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Integrated genomic and functional analyses of human skin-associated Staphylococcus reveals extensive inter- and intra-species diversity

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 speci...

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Autores principales: Joglekar, Payal, Conlan, Sean, Lee-Lin, Shih-Queen, Deming, Clay, Kashaf, Sara Saheb, Kong, Heidi H., Segre, Julia A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10370188/
https://www.ncbi.nlm.nih.gov/pubmed/37503282
http://dx.doi.org/10.1101/2023.06.22.546190
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author Joglekar, Payal
Conlan, Sean
Lee-Lin, Shih-Queen
Deming, Clay
Kashaf, Sara Saheb
Kong, Heidi H.
Segre, Julia A.
author_facet Joglekar, Payal
Conlan, Sean
Lee-Lin, Shih-Queen
Deming, Clay
Kashaf, Sara Saheb
Kong, Heidi H.
Segre, Julia A.
author_sort Joglekar, Payal
collection PubMed
description 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 fully characterize the functional diversity of this genus within the context of the skin environment. We conducted metagenome and pan-genome analyses of isolates 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 species present in all volunteers and were detected at all body sites. Pan-genome analysis of these three species revealed that the genus-core was dominated by central metabolism genes. Species-specific core genes were enriched in 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.
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spelling pubmed-103701882023-07-27 Integrated genomic and functional analyses of human skin-associated Staphylococcus reveals extensive inter- and intra-species diversity Joglekar, Payal Conlan, Sean Lee-Lin, Shih-Queen Deming, Clay Kashaf, Sara Saheb Kong, Heidi H. Segre, Julia A. bioRxiv Article 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 fully characterize the functional diversity of this genus within the context of the skin environment. We conducted metagenome and pan-genome analyses of isolates 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 species present in all volunteers and were detected at all body sites. Pan-genome analysis of these three species revealed that the genus-core was dominated by central metabolism genes. Species-specific core genes were enriched in 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. Cold Spring Harbor Laboratory 2023-06-23 /pmc/articles/PMC10370188/ /pubmed/37503282 http://dx.doi.org/10.1101/2023.06.22.546190 Text en https://creativecommons.org/licenses/by/4.0/This work is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Joglekar, Payal
Conlan, Sean
Lee-Lin, Shih-Queen
Deming, Clay
Kashaf, Sara Saheb
Kong, Heidi H.
Segre, Julia A.
Integrated genomic and functional analyses of human skin-associated Staphylococcus reveals extensive inter- and intra-species diversity
title Integrated genomic and functional analyses of human skin-associated Staphylococcus reveals extensive inter- and intra-species diversity
title_full Integrated genomic and functional analyses of human skin-associated Staphylococcus reveals extensive inter- and intra-species diversity
title_fullStr Integrated genomic and functional analyses of human skin-associated Staphylococcus reveals extensive inter- and intra-species diversity
title_full_unstemmed Integrated genomic and functional analyses of human skin-associated Staphylococcus reveals extensive inter- and intra-species diversity
title_short Integrated genomic and functional analyses of human skin-associated Staphylococcus reveals extensive inter- and intra-species diversity
title_sort integrated genomic and functional analyses of human skin-associated staphylococcus reveals extensive inter- and intra-species diversity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10370188/
https://www.ncbi.nlm.nih.gov/pubmed/37503282
http://dx.doi.org/10.1101/2023.06.22.546190
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