Commensal Oral <named-content content-type="genus-species">Rothia mucilaginosa</named-content> Produces Enterobactin, a Metal-Chelating Siderophore

ABSTRACT Next-generation sequencing studies of saliva and dental plaque from subjects in both healthy and diseased states have identified bacteria belonging to the Rothia genus as ubiquitous members of the oral microbiota. To gain a deeper understanding of molecular mechanisms underlying the chemica...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Carla C. Uranga, Pablo Arroyo, Brendan M. Duggan, William H. Gerwick, Anna Edlund
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	oral microbiota Rothia mucilaginosa enterobactin Staphylococcus aureus Streptococcus spp. Actinomyces timonensis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/fa03b0ca152f4006b59944c643a5be70
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:fa03b0ca152f4006b59944c643a5be70
record_format	dspace
spelling	oai:doaj.org-article:fa03b0ca152f4006b59944c643a5be702021-12-02T18:15:47ZCommensal Oral <named-content content-type="genus-species">Rothia mucilaginosa</named-content> Produces Enterobactin, a Metal-Chelating Siderophore10.1128/mSystems.00161-202379-5077https://doaj.org/article/fa03b0ca152f4006b59944c643a5be702020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00161-20https://doaj.org/toc/2379-5077ABSTRACT Next-generation sequencing studies of saliva and dental plaque from subjects in both healthy and diseased states have identified bacteria belonging to the Rothia genus as ubiquitous members of the oral microbiota. To gain a deeper understanding of molecular mechanisms underlying the chemical ecology of this unexplored group, we applied a genome mining approach that targets functionally important biosynthetic gene clusters (BGCs). All 45 genomes that were mined, representing Rothia mucilaginosa, Rothia dentocariosa, and Rothia aeria, harbored a catechol-siderophore-like BGC. To explore siderophore production further, we grew the previously characterized R. mucilaginosa ATCC 25296 in liquid cultures, amended with glycerol, which led to the identification of the archetype siderophore enterobactin by using tandem liquid chromatography-mass spectrometry (LC-MS/MS), high-performance liquid chromatography (HPLC), and nuclear magnetic resonance (NMR) spectroscopy. Normally attributed to pathogenic gut bacteria, R. mucilaginosa is the first commensal oral bacterium found to produce enterobactin. Cocultivation studies including R. mucilaginosa or purified enterobactin revealed that enterobactin reduced growth of certain strains of cariogenic Streptococcus mutans and pathogenic strains of Staphylococcus aureus. Commensal oral bacteria were either unaffected, reduced in growth, or induced to grow adjacent to enterobactin-producing R. mucilaginosa or the pure compound. Taken together with Rothia’s known capacity to ferment a variety of carbohydrates and amino acids, our findings of enterobactin production add an additional level of explanation to R. mucilaginosa’s prevalence in the oral cavity. Enterobactin is the strongest Fe(III) binding siderophore known, and its role in oral health requires further investigation. IMPORTANCE The communication language of the human oral microbiota is vastly underexplored. However, a few studies have shown that specialized small molecules encoded by BGCs have critical roles such as in colonization resistance against pathogens and quorum sensing. Here, by using a genome mining approach in combination with compound screening of growth cultures, we identified that the commensal oral community member R. mucilaginosa harbors a catecholate-siderophore BGC, which is responsible for the biosynthesis of enterobactin. The iron-scavenging role of enterobactin is known to have positive effects on the host’s iron pool and negative effects on host immune function; however, its role in oral health remains unexplored. R. mucilaginosa was previously identified as an abundant community member in cystic fibrosis, where bacterial iron cycling plays a major role in virulence development. With respect to iron’s broad biological importance, iron-chelating enterobactin may explain R. mucilaginosa’s colonization success in both health and disease.Carla C. UrangaPablo ArroyoBrendan M. DugganWilliam H. GerwickAnna EdlundAmerican Society for Microbiologyarticleoral microbiotaRothia mucilaginosaenterobactinStaphylococcus aureusStreptococcus spp.Actinomyces timonensisMicrobiologyQR1-502ENmSystems, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	oral microbiota Rothia mucilaginosa enterobactin Staphylococcus aureus Streptococcus spp. Actinomyces timonensis Microbiology QR1-502
spellingShingle	oral microbiota Rothia mucilaginosa enterobactin Staphylococcus aureus Streptococcus spp. Actinomyces timonensis Microbiology QR1-502 Carla C. Uranga Pablo Arroyo Brendan M. Duggan William H. Gerwick Anna Edlund Commensal Oral <named-content content-type="genus-species">Rothia mucilaginosa</named-content> Produces Enterobactin, a Metal-Chelating Siderophore
