Parallel evolution of two clades of a major Atlantic endemic<i>Vibrio parahaemolyticus</i>pathogen lineage by independent acquisition of related pathogenicity islands

Xu, Feng; González-Escalona, Narjol; Drees, Kevin P.; Sebra, Robert; Cooper, Vaughn S.; Jones, Stephen H.; Whistler, Cheryl A.

doi:10.1101/155234

Cited by 2 publications

(5 citation statements)

References 54 publications

(1 reference statement)

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“…S6). Notable among these are emergent pathogenic lineages including ST43 and the prevalent Atlantic endemic ST631 lineage that has caused illnesses along the North American Atlantic coast (4), the pandemic complex (ST3) and a diverse and far-spreading Asian lineage that is now an Atlantic resident (ST8).…”

Section: Resultsmentioning

confidence: 99%

“…The sequence types were determined using the SRST2 pipeline (82) or using assemblies (83) referencing https://pubmlst.org/vparahaemolyticus/ (84). Reference inoviruses were extracted from genomes sequenced using the Pacific Biosciences RSII technology and with Illumina short read error correction as described (4).…”

Section: Methodsmentioning

confidence: 99%

“…Cases of V. parahaemolyticus, the leading cause of bacterial seafood-borne gastroenteritis world-wide, recently increased along the United States (US) Atlantic coast (1)(2)(3). This rise in illnesses was tied to warming ocean temperatures, a growing aquaculture industry, and the emergence of endemic pathogens (3)(4)(5)(6). But incursion of a Pacific endemic lineage called sequence type (ST) 36 into the Atlantic is arguably the most important driver of this epidemiological shift (3,5,7).…”

Section: Introductionmentioning

confidence: 99%

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

Means

Marcinkiewicz

Foxall

et al. 2023

Preprint

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The epidemiology ofVibrio parahaemolyticus, the leading cause of seafood-borne gastroenteritis world-wide, dramatically changed in the United States following the translocation and establishment of a Pacific lineage ofV. parahaemolyticus, sequence type (ST) 36, into the Atlantic. In this study we used phylogeography based on traceback locations and comparative genomics to identify features that promoted evolution, dispersal, and competitive dominance of ST36. This revealed a striking shuffling of filamentous prophage in the familyInoviridae(inoviruses), including loss of a prophage that had been maintained for decades, accompanied modern diversification and competitive replacement of 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 diagnostic inoviruses while other subpopulations that apparently declined did not. Broader surveys indicate inoviruses are common and active among the global population ofV. parahaemolyticusand though parallel inovirus replacements, such as in ST36, appear infrequent, they are notable in pathogenic lineages that dispersed. Importance: An understanding of the processes that contribute to emergence of pathogens from environmental reservoirs is critical as changing climate precipitates pathogen evolution and population expansion. Phylogeographic analysis ofVibrio parahaemolyticushosts combined with analysis of theirInoviridaephage 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.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Means

Marcinkiewicz

Foxall

et al. 2023

Preprint

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“…Interestingly, the WU75_11415 homologue of non‐O1/non‐O139 V. cholerae AM‐19226 was identified as a novel bona fide T3SS effector (Alam et al ., 2011; Seward et al ., 2015) and has been classified as an ‘accessory T3SS effector’, which might be important, but not indispensable for enterotoxicity (Matsuda et al ., 2020). To understand its position within V. parahaemolyticus T3SS2β, the gene WU75_11415 was aligned with the pathogenicity island region of V. parahaemolyticus strain TH3996 (Vp PAI TH3996 , also called trh VPI or VPaIβ) (Xu et al ., 2017). This comparison revealed that WU75_11415 was 99% identical to the ORF RPI26 of V. parahaemolyticus TH3996 and was positioned flanking the core T3SS2 region, between the trh ‐ ureR ‐ nik ‐ ure gene cluster and T3SS apparatus genes (Supporting Information Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Unique putative T3SS effectors are present in trh containing V. parahaemolyticus To find out the differential genes between tdh-and trhpathotypes, we compared the genomes of tdh + trh À isolates with that of tdh À trh + and tdh + trh + strains. The pathotypes tdh À trh + and tdh + trh + were considered together in the analysis as the pathogenicity island, VPaIγ harbouring T3SS2 of tdh + trh + strains is believed to be a derivative of VPaIβ of tdh À trh + isolates (Xu et al, 2017). The analysis revealed 215 genes found only in the tdh + trh À pathotype, and 67 genes exclusive to tdh À trh + and tdh + trh + isolates (LS-BSR value ≥0.8; Supporting Information Table S6).…”

Section: Environmental Isolates Of V Parahaemolyticus Contain a Cellu...mentioning

confidence: 99%

Genomic attributes differ between Vibrio parahaemolyticus environmental and clinical isolates including pathotypes

Prabhakaran

Patel

Chandrika

et al. 2021

Environ Microbiol Rep

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Summary Vibrio parahaemolyticus is a marine bacterium and causes opportunistic gastroenteritis in humans. Clinical strains of V. parahaemolyticus contain haemolysin and type III secretion systems (T3SS) that define their pathotype. A growing number of strains isolated recently from the environment have acquired these virulence genes constituting a pool of potential pathogens. This study used comparative genomics to identify genetic factors that delineate environmental and clinical V. parahaemolyticus population and understand the similarities and differences between the T3SS2 phylotypes. The comparative analysis revealed the presence of a cluster of genes belonging to bacterial cellulose synthesis (bcs) in isolates of environmental origin. This cluster, previously unreported in V. parahaemolyticus, exhibit significant similarity to that of Aliivibrio fischeri, and might dictate a potentially new mechanism of its environmental adaptation and persistence. The study also identified many genes predicted in silico to be T3SS effectors that are unique to T3SS2β of tdh−trh+ and tdh+trh+ pathotype and having no identifiable homologue in tdh+trh− T3SS2α. Overall, these findings highlight the importance of understanding the genes and strategies V. parahaemolyticus utilize for the myriad interactions with its hosts, either marine invertebrates or humans.

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Parallel evolution of two clades of a major Atlantic endemicVibrio parahaemolyticuspathogen lineage by independent acquisition of related pathogenicity islands

Cited by 2 publications

References 54 publications

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

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

Genomic attributes differ between Vibrio parahaemolyticus environmental and clinical isolates including pathotypes

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