1887

Abstract

This study utilized pyrosequencing-based phylogenetic library results to assess bacterial communities on the hands of women in Tanzania and compared these communities with bacteria assemblages on the hands of US women. Bacterial population profiles and phylogenetically based ordinate analysis demonstrated that the bacterial communities on hands were more similar for selected populations within a country than between the two countries considered. Organisms that have commonly been identified in prior human skin microbiome studies, including members of the , and families, were highly abundant on US hands and drove the clustering of US hand microbial communities into a distinct group. The most abundant bacterial taxa on Tanzanian hands were the soil-associated and . These results help to expand human microbiome results beyond US and European populations, and the identification and abundance of soil-associated bacteria on Tanzanian hands demonstrated the important role of the environment in shaping the microbial communities on human hands.

Funding
This study was supported by the:
  • Alfred P. Sloan Foundation
  • The Yale University Global Health Initiative
  • Stanford University’s School of Earth Sciences, Center for African Studies and Woods Institute for the Environment
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2014-06-01
2024-03-29
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References

  1. Aiello A. E., Larson E. L. ( 2002). What is the evidence for a causal link between hygiene and infections. Lancet Infect Dis 2:103–110 [View Article][PubMed]
    [Google Scholar]
  2. Blaser M. J., Dominguez-Bello M. G., Contreras M., Magris M., Hidalgo G., Estrada I., Gao Z., Clemente J. C., Costello E. K., Knight R. ( 2013). Distinct cutaneous bacterial assemblages in a sampling of South American Amerindians and US residents. ISME J 7:85–95 [View Article][PubMed]
    [Google Scholar]
  3. Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., Fierer N., Peña A. G., Goodrich J. K. & other authors ( 2010). qiime allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336 [View Article][PubMed]
    [Google Scholar]
  4. Costello E. K., Lauber C. L., Hamady M., Fierer N., Gordon J. I., Knight R. ( 2009). Bacterial community variation in human body habitats across space and time. Science 326:1694–1697 [View Article][PubMed]
    [Google Scholar]
  5. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J. B., Massart S., Collini S., Pieraccini G., Lionetti P. ( 2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 107:14691–14696 [View Article][PubMed]
    [Google Scholar]
  6. DeSantis T. Z., Hugenholtz P., Larsen N., Rojas M., Brodie E. L., Keller K., Huber T., Dalevi D., Hu P., Andersen G. L. ( 2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with arb. Appl Environ Microbiol 72:5069–5072 [View Article][PubMed]
    [Google Scholar]
  7. Eckburg P. B., Bik E. M., Bernstein C. N., Purdom E., Dethlefsen L., Sargent M., Gill S. R., Nelson K. E., Relman D. A. ( 2005). Diversity of the human intestinal microbial flora. Science 308:1635–1638 [View Article][PubMed]
    [Google Scholar]
  8. Fierer N., Hamady M., Lauber C. L., Knight R. ( 2008). The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci U S A 105:17994–17999 [View Article][PubMed]
    [Google Scholar]
  9. Flores G. E., Bates S. T., Knights D., Lauber C. L., Stombaugh J., Knight R., Fierer N. ( 2011). Microbial biogeography of public restroom surfaces. PLoS ONE 6:e28132 [View Article][PubMed]
    [Google Scholar]
  10. Garrity G. M., Bell J. G., Lilburn T. ( 2001). Taxonomic outline of the Archaea and Bacteria. Bergey’s Manual of Systematic Bacteriology vol. 1, 2nd edn.21–217 Boone D. R., Castenholz R. W. New York: Springer;
    [Google Scholar]
  11. Giacomoni P. U., Mammone T., Teri M. ( 2009). Gender-linked differences in human skin. J Dermatol Sci 55:144–149 [View Article][PubMed]
    [Google Scholar]
  12. Gilbert J. A., Meyer F., Antonopoulos D., Balaji P., Brown C. T., Brown C. T., Desai N., Eisen J. A., Evers D. & other authors ( 2010). Meeting Report. The terabase metagenomic workshop and the vision of an earth microbiome project. Stand Genomic Sci 3:3 [View Article]
    [Google Scholar]
  13. Grice E. A., Kong H. H., Renaud G., Young A. C., Bouffard G. G., Blakesley R. W., Wolfsberg T. G., Turner M. L., Segre J. A. NISC Comparative Sequencing Program ( 2008). A diversity profile of the human skin microbiota. Genome Res 18:1043–1050 [View Article][PubMed]
    [Google Scholar]
  14. Grice E. A., Kong H. H., Conlan S., Deming C. B., Davis J., Young A. C., Bouffard G. G., Blakesley R. W., Murray P. R. & other authors ( 2009). Topographical and temporal diversity of the human skin microbiome. Science 324:1190–1192 [View Article][PubMed]
    [Google Scholar]
  15. Hamady M., Lozupone C., Knight R. ( 2010). Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27 [View Article][PubMed]
    [Google Scholar]
  16. Hanski I., von Hertzen L., Fyhrquist N., Koskinen K., Torppa K., Laatikainen T., Karisola P., Auvinen P., Paulin L. & other authors ( 2012). Environmental biodiversity, human microbiota, and allergy are interrelated. Proc Natl Acad Sci U S A 109:8334–8339 [View Article][PubMed]
