Genomic Variation and Evolution ofVibrio parahaemolyticusST36 over the Course of a Transcontinental Epidemic Expansion

Abstract

Vibrio parahaemolyticus is the leading cause of seafood-related infections with illnesses undergoing a geographic expansion. In this process of expansion, the most fundamental change has been the transition from infections caused by local strains to the surge of pandemic clonal types. Pandemic clone sequence type 3 (ST3) was the only example of transcontinental spreading until 2012, when ST36 was detected outside the region where it is endemic in the U.S. Pacific Northwest causing infections along the U.S. northeast coast and Spain. Here, we used genome-wide analyses to reconstruct the evolutionary history of the V. parahaemolyticus ST36 clone over the course of its geographic expansion during the previous 25 years. The origin of this lineage was estimated to be in~1985. By 1995, a new variant emerged in the region and quickly replaced the old clone, which has not been detected since 2000. The new Pacific Northwest (PNW) lineage was responsible for the first cases associated with this clone outside the Pacific Northwest region. After several introductions into the northeast coast, the new PNW clone differentiated into a highly dynamic group that continues to cause illness on the northeast coast of the United States. Surprisingly, the strains detected in Europe in 2012 diverged from this ancestral group around 2000 and have conserved genetic features present only in the old PNW lineage. Recombination was identified as the major driver of diversification, with some preliminary observations suggesting a trend toward a more specialized lifestyle, which may represent a critical element in the expansion of epidemics under scenarios of coastal warming.IMPORTANCE Vibrio parahaemolyticus and Vibrio cholerae represent the only two instances of pandemic expansions of human pathogens originating in the marine environment. However, while the current pandemic of V. cholerae emerged more than 50 years ago, the global expansion of V. parahaemolyticus is a recent phenomenon. These modern expansions provide an exceptional opportunity to study the evolutionary process of these pathogens at first hand and gain an understanding of the mechanisms shaping the epidemic dynamics of these diseases, in particular, the emergence, dispersal, and successful introduction in new regions facilitating global spreading of infections. In this study, we used genomic analysis to examine the evolutionary divergence that has occurred over the course of the most recent transcon-

Recent mixing of Vibrio parahaemolyticus populations

“…Differences in species level or genus level composition between locations are as likely to reflect environmental heterogeneity as dispersal, making the patterns difficult to interpret. Recent spread of microbes between continents has been documented for lineages that cause pathogenic infection of humans, including notorious clonal groups within Vibrio parahaemolyticus and Vibrio cholerae [5-8]. However, these lineages are unusual in using humans as vectors, which might facilitate long-range dispersal as in the case of the Haitian cholera outbreak [9].…”

Epidemic Dynamics ofVibrio parahaemolyticusIllness in a Hotspot of Disease Emergence, Galicia, Spain

“…This particular population structure suggests the existence of a lineage replacement in the PNW coast and western Canada, where only strains belonging to the second cluster were identified from 2005 onward. Surprisingly, we unequivocally identified the strains in the 2012 Galicia outbreak as belonging to the first cluster composed of strains extinct in their original location along the PNW coast, which suggests an early introduction of these strains into waters of Galicia and Europe ( 14 ). Furthermore, we identified a single strain from Canada as closely related to the genomes from the Galician strains with a minimum difference of 20–22 SNPs in an alignment of 3,310,986 bp, whereas variations among genomes of the ST36 strains from Galicia were 0–19 SNPs.…”

“…However, we cannot rule out the introduction of foreign mollusks into the marine water of Galicia as a possible source of new variants of pathogenic Vibrio bacteria from disparate and remote sources because of the magnitude of the shellfish trade in the region; the importation of shellfish from other geographic areas is a common practice to supply the high demand for products. A recent study analyzing the population structure and evolution of the ST36 clone suggests that the importation of clams from the PNW to Spain circa 2000 is the probable source of ST36 strains ( 14 ). Moreover, 2 other recent studies tracking the routes of introduction of the Manila clam from its original place of distribution in the Indo-Pacific region to Europe has also linked the origin of clam populations introduced in Spain to the PNW of the United States (area of endemicity of ST36 populations) during the importations of clams in the mid- and late 1990s ( 21 , 22 ).…”

“…The concomitant introduction of foreign Vibrio variants with a significant warming trend in the region, coupled with the consumption of locally produced shellfish in the region, may be major contributing factors for the emergence of infections in Galicia. Parallel circumstances may also drive disease emergence in other areas of the world with similar environmental conditions, such as the Pacific Northwest ( 24 , 25 ) and the Atlantic Northeast ( 14 , 26 ) in the United States or the south of Chile ( 27 ). In these areas.…”

Adaptation to temperature stress by Vibrio fischeri facilitates this microbe's symbiosis with the Hawaiian bobtail squid ( Euprymna scolopes )

“…These characteristics greatly facilitate the Vibrionaceae's ability to disseminate throughout the world's oceans, a feature that will be immensely heightened with climate change (Martinez-Urtaza et al 2016;Racault et al 2016). Even single strains have been able to cross entire ocean basins (González-Escalona et al 2015;Martinez-Urtaza et al 2017).…”