Genomic and ecological attributes of marine bacteriophages encoding bacterial virulence genes

Cynthia B Silveira,Cristiane C Thompson,Robert A Edwards,Sean Benler,Giselle S Cavalcanti,Forest L Rohwer,Fabiano Thompson,Michael P Doane,Elizabeth A Dinsdale,Felipe H Coutinho,Antoni Luque,Ronaldo B Francini-Filho

doi:10.1186/s12864-020-6523-2

Abstract

BackgroundBacteriophages encode genes that modify bacterial functions during infection. The acquisition of phage-encoded virulence genes is a major mechanism for the rise of bacterial pathogens. In coral reefs, high bacterial density and lysogeny has been proposed to exacerbate reef decline through the transfer of phage-encoded virulence genes. However, the functions and distribution of these genes in phage virions on the reef remain unknown.ResultsHere, over 28,000 assembled viral genomes from the free viral community in Atlantic and Pacific Ocean coral reefs were queried against a curated database of virulence genes. The diversity of virulence genes encoded in the viral genomes was tested for relationships with host taxonomy and bacterial density in the environment. These analyses showed that bacterial density predicted the profile of virulence genes encoded by phages. The Shannon diversity of virulence-encoding phages was negatively related with bacterial density, leading to dominance of fewer genes at high bacterial abundances. A statistical learning analysis showed that reefs with high microbial density were enriched in viruses encoding genes enabling bacterial recognition and invasion of metazoan epithelium. Over 60% of phages could not have their hosts identified due to limitations of host prediction tools; for those which hosts were identified, host taxonomy was not an indicator of the presence of virulence genes.ConclusionsThis study described bacterial virulence factors encoded in the genomes of bacteriophages at the community level. The results showed that the increase in microbial densities that occurs during coral reef degradation is associated with a change in the genomic repertoire of bacteriophages, specifically in the diversity and distribution of bacterial virulence genes. This suggests that phages are implicated in the rise of pathogens in disturbed marine ecosystems.

Highlights

Bacteriophages encode genes that modify bacterial functions during infection
Bacterial virulence genes are often carried by Silveira et al BMC Genomics (2020) 21:126 temperate phages, and lysogenic conversion is a major mechanism for the emergence of pathogens [13]
There was only marginal evidence for a role of host taxonomy in virulence gene distribution. These findings indicate that phages represent a reservoir of bacterial virulence factors in marine environments that contributes to the rise of pathogens during microbialization

Summary

Introduction

Bacteriophages encode genes that modify bacterial functions during infection. The acquisition of phageencoded virulence genes is a major mechanism for the rise of bacterial pathogens. The CTX toxin in V. cholera is a canonical example of phage-encoded pathogenicity through the direct acquisition of a toxicity function, and through the regulation of the global bacterial transcriptome increasing the pathogen’s fitness in the animal-associated environment [15]. Prophages inserted in the genome of the coral pathogen Vibrio corallilyticus show high nucleotide sequence identity and similar gene organization with virulence gene-encoding V. cholerae phages, suggesting that lysogenic conversion cause coral disease [16, 17]. These studies suggest that phage-mediated bacterial virulence contribute to pathogenicity in many marine diseases. A community-level analysis of phage-encoded virulence genes in marine environments is still missing

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Discussion

Conclusion