<named-content content-type="genus-species">Dolosigranulum pigrum</named-content> Cooperation and Competition in Human Nasal Microbiota

ABSTRACT Multiple epidemiological studies identify Dolosigranulum pigrum as a candidate beneficial bacterium based on its positive association with health, including negative associations with nasal/nasopharyngeal colonization by the pathogenic species Staphylococcus aureus and Streptococcus pneumon...

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Autores principales:	Silvio D. Brugger, Sara M. Eslami, Melinda M. Pettigrew, Isabel F. Escapa, Matthew T. Henke, Yong Kong, Katherine P. Lemon
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Dolosigranulum pigrum Corynebacterium Staphylococcus aureus Streptococcus pneumoniae microbe-microbe interactions interspecies interactions Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5a2a7dfe6af344c7b7ac6126ff5a23e3
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spelling	oai:doaj.org-article:5a2a7dfe6af344c7b7ac6126ff5a23e32021-11-15T15:30:58Z<named-content content-type="genus-species">Dolosigranulum pigrum</named-content> Cooperation and Competition in Human Nasal Microbiota10.1128/mSphere.00852-202379-5042https://doaj.org/article/5a2a7dfe6af344c7b7ac6126ff5a23e32020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00852-20https://doaj.org/toc/2379-5042ABSTRACT Multiple epidemiological studies identify Dolosigranulum pigrum as a candidate beneficial bacterium based on its positive association with health, including negative associations with nasal/nasopharyngeal colonization by the pathogenic species Staphylococcus aureus and Streptococcus pneumoniae. Using a multipronged approach to gain new insights into D. pigrum function, we observed phenotypic interactions and predictions of genomic capacity that support the idea of a role for microbe-microbe interactions involving D. pigrum in shaping the composition of human nasal microbiota. We identified in vivo community-level and in vitro phenotypic cooperation by specific nasal Corynebacterium species. Also, D. pigrum inhibited S. aureus growth in vitro, whereas robust inhibition of S. pneumoniae required both D. pigrum and a nasal Corynebacterium together. D. pigrum l-lactic acid production was insufficient to account for these inhibitions. Genomic analysis of 11 strains revealed that D. pigrum has a small genome (average 1.86 Mb) and multiple predicted auxotrophies consistent with D. pigrum relying on its human host and on cocolonizing bacteria for key nutrients. Further, the accessory genome of D. pigrum harbored a diverse repertoire of biosynthetic gene clusters, some of which may have a role in microbe-microbe interactions. These new insights into D. pigrum’s functions advance the field from compositional analysis to genomic and phenotypic experimentation on a potentially beneficial bacterial resident of the human upper respiratory tract and lay the foundation for future animal and clinical experiments. IMPORTANCE Staphylococcus aureus and Streptococcus pneumoniae infections cause significant morbidity and mortality in humans. For both, nasal colonization is a risk factor for infection. Studies of nasal microbiota identify Dolosigranulum pigrum as a benign bacterium present when adults are free of S. aureus or when children are free of S. pneumoniae. Here, we validated these in vivo associations with functional assays. We found that D. pigrum inhibited S. aureus in vitro and, together with a specific nasal Corynebacterium species, also inhibited S. pneumoniae. Furthermore, genomic analysis of D. pigrum indicated that it must obtain key nutrients from other nasal bacteria or from humans. These phenotypic interactions support the idea of a role for microbe-microbe interactions in shaping the composition of human nasal microbiota and implicate D. pigrum as a mutualist of humans. These findings support the feasibility of future development of microbe-targeted interventions to reshape nasal microbiota composition to exclude S. aureus and/or S. pneumoniae.Silvio D. BruggerSara M. EslamiMelinda M. PettigrewIsabel F. EscapaMatthew T. HenkeYong KongKatherine P. LemonAmerican Society for MicrobiologyarticleDolosigranulum pigrumCorynebacteriumStaphylococcus aureusStreptococcus pneumoniaemicrobe-microbe interactionsinterspecies interactionsMicrobiologyQR1-502ENmSphere, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Dolosigranulum pigrum Corynebacterium Staphylococcus aureus Streptococcus pneumoniae microbe-microbe interactions interspecies interactions Microbiology QR1-502
