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Topographic diversity of fungal and bacterial communities in human skin

Nature volume 498, pages 367–370 (2013)Cite this article

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Abstract

Traditional culture-based methods have incompletely defined the microbial landscape of common recalcitrant human fungal skin diseases, including athlete’s foot and toenail infections. Skin protects humans from invasion by pathogenic microorganisms and provides a home for diverse commensal microbiota1. Bacterial genomic sequence data have generated novel hypotheses about species and community structures underlying human disorders2,3,4. However, microbial diversity is not limited to bacteria; microorganisms such as fungi also have major roles in microbial community stability, human health and disease5. Genomic methodologies to identify fungal species and communities have been limited compared with those that are available for bacteria6. Fungal evolution can be reconstructed with phylogenetic markers, including ribosomal RNA gene regions and other highly conserved genes7. Here we sequenced and analysed fungal communities of 14 skin sites in 10 healthy adults. Eleven core-body and arm sites were dominated by fungi of the genus Malassezia, with only species-level classifications revealing fungal-community composition differences between sites. By contrast, three foot sites—plantar heel, toenail and toe web—showed high fungal diversity. Concurrent analysis of bacterial and fungal communities demonstrated that physiologic attributes and topography of skin differentially shape these two microbial communities. These results provide a framework for future investigation of the contribution of interactions between pathogenic and commensal fungal and bacterial communities to the maintainenace of human health and to disease pathogenesis.

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Figure 1: Relative abundance of fungal genera and Malassezia species at different human skin sites.
Figure 2: Median richness of fungal and bacterial genera.
Figure 3: Forces that shape fungal and bacterial communities.
Figure 4: Clinical involvement alters shared fungal community structure.

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Accession codes

Accessions

GenBank/EMBL/DDBJ

Sequence Read Archive

Data deposits

Sequence data from this study have been submitted to GenBank/EMBL/DDBJ under accession numbers KC669797–KC675175, and the Sequence Read Archive,and can be accessed through BioProject identification no.46333. Patient and sample metadata have been deposited in the controlled-access Database of Genotypes and Phenotypes (dbGaP) under study accession phs000266.v1.p1.

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Acknowledgements

We thank J. Heitman, A. Amend, Y. Shea, M. Turner, I. Brownell and M. Udey for helpful discussions. We thank J. Fekecs for assistance with the figures. This work was supported by the US National Institutes of Health (NIH) NHGRI and NCI Intramural Research Programs, and in part by NIH grant no. 1K99AR059222 (to H.H.K.). Sequencing was funded by grants from the NIH (1UH2AR057504-01 and 4UH3AR057504-02).

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Author notes

  1. Heidi H. Kong and Julia A. Segre: These authors contributed equally to this work.

Authors and Affiliations

  1. Genetics and Molecular Biology Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, 20892, Maryland, USA

    Keisha Findley, Julia Oh, Joy Yang, Sean Conlan, Clayton Deming, Jennifer A. Meyer & Julia A. Segre

  2. Dermatology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, 20892, Maryland, USA

    Deborah Schoenfeld, Effie Nomicos & Heidi H. Kong

  3. NIH Intramural Sequencing Center, National Human Genome Research Institute, National Institutes of Health, Rockville, 20852, Maryland, USA

    Morgan Park

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Consortia

NIH Intramural Sequencing Center Comparative Sequencing Program

  • Jesse Becker
  • , Betty Benjamin
  • , Robert Blakesley
  • , Gerry Bouffard
  • , Shelise Brooks
  • , Holly Coleman
  • , Mila Dekhtyar
  • , Michael Gregory
  • , Xiaobin Guan
  • , Jyoti Gupta
  • , Joel Han
  • , April Hargrove
  • , Shi-ling Ho
  • , Taccara Johnson
  • , Richelle Legaspi
  • , Sean Lovett
  • , Quino Maduro
  • , Cathy Masiello
  • , Baishali Maskeri
  • , Jenny McDowell
  • , Casandra Montemayor
  • , James Mullikin
  • , Morgan Park
  • , Nancy Riebow
  • , Karen Schandler
  • , Brian Schmidt
  • , Christina Sison
  • , Mal Stantripop
  • , James Thomas
  • , Pam Thomas
  • , Meg Vemulapalli
  •  & Alice Young

Contributions

K.F., H.H.K. and J.A.S. designed the outline of the study. D.S. and E.N. recruited human subjects and assisted H.H.K. in sample collection for the experiment. K.F. and J.Y. assembled and curated the fungal database. J.A.M. and C.D. prepared the clinical samples for sequencing. The members of the NIH Intramural Sequencing Center Comparative Sequencing program carried out sequencing. K.F., J.O., S.C. and M.P. analysed sequence data. K.F., H.H.K. and J.A.S. drafted the manuscript with specific contributions from J.O., J.Y. and S.C. All authors read and approved the final version of the manuscript.

Corresponding authors

Correspondence to Heidi H. Kong or Julia A. Segre.

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The authors declare no competing financial interests.

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Findley, K., Oh, J., Yang, J. et al. Topographic diversity of fungal and bacterial communities in human skin. Nature 498, 367–370 (2013). https://doi.org/10.1038/nature12171

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