Cargando…

Sequencing and characterization of Helcococcus ovis: a comprehensive comparative genomic analysis of virulence

BACKGROUND: Helcococcus ovis (H. ovis) is an emerging bacterial pathogen that commonly causes opportunistic respiratory, mammary, and uterine infections across mammalian hosts. This study applied long- and short-read whole genome sequencing technologies to identify virulence factors in five H. ovis...

Descripción completa

Detalles Bibliográficos
Autores principales: Cunha, Federico, Casaro, Segundo, Jones, Kristi L., Bisinotto, Rafael S., Kariyawasam, Subhashinie, Brown, Mary B., Galvão, Klibs N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10466703/
https://www.ncbi.nlm.nih.gov/pubmed/37648976
http://dx.doi.org/10.1186/s12864-023-09581-1
_version_ 1785098946508488704
author Cunha, Federico
Casaro, Segundo
Jones, Kristi L.
Bisinotto, Rafael S.
Kariyawasam, Subhashinie
Brown, Mary B.
Galvão, Klibs N.
author_facet Cunha, Federico
Casaro, Segundo
Jones, Kristi L.
Bisinotto, Rafael S.
Kariyawasam, Subhashinie
Brown, Mary B.
Galvão, Klibs N.
author_sort Cunha, Federico
collection PubMed
description BACKGROUND: Helcococcus ovis (H. ovis) is an emerging bacterial pathogen that commonly causes opportunistic respiratory, mammary, and uterine infections across mammalian hosts. This study applied long- and short-read whole genome sequencing technologies to identify virulence factors in five H. ovis isolates with low, medium, and high virulence phenotypes. RESULTS: The resulting assemblies contained one circular chromosome ranging from 1,744,566 to 1,850,083 bp in length and had a mean GC content of 27.6%. Phylogenetic and nucleotide identity analyses found low virulence strain KG38 to be part of a clade that forms an outgroup apart from the rest of the H. ovis taxon. Assembling the first complete genomes of the species revealed major genomic rearrangements in KG38. One to six prophage regions were identified in each genome. A novel pathogenicity island was found exclusively in the two high virulence strains (KG37 and KG104), along with two hypothetical transmembrane proteins designated as putative VFs. Finally, three zinc ABC transporters and three Type-II/IV secretion systems were identified as possible virulence determinants in this species. The low virulence strain KG38 has fewer intact paralogs of these operons in its genome compared to the higher virulence isolates, which strongly suggests a role in virulence. This strain is also missing four putative virulence factors (VFs) found in other isolates associated with adherence (collagen adhesin precursor), immune evasion (choline-binding protein A and a PspA-like hypothetical protein) and cell wall synthesis (glycerol-3-phosphate cytidylyltransferase). CONCLUSIONS: In this study, we assembled reference-quality complete genomes for five H. ovis strains to identify putative virulence factors. Phylogenetic analyses of H. ovis isolates revealed the presence of a clade representing a potentially novel species within the genus Helcococcus. A novel pathogenicity island and two hypothetical transmembrane proteins were found exclusively in high-virulence strains. The identification of Zinc ABC transporters and Type-II/IV secretion systems as possible virulence determinants, along with the differences in operon content between the low and high virulence isolates, strongly suggests they also play a role in the bacterium’s pathogenicity. Taken together, these findings are a valuable first step toward deciphering the pathogenesis of H. ovis infections. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09581-1.
format Online
Article
Text
id pubmed-10466703
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-104667032023-08-31 Sequencing and characterization of Helcococcus ovis: a comprehensive comparative genomic analysis of virulence Cunha, Federico Casaro, Segundo Jones, Kristi L. Bisinotto, Rafael S. Kariyawasam, Subhashinie Brown, Mary B. Galvão, Klibs N. BMC Genomics Research BACKGROUND: Helcococcus ovis (H. ovis) is an emerging bacterial pathogen that commonly causes opportunistic respiratory, mammary, and uterine infections across mammalian hosts. This study applied long- and short-read whole genome sequencing technologies to identify virulence factors in five H. ovis isolates with low, medium, and high virulence phenotypes. RESULTS: