The Human Skin Microbiome Associates with the Outcome of and Is Influenced by Bacterial Infection

ABSTRACT The influence of the skin microbiota on host susceptibility to infectious agents is largely unexplored. The skin harbors diverse bacterial species that may promote or antagonize the growth of an invading pathogen. We developed a human infection model for Haemophilus ducreyi in which human v...

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Autores principales:	Julia J. van Rensburg, Huaiying Lin, Xiang Gao, Evelyn Toh, Kate R. Fortney, Sheila Ellinger, Beth Zwickl, Diane M. Janowicz, Barry P. Katz, David E. Nelson, Qunfeng Dong, Stanley M. Spinola
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/14f27fe6aea4450db5812d4f62e2b968
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spelling	oai:doaj.org-article:14f27fe6aea4450db5812d4f62e2b9682021-11-15T15:41:31ZThe Human Skin Microbiome Associates with the Outcome of and Is Influenced by Bacterial Infection10.1128/mBio.01315-152150-7511https://doaj.org/article/14f27fe6aea4450db5812d4f62e2b9682015-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01315-15https://doaj.org/toc/2150-7511ABSTRACT The influence of the skin microbiota on host susceptibility to infectious agents is largely unexplored. The skin harbors diverse bacterial species that may promote or antagonize the growth of an invading pathogen. We developed a human infection model for Haemophilus ducreyi in which human volunteers are inoculated on the upper arm. After inoculation, papules form and either spontaneously resolve or progress to pustules. To examine the role of the skin microbiota in the outcome of H. ducreyi infection, we analyzed the microbiomes of four dose-matched pairs of “resolvers” and “pustule formers” whose inoculation sites were swabbed at multiple time points. Bacteria present on the skin were identified by amplification and pyrosequencing of 16S rRNA genes. Nonmetric multidimensional scaling (NMDS) using Bray-Curtis dissimilarity between the preinfection microbiomes of infected sites showed that sites from the same volunteer clustered together and that pustule formers segregated from resolvers (P = 0.001, permutational multivariate analysis of variance [PERMANOVA]), suggesting that the preinfection microbiomes were associated with outcome. NMDS using Bray-Curtis dissimilarity of the endpoint samples showed that the pustule sites clustered together and were significantly different than the resolved sites (P = 0.001, PERMANOVA), suggesting that the microbiomes at the endpoint differed between the two groups. In addition to H. ducreyi, pustule-forming sites had a greater abundance of Proteobacteria, Bacteroidetes, Micrococcus, Corynebacterium, Paracoccus, and Staphylococcus species, whereas resolved sites had higher levels of Actinobacteria and Propionibacterium species. These results suggest that at baseline, resolvers and pustule formers have distinct skin bacterial communities which change in response to infection and the resultant immune response. IMPORTANCE Human skin is home to a diverse community of microorganisms, collectively known as the skin microbiome. Some resident bacteria are thought to protect the skin from infection by outcompeting pathogens for resources or by priming the immune system's response to invaders. However, the influence of the skin microbiome on the susceptibility to or protection from infection has not been prospectively evaluated in humans. We characterized the skin microbiome before, during, and after experimental inoculation of the arm with Haemophilus ducreyi in matched volunteers who subsequently resolved the infection or formed abscesses. Our results suggest that the preinfection microbiomes of pustule formers and resolvers have distinct community structures which change in response to the progression of H. ducreyi infection to abscess formation.Julia J. van RensburgHuaiying LinXiang GaoEvelyn TohKate R. FortneySheila EllingerBeth ZwicklDiane M. JanowiczBarry P. KatzDavid E. NelsonQunfeng DongStanley M. SpinolaAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 5 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Julia J. van Rensburg Huaiying Lin Xiang Gao Evelyn Toh Kate R. Fortney Sheila Ellinger Beth Zwickl Diane M. Janowicz Barry P. Katz David E. Nelson Qunfeng Dong Stanley M. Spinola The Human Skin Microbiome Associates with the Outcome of and Is Influenced by Bacterial Infection
description	ABSTRACT The influence of the skin microbiota on host susceptibility to infectious agents is largely unexplored. The skin harbors diverse bacterial species that may promote or antagonize the growth of an invading pathogen. We developed a human infection model for Haemophilus ducreyi in which human volunteers are inoculated on the upper arm. After inoculation, papules form and either spontaneously resolve or progress to pustules. To examine the role of the skin microbiota in the outcome of H. ducreyi infection, we analyzed the microbiomes of four dose-matched pairs of “resolvers” and “pustule formers” whose inoculation sites were swabbed at multiple time points. Bacteria present on the skin were identified by amplification and pyrosequencing of 16S rRNA genes. Nonmetric multidimensional scaling (NMDS) using Bray-Curtis dissimilarity between the preinfection microbiomes of infected sites showed that sites from the same volunteer clustered together and that pustule formers segregated from resolvers (P = 0.001, permutational multivariate analysis of variance [PERMANOVA]), suggesting that the preinfection microbiomes were associated with outcome. NMDS using Bray-Curtis dissimilarity of the endpoint samples showed that the pustule sites clustered together and were significantly different than the resolved sites (P = 0.001, PERMANOVA), suggesting that the microbiomes at the endpoint differed between the two groups. In addition to H. ducreyi, pustule-forming sites had a greater abundance of Proteobacteria, Bacteroidetes, Micrococcus, Corynebacterium, Paracoccus, and Staphylococcus species, whereas resolved sites had higher levels of Actinobacteria and Propionibacterium species. These results suggest that at baseline, resolvers and pustule formers have distinct skin bacterial communities which change in response to infection and the resultant immune response. IMPORTANCE Human skin is home to a diverse community of microorganisms, collectively known as the skin microbiome. Some resident bacteria are thought to protect the skin from infection by outcompeting pathogens for resources or by priming the immune system's response to invaders. However, the influence of the skin microbiome on the susceptibility to or protection from infection has not been prospectively evaluated in humans. We characterized the skin microbiome before, during, and after experimental inoculation of the arm with Haemophilus ducreyi in matched volunteers who subsequently resolved the infection or formed abscesses. Our results suggest that the preinfection microbiomes of pustule formers and resolvers have distinct community structures which change in response to the progression of H. ducreyi infection to abscess formation.
format	article
author	Julia J. van Rensburg Huaiying Lin Xiang Gao Evelyn Toh Kate R. Fortney Sheila Ellinger Beth Zwickl Diane M. Janowicz Barry P. Katz David E. Nelson Qunfeng Dong Stanley M. Spinola
author_facet	Julia J. van Rensburg Huaiying Lin Xiang Gao Evelyn Toh Kate R. Fortney Sheila Ellinger Beth Zwickl Diane M. Janowicz Barry P. Katz David E. Nelson Qunfeng Dong Stanley M. Spinola
author_sort	Julia J. van Rensburg
title	The Human Skin Microbiome Associates with the Outcome of and Is Influenced by Bacterial Infection
title_short	The Human Skin Microbiome Associates with the Outcome of and Is Influenced by Bacterial Infection
title_full	The Human Skin Microbiome Associates with the Outcome of and Is Influenced by Bacterial Infection
title_fullStr	The Human Skin Microbiome Associates with the Outcome of and Is Influenced by Bacterial Infection
title_full_unstemmed	The Human Skin Microbiome Associates with the Outcome of and Is Influenced by Bacterial Infection
title_sort	human skin microbiome associates with the outcome of and is influenced by bacterial infection
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/14f27fe6aea4450db5812d4f62e2b968
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The Human Skin Microbiome Associates with the Outcome of and Is Influenced by Bacterial Infection

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