| Summary: | Populations of genetically uniform microorganisms
exhibit phenotypic heterogeneity, where individual
cells have varying phenotypes. Such phenotypes
include fitness-determining traits. Phenotypic heterogeneity
has been linked to increased population-level
fitness in laboratory studies, but its adaptive significance
for wild microorganisms in the natural environment
is unknown. Here, we addressed this by testing
heterogeneity in yeast isolates from diverse environmental
sites, each polluted with a different principal
contaminant, as well as from corresponding control
locations. We found that cell-to-cell heterogeneity (in
resistance to the appropriate principal pollutant) was
prevalent in the wild yeast isolates. Moreover, isolates
with the highest heterogeneity were consistently
observed in the polluted environments, indicating
that heterogeneity is positively related to survival in
adverse conditions in the wild. This relationship with
survival was stronger than for the property of mean
resistance (IC50) of an isolate. Therefore, heterogeneity
could be the major determinant of microbial survival
in adverse conditions. Indeed, growth assays
indicated that isolates with high heterogeneities
had a significant competitive advantage during
stress. Analysis of yeasts after cultivation for ≥ 500
generations additionally showed that high heterogeneity
evolved as a heritable trait during stress. The
results showed that environmental stress selects for
wild microorganisms with high levels of phenotypic
heterogeneity.
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