Abstract
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.
Highlights
Individual cells of genetically uniform populations can exhibit marked heterogeneity despite being isogenic
In order to test the hypothesis that phenotypic heterogeneity is a selected trait in stressed wild environments, yeasts were isolated from unpolluted and polluted locations at three environmental sites, as detailed in the Methods section
Multiple independent non-clonal isolates of C. podzolicus were collected from the polluted and control locations, as we corroborated by the random amplification of polymorphic DNA (RAPD) analyses
Summary
Individual cells of genetically uniform populations can exhibit marked heterogeneity despite being isogenic This is evident in effectively any cell phenotype, including virulence of pathogenic organisms (Halliwell et al, 2012; Stewart and Cookson, 2012), cell differentiation and reprogramming (Mirouze et al, 2011; Buganim et al, 2012), and resistance to antibiotics (Balaban et al, 2004; Wakamoto et al, 2013) and other stressors (Kale and Jazwinski, 1996; Sumner et al, 2003; Bishop et al, 2007; Smith et al, 2007; Levy et al, 2012). Studies in recent years have shown that variation in gene expression between such isogenic cells is the principal basis for heterogeneity. Gene promoter sequences that can determine the level of noise in gene expression in prokaryotes and eukaryotes have been identified (Raser and O’Shea, 2004; Blake et al, 2006; Freed et al, 2008; Li et al, 2010; Hornung et al, 2012; Silander et al, 2012; Carey et al, 2013)
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