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

Publisher: BioMed Central Country of Publication: England NLM ID: 100965258 Publication Model: Electronic Cited Medium: Internet ISSN: 1471-2164 (Electronic) Linking ISSN: 14712164 NLM ISO Abbreviation: BMC Genomics Subsets: MEDLINE

Original Publication: London : BioMed Central, [2000-

Virulence Factors*/genetics ; ATP-Binding Cassette Transporters*; Mammals ; Phylogeny ; Firmicutes ; Virulence/genetics ; Clostridiales ; Animals

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.
(© 2023. BioMed Central Ltd., part of Springer Nature.)

Nucleic Acids Res. 2013 Jul;41(Web Server issue):W29-33. (PMID: 23609542)
Microbiol Spectr. 2019 May;7(3):. (PMID: 31172913)
ISME J. 2016 Nov;10(11):2744-2754. (PMID: 27015004)
Nat Biotechnol. 2019 May;37(5):540-546. (PMID: 30936562)
Nucleic Acids Res. 2005 Jan 1;33(Database issue):D325-8. (PMID: 15608208)
Curr Protoc Bioinformatics. 2013 Jun;Chapter 3:3.1.1-3.1.8. (PMID: 23749753)
Front Cell Infect Microbiol. 2018 Aug 07;8:253. (PMID: 30131942)
PLoS Comput Biol. 2020 Jun 26;16(6):e1007981. (PMID: 32589667)
Nucleic Acids Res. 2019 Jan 8;47(D1):D309-D314. (PMID: 30418610)
Genome Biol. 2021 Sep 14;22(1):266. (PMID: 34521459)
New Microbes New Infect. 2017 Dec 29;22:24-29. (PMID: 29556405)
Front Mol Biosci. 2021 Apr 22;8:668910. (PMID: 33968993)
Infect Immun. 2021 Oct 15;89(11):e0031121. (PMID: 34370507)
BMC Vet Res. 2021 Sep 3;17(1):291. (PMID: 34479562)
Theriogenology. 2018 Jul 1;114:25-33. (PMID: 29574306)
Sci Rep. 2015 Feb 10;5:8365. (PMID: 25666585)
Nat Commun. 2018 Nov 30;9(1):5114. (PMID: 30504855)
Genome Biol Evol. 2023 Jun 1;15(6):. (PMID: 37293824)
Int J Syst Bacteriol. 1999 Oct;49 Pt 4:1429-32. (PMID: 10555322)
J Clin Microbiol. 2008 Oct;46(10):3291-5. (PMID: 18716228)
PLoS One. 2010 Jun 25;5(6):e11147. (PMID: 20593022)
Appl Environ Microbiol. 2020 Sep 1;86(18):. (PMID: 32651210)
Appl Environ Microbiol. 2015 Sep;81(18):6324-32. (PMID: 26150453)
F1000Res. 2019 Dec 23;8:2138. (PMID: 31984131)
Nucleic Acids Res. 2019 Jan 8;47(D1):D660-D665. (PMID: 30407568)
Cell Microbiol. 2010 Sep 1;12(9):1203-12. (PMID: 20642798)
Mol Biol Evol. 2021 Sep 27;38(10):4647-4654. (PMID: 34320186)
Nucleic Acids Res. 2023 Jan 6;51(D1):D678-D689. (PMID: 36350631)
Nucleic Acids Res. 2021 Jul 2;49(W1):W293-W296. (PMID: 33885785)
Metallomics. 2017 Jun 21;9(6):757-772. (PMID: 28540946)
Nat Rev Microbiol. 2005 Sep;3(9):722-32. (PMID: 16138100)
PLoS Comput Biol. 2023 Mar 2;19(3):e1010905. (PMID: 36862631)
Microbiol Resour Announc. 2019 May 30;8(22):. (PMID: 31147432)
Bioinformatics. 2018 Aug 1;34(15):2666-2669. (PMID: 29547981)
Genomics Proteomics Bioinformatics. 2022 Dec;20(6):1207-1213. (PMID: 36257484)
BMC Microbiol. 2011 Feb 21;11:36. (PMID: 21338480)
Elife. 2021 Jun 11;10:. (PMID: 34114561)
Nat Rev Microbiol. 2010 May;8(5):373-82. (PMID: 20395967)
PLoS Comput Biol. 2022 Jan 24;18(1):e1009802. (PMID: 35073327)
PLoS One. 2016 Nov 1;11(11):e0165740. (PMID: 27802303)
Front Vet Sci. 2022 Feb 11;8:756438. (PMID: 35224069)
Front Microbiol. 2021 Apr 12;12:628622. (PMID: 33912145)
Bioinformatics. 2016 Mar 15;32(6):929-31. (PMID: 26576653)
Nucleic Acids Res. 2023 Jan 6;51(D1):D418-D427. (PMID: 36350672)
Nucleic Acids Res. 2022 Jan 7;50(D1):D808-D816. (PMID: 34718713)
PLoS Pathog. 2010 Jan 08;6(1):e1000716. (PMID: 20072611)
Virulence. 2023 Dec;14(1):2186377. (PMID: 36862000)
BMC Infect Dis. 2018 Aug 14;18(1):401. (PMID: 30107836)

Accession No. 1026802 U.S. Department of Agriculture; Accession No. 1026802 U.S. Department of Agriculture; Grant FLA-VME- 00131662 CVM Research Competitive Award

Keywords: Complete genome; Dairy cow; Helcococcus ovis; Hybrid genome assembly; Nanopore; Uterine disease

0 (ATP-Binding Cassette Transporters)
0 (Virulence Factors)

Helcococcus ovis

Date Created: 20230830 Date Completed: 20230912 Latest Revision: 20231123

20250114

PMC10466703

10.1186/s12864-023-09581-1

37648976