphere

“…Accounting for the fitness outcomes for microbial partners will allow better prediction of the stability of beneficial plant–microbe interactions. Likewise, experimental evolution has become a powerful tool to study the precise selection pressures driving antagonistic strains to evolve mutualistic behavior (Li, de Jonge, et al, 2021 ; Li et al, 2021 ; Manriquez et al, 2021 ). However, because of the difficulties in following the evolution of traits in genetically diverse consortia over time, these experiments are often performed in low‐diversity (e.g., one strain) systems (Marchetti et al, 2014 , 2017 ; Quides et al, 2021 ).…”

Soil pH Filters the Association Patterns of Aluminum-Tolerant Microorganisms in Rice Paddies

“…Environmental stresses can collectively affect various microbial functions to resist selective stresses ( 42 ). In turn, the function of microbial communities affects their environment, leading to further changes in associations with its members ( 43 ). For example, resistant microorganisms may coexist to relieve environmental stress and provide favorable conditions for the survival of sensitive microorganisms ( 44 ).…”

“…As we inferred from the directed network, the influential and bidirectional taxa may have effects on sensitive taxa and benefit them under acidic stress. In microbial community dynamics, species always evolve with other species and adapt not only to the environment itself but also to the biological environment formed by other species ( 43 ). Here, different microbial functional roles may be determined in part by their different ecological niches.…”