Genomic and ecological attributes of marine bacteriophages encoding bacterial virulence genes

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

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Abstract

Background: Bacteriophages 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. Results: Here, 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. Conclusions: This 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.

Original languageEnglish
Article number126
Number of pages11
JournalBMC Genomics
Volume21
DOIs
Publication statusPublished - 5 Feb 2020
Externally publishedYes

Bibliographical note

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Keywords

  • Bacterial pathogenicity
  • Lysogeny
  • Marine phage
  • Virome
  • Virulence genes

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    Silveira, C. B., Coutinho, F. H., Cavalcanti, G. S., Benler, S., Doane, M. P., Dinsdale, E. A., Edwards, R. A., Francini-Filho, R. B., Thompson, C. C., Luque, A., Rohwer, F. L., & Thompson, F. (2020). Genomic and ecological attributes of marine bacteriophages encoding bacterial virulence genes. BMC Genomics, 21, [126]. https://doi.org/10.1186/s12864-020-6523-2