The human skin microbiome associates with the outcome of and is influenced by bacterial infection

Julia J. Van Rensburg, Huaiying Lin, Xiang Gao, Evelyn Toh, Kate R. Fortney, Sheila Ellinger, Beth Zwickl, Diane Janowicz, Barry Katz, David E. Nelson, Qunfeng Dong, Stanley M. Spinolaa

Research output: Contribution to journalArticle

45 Citations (Scopus)

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.

Original languageEnglish (US)
Article numbere01315-15
JournalmBio
Volume6
Issue number5
DOIs
StatePublished - 2015

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Microbiota
Bacterial Infections
Haemophilus ducreyi
Skin
Volunteers
Analysis of Variance
Paracoccus
Multivariate Analysis
Haemophilus Infections
Bacteroidetes
Propionibacterium
Micrococcus
Proteobacteria
Corynebacterium
Actinobacteria
Infection
Staphylococcus
rRNA Genes
Arm
Bacteria

ASJC Scopus subject areas

  • Microbiology
  • Virology

Cite this

Van Rensburg, J. J., Lin, H., Gao, X., Toh, E., Fortney, K. R., Ellinger, S., ... Spinolaa, S. M. (2015). The human skin microbiome associates with the outcome of and is influenced by bacterial infection. mBio, 6(5), [e01315-15]. https://doi.org/10.1128/mBio.01315-15

The human skin microbiome associates with the outcome of and is influenced by bacterial infection. / Van Rensburg, Julia J.; Lin, Huaiying; Gao, Xiang; Toh, Evelyn; Fortney, Kate R.; Ellinger, Sheila; Zwickl, Beth; Janowicz, Diane; Katz, Barry; Nelson, David E.; Dong, Qunfeng; Spinolaa, Stanley M.

In: mBio, Vol. 6, No. 5, e01315-15, 2015.

Research output: Contribution to journalArticle

Van Rensburg, JJ, Lin, H, Gao, X, Toh, E, Fortney, KR, Ellinger, S, Zwickl, B, Janowicz, D, Katz, B, Nelson, DE, Dong, Q & Spinolaa, SM 2015, 'The human skin microbiome associates with the outcome of and is influenced by bacterial infection', mBio, vol. 6, no. 5, e01315-15. https://doi.org/10.1128/mBio.01315-15
Van Rensburg JJ, Lin H, Gao X, Toh E, Fortney KR, Ellinger S et al. The human skin microbiome associates with the outcome of and is influenced by bacterial infection. mBio. 2015;6(5). e01315-15. https://doi.org/10.1128/mBio.01315-15
Van Rensburg, Julia J. ; Lin, Huaiying ; Gao, Xiang ; Toh, Evelyn ; Fortney, Kate R. ; Ellinger, Sheila ; Zwickl, Beth ; Janowicz, Diane ; Katz, Barry ; Nelson, David E. ; Dong, Qunfeng ; Spinolaa, Stanley M. / The human skin microbiome associates with the outcome of and is influenced by bacterial infection. In: mBio. 2015 ; Vol. 6, No. 5.
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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.",
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