Widespread distribution of prophage-encoded virulence factors in marine Vibrio communities

Daniel Castillo,Martin F Polz,Panos Kalatzis,Mathias Middelboe,Kathryn Kauffman,Fatima Hussain,Nanna Rørbo

doi:10.1038/s41598-018-28326-9

Daniel Castillo, Martin F Polz + Show 5 more

Open Access

https://doi.org/10.1038/s41598-018-28326-9

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Abstract

Prophages are known to encode important virulence factors in the human pathogen Vibrio cholerae. However, little is known about the occurrence and composition of prophage-encoded traits in environmental vibrios. A database of 5,674 prophage-like elements constructed from 1,874 Vibrio genome sequences, covering sixty-four species, revealed that prophage-like elements encoding possible properties such as virulence and antibiotic resistance are widely distributed among environmental vibrios, including strains classified as non-pathogenic. Moreover, we found that 45% of Vibrio species harbored a complete prophage-like element belonging to the Inoviridae family, which encode the zonula occludens toxin (Zot) previously described in the V. cholerae. Interestingly, these zot-encoding prophages were found in a variety of Vibrio strains covering both clinical and marine isolates, including strains from deep sea hydrothermal vents and deep subseafloor sediments. In addition, the observation that a spacer from the CRISPR locus in the marine fish pathogen V. anguillarum strain PF7 had 95% sequence identity with a zot gene from the Inoviridae prophage found in V. anguillarum strain PF4, suggests acquired resistance to inoviruses in this species. Altogether, our results contribute to the understanding of the role of prophages as drivers of evolution and virulence in the marine Vibrio bacteria.

Highlights

The Vibrio genus is a genetically and metabolically diverse group of heterotrophic bacteria that are ubiquitously distributed in the oceans and often accounts for a large fraction (0.5–5%) of the total bacterial community, occasionally developing massive blooms[1,2]
Prophage-associated toxins have been identified in the marine vibrios such as: V. coralliilyticus[11] and V. anguillarum[7] and V. parahaemolyticus[12], indicating that prophage-encoded virulence genes are disseminated among environmental Vibrio populations
While the ability of prophages to impact the pathogenicity of V. cholerae is well studied[8,13], little is known about the distribution and role of prophage-encoded fitness factors in a broader range of environmental Vibrio bacteria

Summary

Introduction

The Vibrio genus (vibrios) is a genetically and metabolically diverse group of heterotrophic bacteria that are ubiquitously distributed in the oceans and often accounts for a large fraction (0.5–5%) of the total bacterial community, occasionally developing massive blooms[1,2]. Prophage-associated toxins have been identified in the marine vibrios such as: V. coralliilyticus[11] and V. anguillarum[7] and V. parahaemolyticus[12], indicating that prophage-encoded virulence genes are disseminated among environmental Vibrio populations. That prophage-encoded virulence is a dynamic property of environmental vibrios Together, these studies strongly suggest that prophages in Vibrio bacteria harbor multiple and diverse genetic elements with large effects on pathogenicity and host fitness and a large potential for dissemination among the Vibrio group. While the ability of prophages to impact the pathogenicity of V. cholerae is well studied[8,13], little is known about the distribution and role of prophage-encoded fitness factors in a broader range of environmental Vibrio bacteria. Vibrio prophages and temperate phages are potentially key driving forces in niche adaptation, dissemination of virulence and emergence of disease in environmental marine Vibrio communities

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