Abstract

For micro-organisms cycling between free-living and host-associated stages, where reproduction occurs in both of these lifestyles, an interesting inquiry is whether evolution during the free-living stage can be positively pleiotropic to microbial fitness in a host environment. To address this topic, the squid host Euprymna tasmanica and the marine bioluminescent bacterium Vibrio fischeri were utilized. Microbial ecological diversification in static liquid microcosms was used to simulate symbiont evolution during the free-living stage. Thirteen genetically distinct V. fischeri strains from a broad diversity of ecological sources (e.g. squid light organs, fish light organs and seawater) were examined to see if the results were reproducible in many different genetic settings. Genetic backgrounds that are closely related can be predisposed to considerable differences in how they respond to similar selection pressures. For all strains examined, new mutations with striking and facilitating effects on host colonization arose quickly during microbial evolution in the free-living stage, regardless of the ecological context under consideration for a strain’s genetic background. Microbial evolution outside a host environment promoted host range expansion, improved host colonization for a micro-organism, and diminished the negative correlation between biofilm formation and motility.

Highlights

  • Micro-organisms possess the opportunity to adapt to their free-living and host-linked life histories [1]

  • Even in the absence of antagonistic pleiotropy, if prolonged microbial evolution occurs outside the native host environment, microbial fitness might decrease in a host due to the absence of purifying selection [5, 6]

  • By utilizing several different strains, this study investigated how microbial fitness inside the squid host would improve for different bacterial genetic backgrounds after evolution during the free-living stage

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Summary

Introduction

Micro-organisms possess the opportunity to adapt to their free-living and host-linked life histories [1]. The greatest opportunity for a micro-organism to adapt and exploit a host–microbe relationship might be when microbial evolution occurs in the host, since this is the environment where beneficial mutations will arise and be promoted by natural selection [7, 8]. Evolution in the free-living stage has important implications for the movement of microbial populations across host adaptive landscapes, where each fitness peak (i.e. fitness optimum) represents local adaptation to a particular host environment or a specific aspect of a host–microbe interaction [13, 14]. Microbial evolution during the free-living stage may permit fitness valleys to be crossed, enabling peak shifts from lower to higher fitness optima within host adaptive landscapes

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