Abstract
The type VI secretion system (T6SS) operons of Vibrio cholerae contain extraordinarily diverse arrays of toxic effector and cognate immunity genes, which are thought to play an important role in the environmental lifestyle and adaptation of this human pathogen. Through the T6SS, proteinaceous “spears” tipped with antibacterial effectors are injected into adjacent cells, killing those not possessing immunity proteins to these effectors. Here, we investigate the T6SS-mediated dynamics of bacterial competition within a single environmental population of V. cholerae. We show that numerous members of a North American V. cholerae population possess strain-specific repertoires of cytotoxic T6SS effector and immunity genes. Using pairwise competition assays, we demonstrate that the vast majority of T6SS-mediated duels end in stalemates between strains with different T6SS repertoires. However, horizontally acquired effector and immunity genes can significantly alter the outcome of these competitions. Frequently observed horizontal gene transfer events can both increase or reduce competition between distantly related strains by homogenizing or diversifying the T6SS repertoire. Our results also suggest temperature-dependent outcomes in T6SS competition, with environmental isolates faring better against a pathogenic strain under native conditions than under those resembling a host-associated environment. Taken altogether, these interactions produce density-dependent fitness effects and a constant T6SS-mediated arms race in individual V. cholerae populations, which could ultimately preserve intraspecies diversity. Since T6SSs are widespread, we expect within-population diversity in T6SS repertoires and the resulting competitive dynamics to be a common theme in bacterial species harboring this machinery.
Highlights
Environmental populations of Vibrio cholerae, the etiological agent of cholera, are composed of different toxigenic and nontoxigenic lineages living together in brackish water habitats (Pretzer et al, 2017; Mavian et al, 2020)
To understand T6SS-mediated competitive dynamics in V. cholerae populations, we analyzed the structure of T6SS loci in 14 dominant strains from an extensively sampled coastal population in the eastern United States (Kirchberger et al, 2016, 2020)
As previous experimental results show that strains possessing different E-I module combinations are capable of mutual killing, and assuming that orphan immunity genes are capable of detoxifying cognate effectors, the vast majority of strain combinations within this population should not be able to coexist in close contact without mutual T6SS-mediated killing (Supplementary Figure 1)
Summary
Environmental populations of Vibrio cholerae, the etiological agent of cholera, are composed of different toxigenic and nontoxigenic lineages living together in brackish water habitats (Pretzer et al, 2017; Mavian et al, 2020). T6SS structural genes are spread over three loci termed aux-1, aux-2, and large cluster in the V. cholerae genome (Unterweger et al, 2014). Components of these loci form the T6SS apparatus, which has evolved from a bacteriophage tail spike (Pukatzki et al, 2007; Bock et al, 2017; Nguyen et al, 2017). It consists of a hollow tube tipped with a membrane-puncturing protein spear, surrounded by an outer sheath (Leiman et al, 2009; Zoued et al, 2014). Given the large number of E-I modules, strains of V. cholerae could theoretically display millions of different combinations, and the observed strain level diversity in T6SS module combinations is vast (Kirchberger et al, 2017)
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