Inoviridae prophage and bacterial host dynamics during diversification,succession, and Atlantic invasion of Pacific-nativeVibrio parahaemolyticus

Abstract

The epidemiology of Vibrio parahaemolyticus, the leading cause of seafood-borne bacterial gastroenteritis of humans worldwide, dramatically changed in the United States following the establishment of a Pacific-nativelineage called sequence type (ST) 36 in the Atlantic. In this study, we used phylogeography based on traceback to environmental source locations and comparative genomics to identify features that promoted evolution, dispersal, and competitive dominance of ST36. The major genomic differentiationand competitive success of ST36 were associated with a striking succession of filamentousprophage in the family Inoviridae (inoviruses), including loss of an inovirus prophage that had been maintained for decades in the endemic north Pacificpopulation. Subsequently, at least fivedistinct progenitors arising from this diversificationtranslocated from the Pacificinto the Atlantic and established four geographically definedclonal subpopulations with remarkably low migration or mixing. Founders of two prevailing Atlantic subpopulations each acquired new stable and diagnostic inoviruses while other subpopulations that apparently declined did not. Broader surveys indicate inoviruses are common and active among the global population of V. parahaemolyticus, and though inovirus replacements, such as in ST36, appear to be infrequent, they are notable in pathogenic lineages that dispersed. IMPORTANCE An understanding of the processes that contribute to the emergence of pathogens from environmental reservoirs is critical as changing climate precipitates pathogen evolution and population expansion. Phylogeographic analysis of Vibrio parahaemolyticus hosts combined with the analysis of their Inoviridae phage resolved ambiguities of diversificationdynamics which preceded successful Atlantic invasion by the epidemiologically predominant ST36 lineage. It has been established experimentally that filamentousphage can limit host recombination, but here, we show that phage loss is linked to rapid bacterial host diversificationduring epidemic spread in natural ecosystems alluding to a potential role for ubiquitous inoviruses in the adaptability of pathogens. This work paves the way for functional analyses to definethe contribution of inoviruses in the evolutionary dynamics of environmentally transmitted pathogens.