A Commensal Bacterium Promotes Virulence of an Opportunistic Pathogen via Cross-Respiration

ABSTRACT Bacteria rarely inhabit infection sites alone, instead residing in diverse, multispecies communities. Despite this fact, bacterial pathogenesis studies primarily focus on monoculture infections, overlooking how community interactions influence the course of disease. In this study, we used g...

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Autores principales:	Apollo Stacy, Derek Fleming, Richard J. Lamont, Kendra P. Rumbaugh, Marvin Whiteley
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4548db633dfc4c27a80d8f29e436450a
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spelling	oai:doaj.org-article:4548db633dfc4c27a80d8f29e436450a2021-11-15T15:50:16ZA Commensal Bacterium Promotes Virulence of an Opportunistic Pathogen via Cross-Respiration10.1128/mBio.00782-162150-7511https://doaj.org/article/4548db633dfc4c27a80d8f29e436450a2016-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00782-16https://doaj.org/toc/2150-7511ABSTRACT Bacteria rarely inhabit infection sites alone, instead residing in diverse, multispecies communities. Despite this fact, bacterial pathogenesis studies primarily focus on monoculture infections, overlooking how community interactions influence the course of disease. In this study, we used global mutant fitness profiling (transposon sequencing [Tn-seq]) to determine the genetic requirements for the pathogenic bacterium Aggregatibacter actinomycetemcomitans to cause disease when coinfecting with the commensal bacterium Streptococcus gordonii. Our results show that S. gordonii extensively alters A. actinomycetemcomitans requirements for virulence factors and biosynthetic pathways during infection. In addition, we discovered that the presence of S. gordonii enhances the bioavailability of oxygen during infection, allowing A. actinomycetemcomitans to shift from a primarily fermentative to a respiratory metabolism that enhances its growth yields and persistence. Mechanistically, respiratory metabolism enhances the fitness of A. actinomycetemcomitans in vivo by increasing ATP yields via central metabolism and creating a proton motive force. Our results reveal that, similar to cross-feeding, where one species provides another species with a nutrient, commensal bacteria can also provide electron acceptors that promote the respiratory growth and fitness of pathogens in vivo, an interaction that we term cross-respiration. IMPORTANCE Commensal bacteria can enhance the virulence of pathogens in mixed-species infections. However, knowledge of the mechanisms underlying this clinically relevant phenomenon is lacking. To bridge this gap, we comprehensively determined the genes a pathogen needs to establish coinfection with a commensal. Our findings show that the metabolism of the pathogen is low-energy-yielding in monoinfection, but in coinfection, the commensal improves the fitness of the pathogen by increasing the bioavailability of oxygen, thereby shifting the pathogen toward a high-energy-yielding metabolism. Similar to cross-feeding, this interaction, which we term cross-respiration, illustrates that commensal bacteria can provide electron acceptors that enhance the virulence of pathogens during infection.Apollo StacyDerek FlemingRichard J. LamontKendra P. RumbaughMarvin WhiteleyAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 3 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Apollo Stacy Derek Fleming Richard J. Lamont Kendra P. Rumbaugh Marvin Whiteley A Commensal Bacterium Promotes Virulence of an Opportunistic Pathogen via Cross-Respiration
description	ABSTRACT Bacteria rarely inhabit infection sites alone, instead residing in diverse, multispecies communities. Despite this fact, bacterial pathogenesis studies primarily focus on monoculture infections, overlooking how community interactions influence the course of disease. In this study, we used global mutant fitness profiling (transposon sequencing [Tn-seq]) to determine the genetic requirements for the pathogenic bacterium Aggregatibacter actinomycetemcomitans to cause disease when coinfecting with the commensal bacterium Streptococcus gordonii. Our results show that S. gordonii extensively alters A. actinomycetemcomitans requirements for virulence factors and biosynthetic pathways during infection. In addition, we discovered that the presence of S. gordonii enhances the bioavailability of oxygen during infection, allowing A. actinomycetemcomitans to shift from a primarily fermentative to a respiratory metabolism that enhances its growth yields and persistence. Mechanistically, respiratory metabolism enhances the fitness of A. actinomycetemcomitans in vivo by increasing ATP yields via central metabolism and creating a proton motive force. Our results reveal that, similar to cross-feeding, where one species provides another species with a nutrient, commensal bacteria can also provide electron acceptors that promote the respiratory growth and fitness of pathogens in vivo, an interaction that we term cross-respiration. IMPORTANCE Commensal bacteria can enhance the virulence of pathogens in mixed-species infections. However, knowledge of the mechanisms underlying this clinically relevant phenomenon is lacking. To bridge this gap, we comprehensively determined the genes a pathogen needs to establish coinfection with a commensal. Our findings show that the metabolism of the pathogen is low-energy-yielding in monoinfection, but in coinfection, the commensal improves the fitness of the pathogen by increasing the bioavailability of oxygen, thereby shifting the pathogen toward a high-energy-yielding metabolism. Similar to cross-feeding, this interaction, which we term cross-respiration, illustrates that commensal bacteria can provide electron acceptors that enhance the virulence of pathogens during infection.
format	article
author	Apollo Stacy Derek Fleming Richard J. Lamont Kendra P. Rumbaugh Marvin Whiteley
author_facet	Apollo Stacy Derek Fleming Richard J. Lamont Kendra P. Rumbaugh Marvin Whiteley
author_sort	Apollo Stacy
title	A Commensal Bacterium Promotes Virulence of an Opportunistic Pathogen via Cross-Respiration
title_short	A Commensal Bacterium Promotes Virulence of an Opportunistic Pathogen via Cross-Respiration
title_full	A Commensal Bacterium Promotes Virulence of an Opportunistic Pathogen via Cross-Respiration
title_fullStr	A Commensal Bacterium Promotes Virulence of an Opportunistic Pathogen via Cross-Respiration
title_full_unstemmed	A Commensal Bacterium Promotes Virulence of an Opportunistic Pathogen via Cross-Respiration
title_sort	commensal bacterium promotes virulence of an opportunistic pathogen via cross-respiration
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/4548db633dfc4c27a80d8f29e436450a
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A Commensal Bacterium Promotes Virulence of an Opportunistic Pathogen via Cross-Respiration

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