Highly Variable <named-content content-type="genus-species">Streptococcus oralis</named-content> Strains Are Common among Viridans Streptococci Isolated from Primates

ABSTRACT Viridans streptococci were obtained from primates (great apes, rhesus monkeys, and ring-tailed lemurs) held in captivity, as well as from free-living animals (chimpanzees and lemurs) for whom contact with humans is highly restricted. Isolates represented a variety of viridans streptococci,...

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Autores principales:	Dalia Denapaite, Martin Rieger, Sophie Köndgen, Reinhold Brückner, Irma Ochigava, Peter Kappeler, Kerstin Mätz-Rensing, Fabian Leendertz, Regine Hakenbeck
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Streptococcus oralis horizontal gene transfer primates teichoic acid viridans streptococci virulence factors Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2e48d24f9def4c6fb36270a25be8c15a
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spelling	oai:doaj.org-article:2e48d24f9def4c6fb36270a25be8c15a2021-11-15T15:21:22ZHighly Variable <named-content content-type="genus-species">Streptococcus oralis</named-content> Strains Are Common among Viridans Streptococci Isolated from Primates10.1128/mSphere.00041-152379-5042https://doaj.org/article/2e48d24f9def4c6fb36270a25be8c15a2016-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00041-15https://doaj.org/toc/2379-5042ABSTRACT Viridans streptococci were obtained from primates (great apes, rhesus monkeys, and ring-tailed lemurs) held in captivity, as well as from free-living animals (chimpanzees and lemurs) for whom contact with humans is highly restricted. Isolates represented a variety of viridans streptococci, including unknown species. Streptococcus oralis was frequently isolated from samples from great apes. Genotypic methods revealed that most of the strains clustered on separate lineages outside the main cluster of human S. oralis strains. This suggests that S. oralis is part of the commensal flora in higher primates and evolved prior to humans. Many genes described as virulence factors in Streptococcus pneumoniae were present also in other viridans streptococcal genomes. Unlike in S. pneumoniae, clustered regularly interspaced short palindromic repeat (CRISPR)–CRISPR-associated protein (Cas) gene clusters were common among viridans streptococci, and many S. oralis strains were type PI-2 (pilus islet 2) variants. S. oralis displayed a remarkable diversity of genes involved in the biosynthesis of peptidoglycan (penicillin-binding proteins and MurMN) and choline-containing teichoic acid. The small noncoding cia-dependent small RNAs (csRNAs) controlled by the response regulator CiaR might contribute to the genomic diversity, since we observed novel genomic islands between duplicated csRNAs, variably present in some isolates. All S. oralis genomes contained a β-N-acetyl-hexosaminidase gene absent in S. pneumoniae, which in contrast frequently harbors the neuraminidases NanB/C, which are absent in S. oralis. The identification of S. oralis-specific genes will help us to understand their adaptation to diverse habitats. IMPORTANCE Streptococcus pneumoniae is a rare example of a human-pathogenic bacterium among viridans streptococci, which consist of commensal symbionts, such as the close relatives Streptococcus mitis and S. oralis. We have shown that S. oralis can frequently be isolated from primates and a variety of other viridans streptococci as well. Genes and genomic islands which are known pneumococcal virulence factors are present in S. oralis and S. mitis, documenting the widespread occurrence of these compounds, which encode surface and secreted proteins. The frequent occurrence of CRISP-Cas gene clusters and a surprising variation of a set of small noncoding RNAs are factors to be considered in future research to further our understanding of mechanisms involved in the genomic diversity driven by horizontal gene transfer among viridans streptococci.Dalia DenapaiteMartin RiegerSophie KöndgenReinhold BrücknerIrma OchigavaPeter KappelerKerstin Mätz-RensingFabian LeendertzRegine HakenbeckAmerican Society for MicrobiologyarticleStreptococcus oralishorizontal gene transferprimatesteichoic acidviridans streptococcivirulence factorsMicrobiologyQR1-502ENmSphere, Vol 1, Iss 2 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Streptococcus oralis horizontal gene transfer primates teichoic acid viridans streptococci virulence factors Microbiology QR1-502
