Integrated genomic and functional analyses of human skin–associated
Staphylococcus
reveal extensive inter- and intra-species diversity
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Published:2023-11-13
Issue:47
Volume:120
Page:
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ISSN:0027-8424
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Container-title:Proceedings of the National Academy of Sciences
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language:en
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Short-container-title:Proc. Natl. Acad. Sci. U.S.A.
Author:
Joglekar Payal1ORCID, Conlan Sean1, Lee-Lin Shih-Queen1, Deming Clay1, Kashaf Sara Saheb1, Kong Heidi H.2ORCID, Segre Julia A.1, Barnabas Beatrice B, Black Sean, Bouffard Gerard G, Brooks Shelise Y, Crawford Juyun, Marfani Holly, Dekhtyar Lyudmila, Han Joel, Ho Shi-Ling, Legaspi Richelle, Maduro Quino L, Masiello Catherine A, McDowell Jennifer C, Montemayor Casandra, Mullikin James C, Park Morgan, Riebow Nancy L, Schandler Karen, Schmidt Brian, Sison Christina, Stantripop Sirintorn, Thomas James W, Thomas Pamela J, Vemulapalli Meghana, Young Alice C,
Affiliation:
1. Microbial Genomics Section, Translational and Functional Genomics Branch, National Human Genome Research Institute, NIH, Bethesda, MD 20892 2. Cutaneous Microbiome and Inflammation Section, National Institute of Arthritis and Musculoskeletal and Skin Diseases, NIH, Bethesda, MD 20892
Abstract
Human skin is stably colonized by a distinct microbiota that functions together with epidermal cells to maintain a protective physical barrier.
Staphylococcus
, a prominent genus of the skin microbiota, participates in colonization resistance, tissue repair, and host immune regulation in strain-specific manners. To unlock the potential of engineering skin microbial communities, we aim to characterize the diversity of this genus within the context of the skin environment. We reanalyzed an extant 16S rRNA amplicon dataset obtained from distinct body sites of healthy volunteers, providing a detailed biogeographic depiction of staphylococcal species that colonize our skin.
S. epidermidis
,
S. capitis,
and
S. hominis
were the most abundant staphylococcal species present in all volunteers and were detected at all body sites. Pan-genome analysis of isolates from these three species revealed that the genus-core was dominated by central metabolism genes. Species-restricted-core genes encoded known host colonization functions. The majority (~68%) of genes were detected only in a fraction of isolate genomes, underscoring the immense strain-specific gene diversity. Conspecific genomes grouped into phylogenetic clades, exhibiting body site preference. Each clade was enriched for distinct gene sets that are potentially involved in site tropism. Finally, we conducted gene expression studies of select isolates showing variable growth phenotypes in skin-like medium. In vitro expression revealed extensive intra- and inter-species gene expression variation, substantially expanding the functional diversification within each species. Our study provides an important resource for future ecological and translational studies to examine the role of shared and strain-specific staphylococcal genes within the skin environment.
Funder
HHS | NIH | National Human Genome Research Institute HHS | NIH | National Institute of Arthritis and Musculoskeletal and Skin Diseases
Publisher
Proceedings of the National Academy of Sciences
Subject
Multidisciplinary
Cited by
1 articles.
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1. Biogeography of the genus Staphylococci on human skin;Proceedings of the National Academy of Sciences;2023-11-29
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