spellingShingle	Dolosigranulum pigrum Corynebacterium Staphylococcus aureus Streptococcus pneumoniae microbe-microbe interactions interspecies interactions Microbiology QR1-502 Silvio D. Brugger Sara M. Eslami Melinda M. Pettigrew Isabel F. Escapa Matthew T. Henke Yong Kong Katherine P. Lemon <named-content content-type="genus-species">Dolosigranulum pigrum</named-content> Cooperation and Competition in Human Nasal Microbiota
description	ABSTRACT Multiple epidemiological studies identify Dolosigranulum pigrum as a candidate beneficial bacterium based on its positive association with health, including negative associations with nasal/nasopharyngeal colonization by the pathogenic species Staphylococcus aureus and Streptococcus pneumoniae. Using a multipronged approach to gain new insights into D. pigrum function, we observed phenotypic interactions and predictions of genomic capacity that support the idea of a role for microbe-microbe interactions involving D. pigrum in shaping the composition of human nasal microbiota. We identified in vivo community-level and in vitro phenotypic cooperation by specific nasal Corynebacterium species. Also, D. pigrum inhibited S. aureus growth in vitro, whereas robust inhibition of S. pneumoniae required both D. pigrum and a nasal Corynebacterium together. D. pigrum l-lactic acid production was insufficient to account for these inhibitions. Genomic analysis of 11 strains revealed that D. pigrum has a small genome (average 1.86 Mb) and multiple predicted auxotrophies consistent with D. pigrum relying on its human host and on cocolonizing bacteria for key nutrients. Further, the accessory genome of D. pigrum harbored a diverse repertoire of biosynthetic gene clusters, some of which may have a role in microbe-microbe interactions. These new insights into D. pigrum’s functions advance the field from compositional analysis to genomic and phenotypic experimentation on a potentially beneficial bacterial resident of the human upper respiratory tract and lay the foundation for future animal and clinical experiments. IMPORTANCE Staphylococcus aureus and Streptococcus pneumoniae infections cause significant morbidity and mortality in humans. For both, nasal colonization is a risk factor for infection. Studies of nasal microbiota identify Dolosigranulum pigrum as a benign bacterium present when adults are free of S. aureus or when children are free of S. pneumoniae. Here, we validated these in vivo associations with functional assays. We found that D. pigrum inhibited S. aureus in vitro and, together with a specific nasal Corynebacterium species, also inhibited S. pneumoniae. Furthermore, genomic analysis of D. pigrum indicated that it must obtain key nutrients from other nasal bacteria or from humans. These phenotypic interactions support the idea of a role for microbe-microbe interactions in shaping the composition of human nasal microbiota and implicate D. pigrum as a mutualist of humans. These findings support the feasibility of future development of microbe-targeted interventions to reshape nasal microbiota composition to exclude S. aureus and/or S. pneumoniae.
format	article
author	Silvio D. Brugger Sara M. Eslami Melinda M. Pettigrew Isabel F. Escapa Matthew T. Henke Yong Kong Katherine P. Lemon
author_facet	Silvio D. Brugger Sara M. Eslami Melinda M. Pettigrew Isabel F. Escapa Matthew T. Henke Yong Kong Katherine P. Lemon
author_sort	Silvio D. Brugger
title	<named-content content-type="genus-species">Dolosigranulum pigrum</named-content> Cooperation and Competition in Human Nasal Microbiota
title_short	<named-content content-type="genus-species">Dolosigranulum pigrum</named-content> Cooperation and Competition in Human Nasal Microbiota
title_full	<named-content content-type="genus-species">Dolosigranulum pigrum</named-content> Cooperation and Competition in Human Nasal Microbiota
title_fullStr	<named-content content-type="genus-species">Dolosigranulum pigrum</named-content> Cooperation and Competition in Human Nasal Microbiota
title_full_unstemmed	<named-content content-type="genus-species">Dolosigranulum pigrum</named-content> Cooperation and Competition in Human Nasal Microbiota
title_sort	<named-content content-type="genus-species">dolosigranulum pigrum</named-content> cooperation and competition in human nasal microbiota
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/5a2a7dfe6af344c7b7ac6126ff5a23e3
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<named-content content-type="genus-species">Dolosigranulum pigrum</named-content> Cooperation and Competition in Human Nasal Microbiota

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