    [Google Scholar]
  17. Hospodsky D., Qian J., Nazaroff W. W., Yamamoto N., Bibby K., Rismani-Yazdi H., Peccia J. ( 2012). Human occupancy as a source of indoor airborne bacteria. PLoS ONE 7:e34867 [View Article][PubMed]
    [Google Scholar]
  18. Hsu Y. W., Yu C. Y. ( 2010). Hand surface area estimation formula using 3D anthropometry. J Occup Environ Hyg 7:633–639 [View Article][PubMed]
    [Google Scholar]
  19. Kembel S. W., Jones E., Kline J., Northcutt D., Stenson J., Womack A. M., Bohannan B. J. M., Brown G. Z., Green J. L. ( 2012). Architectural design influences the diversity and structure of the built environment microbiome. ISME J 6:1469–1479 [View Article][PubMed]
    [Google Scholar]
  20. Kong H. H. ( 2011). Skin microbiome: genomics-based insights into the diversity and role of skin microbes. Trends Mol Med 17:320–328 [View Article][PubMed]
    [Google Scholar]
  21. Kuykendall L. D., Young J. M., Martinez-Romero E., Kerr A., Sawada H. ( 2001). Genus Rhizobium. Bergey’s Manual of Systematic Bacteriology vol. 2, 2nd edn.325–339 Staley J. T., Brenner D. J., Kreig N. R. New York: Springer;
    [Google Scholar]
  22. Lauber C. L., Hamady M., Knight R., Fierer N. ( 2009). Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120 [View Article][PubMed]
    [Google Scholar]
  23. Lazarevic V., Whiteson K., Hernandez D., François P., Schrenzel J. ( 2010). Study of inter- and intra-individual variations in the salivary microbiota. BMC Genomics 11:523 [View Article][PubMed]
    [Google Scholar]
  24. Lee Z. M.-P., Bussema C. III, Schmidt T. M. ( 2009). rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea. Nucleic Acids Res 37:DatabaseD489–D493 [View Article][PubMed]
    [Google Scholar]
  25. Leyden J. J., McGinley K. J., Nordstrom K. M., Webster G. F. ( 1987). Skin microflora. J Invest Dermatol 88:Suppl65s–72s [View Article][PubMed]
    [Google Scholar]
  26. Liu Z., Lozupone C., Hamady M., Bushman F. D., Knight R. ( 2007). Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35:e120 [View Article][PubMed]
    [Google Scholar]
  27. Logan N. A., DeVos P. ( 2001). Genus Bacillus. Bergey’s Manual of Systematic Bacteriology vol. 321–127 Vos P., Garrity G. M., Jones D., Kreig N. R., Ludwig W., Rainey F., Schleifer K.-H., Whitman W. B. New York: Springer;
    [Google Scholar]
  28. Luby S. P., Agboatwalla M., Feikin D. R., Painter J., Billhimer W., Altaf A., Hoekstra R. M. ( 2005). Effect of handwashing on child health: a randomised controlled trial. Lancet 366:225–233 [View Article][PubMed]
    [Google Scholar]
  29. Marples M. J. ( 1965). The Ecology of the Human Skin Springfield, IL: Charles C Thomas;
    [Google Scholar]
  30. Nasidze I., Li J., Quinque D., Tang K., Stoneking M. ( 2009). Global diversity in the human salivary microbiome. Genome Res 19:636–643 [View Article][PubMed]
    [Google Scholar]
  31. Nasidze I., Li J., Schroeder R., Creasey J. L., Li M., Stoneking M. ( 2011). High diversity of the saliva microbiome in Batwa Pygmies. PLoS ONE 6:e23352 [View Article][PubMed]
    [Google Scholar]
  32. Pickering A. J., Boehm A. B., Mwanjali M., Davis J. ( 2010). Efficacy of waterless hand hygiene compared with handwashing with soap: a field study in Dar es Salaam, Tanzania. Am J Trop Med Hyg 82:270–278 [View Article][PubMed]
    [Google Scholar]
  33. Pickering A. J., Julian T. R., Mamuya S., Boehm A. B., Davis J. ( 2011). Bacterial hand contamination among Tanzanian mothers varies temporally and following household activities. Trop Med Int Health 16:233–239 [View Article][PubMed]
    [Google Scholar]
  34. Price P. B. ( 1938). The bacteriology of normal skin; a new quantitative test applied to a study of the bacterial flora and the disinfectant action of mechanical cleansing. J Infect Dis 63:301–318 [View Article]
    [Google Scholar]
  35. Qian J., Hospodsky D., Yamamoto N., Nazaroff W. W., Peccia J. ( 2012). Size-resolved emission rates of airborne bacteria and fungi in an occupied classroom. Indoor Air 22:339–351 [View Article][PubMed]
    [Google Scholar]
  36. Quince C., Lanzén A., Curtis T. P., Davenport R. J., Hall N., Head I. M., Read L. F., Sloan W. T. ( 2009). Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6:639–641 [View Article][PubMed]
    [Google Scholar]
  37. Quince C., Lanzen A., Davenport R. J., Turnbaugh P. J. ( 2011). Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12:38 [View Article][PubMed]
    [Google Scholar]
  38. Sickbert-Bennett E. E., Weber D. J., Gergen-Teague M. F., Sobsey M. D., Samsa G. P., Rutala W. A. ( 2005). Comparative efficacy of hand hygiene agents in the reduction of bacteria and viruses. Am J Infect Control 33:67–77 [View Article][PubMed]
    [Google Scholar]
  39. Wang Q., Garrity G. M., Tiedje J. M., Cole J. R. ( 2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267 [View Article][PubMed]
    [Google Scholar]
  40. Yamamoto N., Bibby K., Qian J., Hospodsky D., Rismani-Yazdi H., Nazaroff W. W., Peccia J. ( 2012). Particle-size distributions and seasonal diversity of allergenic and pathogenic fungi in outdoor air. ISME J 6:1801–1811 [View Article][PubMed]
    [Google Scholar]
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