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Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes
Bacteriophages from the Inoviridae family (inoviruses) are characterized by their unique morphology, genome content and infection cycle. One of the most striking features of inoviruses is their ability to establish a chronic infection whereby the viral genome resides within the cell in either an exc...
Autores principales: | , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6813254/ https://www.ncbi.nlm.nih.gov/pubmed/31332386 http://dx.doi.org/10.1038/s41564-019-0510-x |
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author | Roux, Simon Krupovic, Mart Daly, Rebecca A. Borges, Adair L. Nayfach, Stephen Schulz, Frederik Sharrar, Allison Matheus Carnevali, Paula B. Cheng, Jan-Fang Ivanova, Natalia N. Bondy-Denomy, Joseph Wrighton, Kelly C. Woyke, Tanja Visel, Axel Kyrpides, Nikos C. Eloe-Fadrosh, Emiley A. |
author_facet | Roux, Simon Krupovic, Mart Daly, Rebecca A. Borges, Adair L. Nayfach, Stephen Schulz, Frederik Sharrar, Allison Matheus Carnevali, Paula B. Cheng, Jan-Fang Ivanova, Natalia N. Bondy-Denomy, Joseph Wrighton, Kelly C. Woyke, Tanja Visel, Axel Kyrpides, Nikos C. Eloe-Fadrosh, Emiley A. |
author_sort | Roux, Simon |
collection | PubMed |
description | Bacteriophages from the Inoviridae family (inoviruses) are characterized by their unique morphology, genome content and infection cycle. One of the most striking features of inoviruses is their ability to establish a chronic infection whereby the viral genome resides within the cell in either an exclusively episomal state or integrated into the host chromosome and virions are continuously released without killing the host. To date, a relatively small number of inovirus isolates have been extensively studied, either for biotechnological applications, such as phage display, or because of their effect on the toxicity of known bacterial pathogens including Vibrio cholerae and Neisseria meningitidis. Here, we show that the current 56 members of the Inoviridae family represent a minute fraction of a highly diverse group of inoviruses. Using a machine learning approach leveraging a combination of marker gene and genome features, we identified 10,295 inovirus-like sequences from microbial genomes and metagenomes. Collectively, our results call for reclassification of the current Inoviridae family into a viral order including six distinct proposed families associated with nearly all bacterial phyla across virtually every ecosystem. Putative inoviruses were also detected in several archaeal genomes, suggesting that, collectively, members of this supergroup infect hosts across the domains Bacteria and Archaea. Finally, we identified an expansive diversity of inovirus-encoded toxin–antitoxin and gene expression modulation systems, alongside evidence of both synergistic (CRISPR evasion) and antagonistic (superinfection exclusion) interactions with co-infecting viruses, which we experimentally validated in a Pseudomonas model. Capturing this previously obscured component of the global virosphere may spark new avenues for microbial manipulation approaches and innovative biotechnological applications. |
format | Online Article Text |
id | pubmed-6813254 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-68132542019-10-28 Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes Roux, Simon Krupovic, Mart Daly, Rebecca A. Borges, Adair L. Nayfach, Stephen Schulz, Frederik Sharrar, Allison Matheus Carnevali, Paula B. Cheng, Jan-Fang Ivanova, Natalia N. Bondy-Denomy, Joseph Wrighton, Kelly C. Woyke, Tanja Visel, Axel Kyrpides, Nikos C. Eloe-Fadrosh, Emiley A. Nat Microbiol Article Bacteriophages from the Inoviridae family (inoviruses) are characterized by their unique morphology, genome content and infection cycle. One of the most striking features of inoviruses is their ability to establish a chronic infection whereby the viral genome resides within the cell in either an exclusively episomal state or integrated into the host chromosome and virions are continuously released without killing the host. To date, a relatively small number of inovirus isolates have been extensively studied, either for biotechnological applications, such as phage display, or because of their effect on the toxicity of known bacterial pathogens including Vibrio cholerae and Neisseria meningitidis. Here, we show that the current 56 members of the Inoviridae family represent a minute fraction of a highly diverse group of inoviruses. Using a machine learning approach leveraging a combination of marker gene and genome features, we identified 10,295 inovirus-like sequences from microbial genomes and metagenomes. Collectively, our results call for reclassification of the current Inoviridae family into a viral order including six distinct proposed families associated with nearly all bacterial phyla across virtually every ecosystem. Putative inoviruses were also detected in several archaeal genomes, suggesting that, collectively, members of this supergroup infect hosts across the domains Bacteria and Archaea. Finally, we identified an expansive diversity of inovirus-encoded toxin–antitoxin and gene expression modulation systems, alongside evidence of both synergistic (CRISPR evasion) and antagonistic (superinfection exclusion) interactions with co-infecting viruses, which we experimentally validated in a Pseudomonas model. Capturing this previously obscured component of the global virosphere may spark new avenues for microbial manipulation approaches and innovative biotechnological applications. Nature Publishing Group UK 2019-07-22 2019 /pmc/articles/PMC6813254/ /pubmed/31332386 http://dx.doi.org/10.1038/s41564-019-0510-x Text en © This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. |
spellingShingle | Article Roux, Simon Krupovic, Mart Daly, Rebecca A. Borges, Adair L. Nayfach, Stephen Schulz, Frederik Sharrar, Allison Matheus Carnevali, Paula B. Cheng, Jan-Fang Ivanova, Natalia N. Bondy-Denomy, Joseph Wrighton, Kelly C. Woyke, Tanja Visel, Axel Kyrpides, Nikos C. Eloe-Fadrosh, Emiley A. Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes |
title | Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes |
title_full | Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes |
title_fullStr | Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes |
title_full_unstemmed | Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes |
title_short | Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes |
title_sort | cryptic inoviruses revealed as pervasive in bacteria and archaea across earth’s biomes |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6813254/ https://www.ncbi.nlm.nih.gov/pubmed/31332386 http://dx.doi.org/10.1038/s41564-019-0510-x |
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