Opportunistic pathogens are environmental microbes that are generally harmless and only occasionally cause disease. Unlike obligate pathogens, the growth and survival of opportunistic pathogens does not rely on host infection or transmission. Their versatile lifestyles make it challenging to decipher how and why virulence has evolved in opportunistic pathogens. The Coincidental Evolution Hypothesis (CEH) postulates that virulence results from exaptation, i.e., traits evolved for adaptation to living in one environment that have a different function in another. Several studies have tested the CEH, but results have been inconclusive. Here we used experimental evolution to determine how the presence of a predator impacts the virulence and fitness of a ubiquitous environmental opportunistic bacterial pathogen that has acquired multi-drug resistance: Serratia marcescens. We evolved S. marcescens in the presence or absence of a generalist protist predator, Tetrahymena thermophila, and evaluated the genotypic and phenotypic changes that occurred after evolution. Overall, we found that evolution in the presence of a predator maintained or increased virulence, whereas evolution in the absence of a predator resulted in attenuated virulence. Strains evolved in the presence or absence of a predator presented different phenotypic traits, such as increased biofilm formation and decreased predation resistance, respectively. Whole genome shotgun (WGS) sequencing of the evolved strains revealed multiple cases of parallel evolution in genes associated with virulence. Our results provide evidence that bacterial virulence is maintained by selective pressures imposed by protist predators, supporting the CEH.
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