The resulting assemblies contained one circular chromosome ranging from 1,744,566 to 1,850,083 bp in length and had a mean GC content of 27.6%. Phylogenetic and nucleotide identity analyses found low virulence strain KG38 to be part of a clade that forms an outgroup apart from the rest of the H. ovis taxon. Assembling the first complete genomes of the species revealed major genomic rearrangements in KG38. One to six prophage regions were identified in each genome. A novel pathogenicity island was found exclusively in the two high virulence strains (KG37 and KG104), along with two hypothetical transmembrane proteins designated as putative VFs. Finally, three zinc ABC transporters and three Type-II/IV secretion systems were identified as possible virulence determinants in this species. The low virulence strain KG38 has fewer intact paralogs of these operons in its genome compared to the higher virulence isolates, which strongly suggests a role in virulence. This strain is also missing four putative virulence factors (VFs) found in other isolates associated with adherence (collagen adhesin precursor), immune evasion (choline-binding protein A and a PspA-like hypothetical protein) and cell wall synthesis (glycerol-3-phosphate cytidylyltransferase). CONCLUSIONS: In this study, we assembled reference-quality complete genomes for five H. ovis strains to identify putative virulence factors. Phylogenetic analyses of H. ovis isolates revealed the presence of a clade representing a potentially novel species within the genus Helcococcus. A novel pathogenicity island and two hypothetical transmembrane proteins were found exclusively in high-virulence strains. The identification of Zinc ABC transporters and Type-II/IV secretion systems as possible virulence determinants, along with the differences in operon content between the low and high virulence isolates, strongly suggests they also play a role in the bacterium’s pathogenicity. Taken together, these findings are a valuable first step toward deciphering the pathogenesis of H. ovis infections. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09581-1. BioMed Central 2023-08-30 /pmc/articles/PMC10466703/ /pubmed/37648976 http://dx.doi.org/10.1186/s12864-023-09581-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/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 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
Cunha, Federico
Casaro, Segundo
Jones, Kristi L.
Bisinotto, Rafael S.
Kariyawasam, Subhashinie
Brown, Mary B.
Galvão, Klibs N.
Sequencing and characterization of Helcococcus ovis: a comprehensive comparative genomic analysis of virulence
title Sequencing and characterization of Helcococcus ovis: a comprehensive comparative genomic analysis of virulence
title_full Sequencing and characterization of Helcococcus ovis: a comprehensive comparative genomic analysis of virulence
title_fullStr Sequencing and characterization of Helcococcus ovis: a comprehensive comparative genomic analysis of virulence
title_full_unstemmed Sequencing and characterization of Helcococcus ovis: a comprehensive comparative genomic analysis of virulence
title_short Sequencing and characterization of Helcococcus ovis: a comprehensive comparative genomic analysis of virulence
title_sort sequencing and characterization of helcococcus ovis: a comprehensive comparative genomic analysis of virulence
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10466703/
https://www.ncbi.nlm.nih.gov/pubmed/37648976
http://dx.doi.org/10.1186/s12864-023-09581-1
work_keys_str_mv AT cunhafederico sequencingandcharacterizationofhelcococcusovisacomprehensivecomparativegenomicanalysisofvirulence
AT casarosegundo sequencingandcharacterizationofhelcococcusovisacomprehensivecomparativegenomicanalysisofvirulence
AT joneskristil sequencingandcharacterizationofhelcococcusovisacomprehensivecomparativegenomicanalysisofvirulence
AT bisinottorafaels sequencingandcharacterizationofhelcococcusovisacomprehensivecomparativegenomicanalysisofvirulence
AT kariyawasamsubhashinie sequencingandcharacterizationofhelcococcusovisacomprehensivecomparativegenomicanalysisofvirulence
AT brownmaryb sequencingandcharacterizationofhelcococcusovisacomprehensivecomparativegenomicanalysisofvirulence
AT galvaoklibsn sequencingandcharacterizationofhelcococcusovisacomprehensivecomparativegenomicanalysisofvirulence