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Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex

BACKGROUND: Ralstonia solanacearum species complex (RSSC) strains are destructive plant pathogenic bacteria and the causative agents of bacterial wilt disease, infecting over 200 plant species worldwide. In addition to chromosomal genes, their virulence is mediated by mobile genetic elements includi...

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Autores principales: Greenrod, Samuel T. E., Stoycheva, Martina, Elphinstone, John, Friman, Ville-Petri
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9535894/
https://www.ncbi.nlm.nih.gov/pubmed/36199029
http://dx.doi.org/10.1186/s12864-022-08909-7
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author Greenrod, Samuel T. E.
Stoycheva, Martina
Elphinstone, John
Friman, Ville-Petri
author_facet Greenrod, Samuel T. E.
Stoycheva, Martina
Elphinstone, John
Friman, Ville-Petri
author_sort Greenrod, Samuel T. E.
collection PubMed
description BACKGROUND: Ralstonia solanacearum species complex (RSSC) strains are destructive plant pathogenic bacteria and the causative agents of bacterial wilt disease, infecting over 200 plant species worldwide. In addition to chromosomal genes, their virulence is mediated by mobile genetic elements including integrated DNA of bacteriophages, i.e., prophages, which may carry fitness-associated auxiliary genes or modulate host gene expression. Although experimental studies have characterised several prophages that shape RSSC virulence, the global diversity, distribution, and wider functional gene content of RSSC prophages are unknown. In this study, prophages were identified in a diverse collection of 192 RSSC draft genome assemblies originating from six continents. RESULTS: Prophages were identified bioinformatically and their diversity investigated using genetic distance measures, gene content, GC, and total length. Prophage distributions were characterised using metadata on RSSC strain geographic origin and lineage classification (phylotypes), and their functional gene content was assessed by identifying putative prophage-encoded auxiliary genes. In total, 313 intact prophages were identified, forming ten genetically distinct clusters. These included six prophage clusters with similarity to the Inoviridae, Myoviridae, and Siphoviridae phage families, and four uncharacterised clusters, possibly representing novel, previously undescribed phages. The prophages had broad geographical distributions, being present across multiple continents. However, they were generally host phylogenetic lineage-specific, and overall, prophage diversity was proportional to the genetic diversity of their hosts. The prophages contained many auxiliary genes involved in metabolism and virulence of both phage and bacteria. CONCLUSIONS: Our results show that while RSSC prophages are highly diverse globally, they make lineage-specific contributions to the RSSC accessory genome, which could have resulted from shared coevolutionary history. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08909-7.
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spelling pubmed-95358942022-10-07 Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex Greenrod, Samuel T. E. Stoycheva, Martina Elphinstone, John Friman, Ville-Petri BMC Genomics Research BACKGROUND: Ralstonia solanacearum species complex (RSSC) strains are destructive plant pathogenic bacteria and the causative agents of bacterial wilt disease, infecting over 200 plant species worldwide. In addition to chromosomal genes, their virulence is mediated by mobile genetic elements including integrated DNA of bacteriophages, i.e., prophages, which may carry fitness-associated auxiliary genes or modulate host gene expression. Although experimental studies have characterised several prophages that shape RSSC virulence, the global diversity, distribution, and wider functional gene content of RSSC prophages are unknown. In this study, prophages were identified in a diverse collection of 192 RSSC draft genome assemblies originating from six continents. RESULTS: Prophages were identified bioinformatically and their diversity investigated using genetic distance measures, gene content, GC, and total length. Prophage distributions were characterised using metadata on RSSC strain geographic origin and lineage classification (phylotypes), and their functional gene content was assessed by identifying putative prophage-encoded auxiliary genes. In total, 313 intact prophages were identified, forming ten genetically distinct clusters. These included six prophage clusters with similarity to the Inoviridae, Myoviridae, and Siphoviridae phage families, and four uncharacterised clusters, possibly representing novel, previously undescribed phages. The prophages had broad geographical distributions, being present across multiple continents. However, they were generally host phylogenetic lineage-specific, and overall, prophage diversity was proportional to the genetic diversity of their hosts. The prophages contained many auxiliary genes involved in metabolism and virulence of both phage and bacteria. CONCLUSIONS: Our results show that while RSSC prophages are highly diverse globally, they make lineage-specific contributions to the RSSC accessory genome, which could have resulted from shared coevolutionary history. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08909-7. BioMed Central 2022-10-06 /pmc/articles/PMC9535894/ /pubmed/36199029 http://dx.doi.org/10.1186/s12864-022-08909-7 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Greenrod, Samuel T. E.
Stoycheva, Martina
Elphinstone, John
Friman, Ville-Petri
Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex
title Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex
title_full Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex
title_fullStr Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex
title_full_unstemmed Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex
title_short Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex
title_sort global diversity and distribution of prophages are lineage-specific within the ralstonia solanacearum species complex
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9535894/
https://www.ncbi.nlm.nih.gov/pubmed/36199029
http://dx.doi.org/10.1186/s12864-022-08909-7
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