description	ABSTRACT Next-generation sequencing studies of saliva and dental plaque from subjects in both healthy and diseased states have identified bacteria belonging to the Rothia genus as ubiquitous members of the oral microbiota. To gain a deeper understanding of molecular mechanisms underlying the chemical ecology of this unexplored group, we applied a genome mining approach that targets functionally important biosynthetic gene clusters (BGCs). All 45 genomes that were mined, representing Rothia mucilaginosa, Rothia dentocariosa, and Rothia aeria, harbored a catechol-siderophore-like BGC. To explore siderophore production further, we grew the previously characterized R. mucilaginosa ATCC 25296 in liquid cultures, amended with glycerol, which led to the identification of the archetype siderophore enterobactin by using tandem liquid chromatography-mass spectrometry (LC-MS/MS), high-performance liquid chromatography (HPLC), and nuclear magnetic resonance (NMR) spectroscopy. Normally attributed to pathogenic gut bacteria, R. mucilaginosa is the first commensal oral bacterium found to produce enterobactin. Cocultivation studies including R. mucilaginosa or purified enterobactin revealed that enterobactin reduced growth of certain strains of cariogenic Streptococcus mutans and pathogenic strains of Staphylococcus aureus. Commensal oral bacteria were either unaffected, reduced in growth, or induced to grow adjacent to enterobactin-producing R. mucilaginosa or the pure compound. Taken together with Rothia’s known capacity to ferment a variety of carbohydrates and amino acids, our findings of enterobactin production add an additional level of explanation to R. mucilaginosa’s prevalence in the oral cavity. Enterobactin is the strongest Fe(III) binding siderophore known, and its role in oral health requires further investigation. IMPORTANCE The communication language of the human oral microbiota is vastly underexplored. However, a few studies have shown that specialized small molecules encoded by BGCs have critical roles such as in colonization resistance against pathogens and quorum sensing. Here, by using a genome mining approach in combination with compound screening of growth cultures, we identified that the commensal oral community member R. mucilaginosa harbors a catecholate-siderophore BGC, which is responsible for the biosynthesis of enterobactin. The iron-scavenging role of enterobactin is known to have positive effects on the host’s iron pool and negative effects on host immune function; however, its role in oral health remains unexplored. R. mucilaginosa was previously identified as an abundant community member in cystic fibrosis, where bacterial iron cycling plays a major role in virulence development. With respect to iron’s broad biological importance, iron-chelating enterobactin may explain R. mucilaginosa’s colonization success in both health and disease.
format	article
author	Carla C. Uranga Pablo Arroyo Brendan M. Duggan William H. Gerwick Anna Edlund
author_facet	Carla C. Uranga Pablo Arroyo Brendan M. Duggan William H. Gerwick Anna Edlund
author_sort	Carla C. Uranga
title	Commensal Oral <named-content content-type="genus-species">Rothia mucilaginosa</named-content> Produces Enterobactin, a Metal-Chelating Siderophore
title_short	Commensal Oral <named-content content-type="genus-species">Rothia mucilaginosa</named-content> Produces Enterobactin, a Metal-Chelating Siderophore
title_full	Commensal Oral <named-content content-type="genus-species">Rothia mucilaginosa</named-content> Produces Enterobactin, a Metal-Chelating Siderophore
title_fullStr	Commensal Oral <named-content content-type="genus-species">Rothia mucilaginosa</named-content> Produces Enterobactin, a Metal-Chelating Siderophore
title_full_unstemmed	Commensal Oral <named-content content-type="genus-species">Rothia mucilaginosa</named-content> Produces Enterobactin, a Metal-Chelating Siderophore
title_sort	commensal oral <named-content content-type="genus-species">rothia mucilaginosa</named-content> produces enterobactin, a metal-chelating siderophore
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/fa03b0ca152f4006b59944c643a5be70
work_keys_str_mv	AT carlacuranga commensaloralnamedcontentcontenttypegenusspeciesrothiamucilaginosanamedcontentproducesenterobactinametalchelatingsiderophore AT pabloarroyo commensaloralnamedcontentcontenttypegenusspeciesrothiamucilaginosanamedcontentproducesenterobactinametalchelatingsiderophore AT brendanmduggan commensaloralnamedcontentcontenttypegenusspeciesrothiamucilaginosanamedcontentproducesenterobactinametalchelatingsiderophore AT williamhgerwick commensaloralnamedcontentcontenttypegenusspeciesrothiamucilaginosanamedcontentproducesenterobactinametalchelatingsiderophore AT annaedlund commensaloralnamedcontentcontenttypegenusspeciesrothiamucilaginosanamedcontentproducesenterobactinametalchelatingsiderophore
_version_	1718378371525640192

Commensal Oral <named-content content-type="genus-species">Rothia mucilaginosa</named-content> Produces Enterobactin, a Metal-Chelating Siderophore

Ejemplares similares