spellingShingle	Streptococcus oralis horizontal gene transfer primates teichoic acid viridans streptococci virulence factors Microbiology QR1-502 Dalia Denapaite Martin Rieger Sophie Köndgen Reinhold Brückner Irma Ochigava Peter Kappeler Kerstin Mätz-Rensing Fabian Leendertz Regine Hakenbeck Highly Variable <named-content content-type="genus-species">Streptococcus oralis</named-content> Strains Are Common among Viridans Streptococci Isolated from Primates
description	ABSTRACT Viridans streptococci were obtained from primates (great apes, rhesus monkeys, and ring-tailed lemurs) held in captivity, as well as from free-living animals (chimpanzees and lemurs) for whom contact with humans is highly restricted. Isolates represented a variety of viridans streptococci, including unknown species. Streptococcus oralis was frequently isolated from samples from great apes. Genotypic methods revealed that most of the strains clustered on separate lineages outside the main cluster of human S. oralis strains. This suggests that S. oralis is part of the commensal flora in higher primates and evolved prior to humans. Many genes described as virulence factors in Streptococcus pneumoniae were present also in other viridans streptococcal genomes. Unlike in S. pneumoniae, clustered regularly interspaced short palindromic repeat (CRISPR)–CRISPR-associated protein (Cas) gene clusters were common among viridans streptococci, and many S. oralis strains were type PI-2 (pilus islet 2) variants. S. oralis displayed a remarkable diversity of genes involved in the biosynthesis of peptidoglycan (penicillin-binding proteins and MurMN) and choline-containing teichoic acid. The small noncoding cia-dependent small RNAs (csRNAs) controlled by the response regulator CiaR might contribute to the genomic diversity, since we observed novel genomic islands between duplicated csRNAs, variably present in some isolates. All S. oralis genomes contained a β-N-acetyl-hexosaminidase gene absent in S. pneumoniae, which in contrast frequently harbors the neuraminidases NanB/C, which are absent in S. oralis. The identification of S. oralis-specific genes will help us to understand their adaptation to diverse habitats. IMPORTANCE Streptococcus pneumoniae is a rare example of a human-pathogenic bacterium among viridans streptococci, which consist of commensal symbionts, such as the close relatives Streptococcus mitis and S. oralis. We have shown that S. oralis can frequently be isolated from primates and a variety of other viridans streptococci as well. Genes and genomic islands which are known pneumococcal virulence factors are present in S. oralis and S. mitis, documenting the widespread occurrence of these compounds, which encode surface and secreted proteins. The frequent occurrence of CRISP-Cas gene clusters and a surprising variation of a set of small noncoding RNAs are factors to be considered in future research to further our understanding of mechanisms involved in the genomic diversity driven by horizontal gene transfer among viridans streptococci.
format	article
author	Dalia Denapaite Martin Rieger Sophie Köndgen Reinhold Brückner Irma Ochigava Peter Kappeler Kerstin Mätz-Rensing Fabian Leendertz Regine Hakenbeck
author_facet	Dalia Denapaite Martin Rieger Sophie Köndgen Reinhold Brückner Irma Ochigava Peter Kappeler Kerstin Mätz-Rensing Fabian Leendertz Regine Hakenbeck
author_sort	Dalia Denapaite
title	Highly Variable <named-content content-type="genus-species">Streptococcus oralis</named-content> Strains Are Common among Viridans Streptococci Isolated from Primates
title_short	Highly Variable <named-content content-type="genus-species">Streptococcus oralis</named-content> Strains Are Common among Viridans Streptococci Isolated from Primates
title_full	Highly Variable <named-content content-type="genus-species">Streptococcus oralis</named-content> Strains Are Common among Viridans Streptococci Isolated from Primates
title_fullStr	Highly Variable <named-content content-type="genus-species">Streptococcus oralis</named-content> Strains Are Common among Viridans Streptococci Isolated from Primates
title_full_unstemmed	Highly Variable <named-content content-type="genus-species">Streptococcus oralis</named-content> Strains Are Common among Viridans Streptococci Isolated from Primates
title_sort	highly variable <named-content content-type="genus-species">streptococcus oralis</named-content> strains are common among viridans streptococci isolated from primates
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/2e48d24f9def4c6fb36270a25be8c15a
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Highly Variable <named-content content-type="genus-species">Streptococcus oralis</named-content> Strains Are Common among Viridans Streptococci Isolated from Primates

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