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-native lineage 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 differentiation and competitive success of ST36 were associated with a striking succession of filamentous prophage in the family
Inoviridae
(inoviruses), including loss of an inovirus prophage that had been maintained for decades in the endemic north Pacific population. Subsequently, at least five distinct progenitors arising from this diversification translocated from the Pacific into the Atlantic and established four geographically defined clonal 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 diversification dynamics which preceded successful Atlantic invasion by the epidemiologically predominant ST36 lineage. It has been established experimentally that filamentous phage can limit host recombination, but here, we show that phage loss is linked to rapid bacterial host diversification during 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 define the contribution of inoviruses in the evolutionary dynamics of environmentally transmitted pathogens.