<italic toggle="yes">Propionibacterium</italic>-Produced Coproporphyrin III Induces <named-content content-type="genus-species">Staphylococcus aureus</named-content> Aggregation and Biofilm Formation

ABSTRACT The majority of bacteria detected in the nostril microbiota of most healthy adults belong to three genera: Propionibacterium, Corynebacterium, and Staphylococcus. Among these staphylococci is the medically important bacterium Staphylococcus aureus. Almost nothing is known about interspecies...

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Autores principales:	Michael S. Wollenberg, Jan Claesen, Isabel F. Escapa, Kelly L. Aldridge, Michael A. Fischbach, Katherine P. Lemon
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ad847d156c7a4f1bb2b461130ace8156
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spelling	oai:doaj.org-article:ad847d156c7a4f1bb2b461130ace81562021-11-15T15:47:22Z<italic toggle="yes">Propionibacterium</italic>-Produced Coproporphyrin III Induces <named-content content-type="genus-species">Staphylococcus aureus</named-content> Aggregation and Biofilm Formation10.1128/mBio.01286-142150-7511https://doaj.org/article/ad847d156c7a4f1bb2b461130ace81562014-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01286-14https://doaj.org/toc/2150-7511ABSTRACT The majority of bacteria detected in the nostril microbiota of most healthy adults belong to three genera: Propionibacterium, Corynebacterium, and Staphylococcus. Among these staphylococci is the medically important bacterium Staphylococcus aureus. Almost nothing is known about interspecies interactions among bacteria in the nostrils. We observed that crude extracts of cell-free conditioned medium from Propionibacterium spp. induce S. aureus aggregation in culture. Bioassay-guided fractionation implicated coproporphyrin III (CIII), the most abundant extracellular porphyrin produced by human-associated Propionibacterium spp., as a cause of S. aureus aggregation. This aggregation response depended on the CIII dose and occurred during early stationary-phase growth, and a low pH (~4 to 6) was necessary but was not sufficient for its induction. Additionally, CIII induced plasma-independent S. aureus biofilm development on an abiotic surface in multiple S. aureus strains. In strain UAMS-1, CIII stimulation of biofilm depended on sarA, a key biofilm regulator. This study is one of the first demonstrations of a small-molecule-mediated interaction among medically relevant members of the nostril microbiota and the first description of a role for CIII in bacterial interspecies interactions. Our results indicate that CIII may be an important mediator of S. aureus aggregation and/or biofilm formation in the nostril or other sites inhabited by Propionibacterium spp. and S. aureus. IMPORTANCE Very little is known about interspecies interactions among the bacteria that inhabit the adult nostril, including Staphylococcus aureus, a potential pathogen that colonizes about a quarter of adults. We demonstrated that coproporphyrin III (CIII), a diffusible small molecule excreted by nostril- and skin-associated Propionibacterium spp., induces S. aureus aggregation in a manner dependent on dose, growth phase, and pH. CIII also induces S. aureus to form a plasma-independent surface-attached biofilm. This report is the first description of a role for CIII in bacterial interspecies interactions at any human body site and a novel demonstration that nostril microbiota physiology is influenced by small-molecule-mediated interactions.Michael S. WollenbergJan ClaesenIsabel F. EscapaKelly L. AldridgeMichael A. FischbachKatherine P. LemonAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 4 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Michael S. Wollenberg Jan Claesen Isabel F. Escapa Kelly L. Aldridge Michael A. Fischbach Katherine P. Lemon <italic toggle="yes">Propionibacterium</italic>-Produced Coproporphyrin III Induces <named-content content-type="genus-species">Staphylococcus aureus</named-content> Aggregation and Biofilm Formation
description	ABSTRACT The majority of bacteria detected in the nostril microbiota of most healthy adults belong to three genera: Propionibacterium, Corynebacterium, and Staphylococcus. Among these staphylococci is the medically important bacterium Staphylococcus aureus. Almost nothing is known about interspecies interactions among bacteria in the nostrils. We observed that crude extracts of cell-free conditioned medium from Propionibacterium spp. induce S. aureus aggregation in culture. Bioassay-guided fractionation implicated coproporphyrin III (CIII), the most abundant extracellular porphyrin produced by human-associated Propionibacterium spp., as a cause of S. aureus aggregation. This aggregation response depended on the CIII dose and occurred during early stationary-phase growth, and a low pH (~4 to 6) was necessary but was not sufficient for its induction. Additionally, CIII induced plasma-independent S. aureus biofilm development on an abiotic surface in multiple S. aureus strains. In strain UAMS-1, CIII stimulation of biofilm depended on sarA, a key biofilm regulator. This study is one of the first demonstrations of a small-molecule-mediated interaction among medically relevant members of the nostril microbiota and the first description of a role for CIII in bacterial interspecies interactions. Our results indicate that CIII may be an important mediator of S. aureus aggregation and/or biofilm formation in the nostril or other sites inhabited by Propionibacterium spp. and S. aureus. IMPORTANCE Very little is known about interspecies interactions among the bacteria that inhabit the adult nostril, including Staphylococcus aureus, a potential pathogen that colonizes about a quarter of adults. We demonstrated that coproporphyrin III (CIII), a diffusible small molecule excreted by nostril- and skin-associated Propionibacterium spp., induces S. aureus aggregation in a manner dependent on dose, growth phase, and pH. CIII also induces S. aureus to form a plasma-independent surface-attached biofilm. This report is the first description of a role for CIII in bacterial interspecies interactions at any human body site and a novel demonstration that nostril microbiota physiology is influenced by small-molecule-mediated interactions.
format	article
author	Michael S. Wollenberg Jan Claesen Isabel F. Escapa Kelly L. Aldridge Michael A. Fischbach Katherine P. Lemon
author_facet	Michael S. Wollenberg Jan Claesen Isabel F. Escapa Kelly L. Aldridge Michael A. Fischbach Katherine P. Lemon
author_sort	Michael S. Wollenberg
title	<italic toggle="yes">Propionibacterium</italic>-Produced Coproporphyrin III Induces <named-content content-type="genus-species">Staphylococcus aureus</named-content> Aggregation and Biofilm Formation
title_short	<italic toggle="yes">Propionibacterium</italic>-Produced Coproporphyrin III Induces <named-content content-type="genus-species">Staphylococcus aureus</named-content> Aggregation and Biofilm Formation
title_full	<italic toggle="yes">Propionibacterium</italic>-Produced Coproporphyrin III Induces <named-content content-type="genus-species">Staphylococcus aureus</named-content> Aggregation and Biofilm Formation
title_fullStr	<italic toggle="yes">Propionibacterium</italic>-Produced Coproporphyrin III Induces <named-content content-type="genus-species">Staphylococcus aureus</named-content> Aggregation and Biofilm Formation
title_full_unstemmed	<italic toggle="yes">Propionibacterium</italic>-Produced Coproporphyrin III Induces <named-content content-type="genus-species">Staphylococcus aureus</named-content> Aggregation and Biofilm Formation
title_sort	<italic toggle="yes">propionibacterium</italic>-produced coproporphyrin iii induces <named-content content-type="genus-species">staphylococcus aureus</named-content> aggregation and biofilm formation
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/ad847d156c7a4f1bb2b461130ace8156
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<italic toggle="yes">Propionibacterium</italic>-Produced Coproporphyrin III Induces <named-content content-type="genus-species">Staphylococcus aureus</named-content> Aggregation and Biofilm Formation

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