Microbial Sequencing Analyses Suggest the Presence of a Fecal Veneer on Indoor Climbing Wall Holds

Current Microbiology volume 69, pages681–689(2014)Cite this article

Abstract

Artificial climbing walls represent a unique indoor environment in which humans interact closely with a variety of surface types. Climbing wall holds may mediate transmission of organisms between individuals, and yet there are no studies that identify microorganisms present on these surfaces. In the current study, the microorganisms found on climbing wall holds were characterized by analysis of amplified SSU rRNA gene sequences. In contrast to many other studies of built environments, the majority of microorganisms on holds were most closely related to microbes annotated as being recovered from environmental sources, such as soil, with human skin also representing an important source. Regional patterns were evident as rRNA gene sequences from the marine cyanobacterium Prochlorococcus were abundant in gyms found within 16 km of the ocean. Enterobacteriaceae were present on 100 % of holds surveyed, and the members detected are commonly associated with fecal matter.

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References

  1. 1.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  Article  CAS  Google Scholar 

  2. 2.

    Archibald LK, Shapiro J, Pass A, Rand K, Southwick F (2008) Methicillin-resistant Staphylococcus aureus infection in a college football team: risk factors outside the locker room and playing field. Infect Control Hosp Epidemiol 29:450–453

    PubMed  Article  Google Scholar 

  3. 3.

    Bartley JM, Olmsted RN (2008) Reservoirs of pathogens causing health care-associated infections in the 21st Century: is renewed attention to inanimate surfaces warranted? Clin Microbiol Newslett 30:113–117

    Article  Google Scholar 

  4. 4.

    Bloomfield SF, Stanwell-Smith R, Crevel RWR, Pickup J (2006) Too clean, or not too clean: the hygiene hypothesis and home hygiene. Clin Exp Allergy 36:402–425

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  5. 5.

    Boone SA, Gerba CP (2007) Significance of fomites in the spread of respiratory and enteric viral disease. Appl Environ Microbiol 73:1687–1696

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  6. 6.

    Bowers AL, Huffman GR, Sennett BJ (2008) Methicillin-resistant Staphylococcus aureus infections in collegiate football players. Med Sci Sports Exerc 40:1362–1367

    PubMed  Article  Google Scholar 

  7. 7.

    Bowers RM, Sullivan AP, Costello EK, Collett JL, Knight R, Fierer N (2011) Sources of bacteria in outdoor air across cities in the midwestern United States. Appl Environ Microbiol 77:6350–6356

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  8. 8.

    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  9. 9.

    Casewell M, Phillips I (1977) Hands as route of transmission for Klebsiella species. BMJ 2:1315–1317

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  10. 10.

    CDC (2009) Methicillin-resistant Staphylococcus aureus among players on a high school football team- New York City, 2007. Morb Mortal Wkly Rep 58:52–55

    Google Scholar 

  11. 11.

    Cohen PR (2005) Cutaneous community-acquired methicillin-resistant Staphylococcus aureus infection in participants of athletic activities. South Med Assoc 98:596–602

    Article  Google Scholar 

  12. 12.

    Cohen PR (2008) The skin in the gym: a comprehensive review of the cutaneous manifestations of community-acquired methicillin-resistant Staphylococcus aureus infection in athletes. Clin Dermatol 26:16–26

    PubMed  Article  Google Scholar 

  13. 13.

    DeSantis T Jr, Hugenholtz P, Keller K, Brodie E, Larsen N, Piceno Y, Phan R, Andersen G (2006) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34:W394–W399

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  14. 14.

    Dethlefsen L, McFall-Ngai M, Relman DA (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811–818

    PubMed  Article  CAS  Google Scholar 

  15. 15.

    Donskey CJ (2010) Preventing transmission of Clostridium difficile: is the answer blowing in the wind? Clin Infect Dis 50:1458–1461

    PubMed  Article  Google Scholar 

  16. 16.

    Dybwad M, Skogan G, Blatny JM (2014) Temporal variability of the bioaerosol background at a subway station: concentration level, size distribution, and diversity of airborne bacteria. Appl Environ Microbiol 80:257–270

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  17. 17.

    Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.68.Distributed by the author Department of Genome Sciences, University of Washington, Seattle

  18. 18.

    Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci USA 105:17994–17999

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  19. 19.

    Fierer N, Lauber CL, Zhou N, McDonald D, Costello EK, Knight R (2010) Forensic identification using skin bacterial communities. Proc Natl Acad Sci USA 107:6477–6481

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  20. 20.

    Flores GE, Bates ST, Knights D, Lauber CL, Stombaugh J, Knight R, Fierer N (2011) Microbial biogeography of public restroom surfaces. PLoS One 6:e28132

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  21. 21.

    Flores GE, Bates ST, Caporaso JG, Lauber CL, Leff JW, Knight R, Fierer N (2013) Diversity, distribution and sources of bacteria in residential kitchens. Environ Microbiol 15:588–596

    PubMed  Article  CAS  Google Scholar 

  22. 22.

    Gihring TM, Green SJ, Schadt CW (2012) Massively parallel rRNA gene sequencing exacerbates the potential for biased community diversity comparisons due to variable library sizes. Environ Microbiol 14:285–290

    PubMed  Article  CAS  Google Scholar 

  23. 23.

    Grad YH, Lipsitch M, Feldgarden M, Arachchi HM, Cerqueira GC, FitzGerald M, Godfrey P, Haas BJ, Murphy CI, Russ C (2012) Genomic epidemiology of the Escherichia coli O104: H4 outbreaks in Europe, 2011. Proc Natl Acad Sci USA 109:3065–3070

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  24. 24.

    Gwaltney JM, Moskalski PB, Hendley JO (1978) Hand-to-hand transmission of rhinovirus colds. Ann Intern Med 88:463–467

    PubMed  Article  Google Scholar 

  25. 25.

    Henderson DK (2006) Managing methicillin-resistant staphylococci: a paradigm for preventing nosocomial transmission of resistant organisms. Am J Infect Control 34:S46–S54

    PubMed  Article  Google Scholar 

  26. 26.

    Hewitt KM, Gerba CP, Maxwell SL, Kelley ST (2012) Office space bacterial abundance and diversity in three metropolitan areas. PLoS One 7:e37849

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  27. 27.

    Hewitt KM, Mannino FL, Gonzalez A, Chase JH, Caporaso JG, Knight R, Kelley ST (2013) Bacterial diversity in two neonatal intensive care units (NICUs). PLoS One 8:e54703

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  28. 28.

    Hospodsky D, Qian J, Nazaroff WW, Yamamoto N, Bibby K, Rismani-Yazdi H, Peccia J (2012) Human occupancy as a source of indoor airborne bacteria. PLoS One 7:e34867

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  29. 29.

    Judah G, Donachie P, Cobb E, Schmidt W, Holland M, Curtis V (2010) Dirty hands: bacteria of faecal origin on commuters’ hands. Epidemiol Infect 138:409

    PubMed  Article  CAS  Google Scholar 

  30. 30.

    Karlsson MS, Bowen A, Reporter R, Folster JP, Grass JE, Howie RL, Taylor J, Whichard JM (2013) Outbreak of infections caused by Shigella sonnei with reduced susceptibility to azithromycin in the United States. Antimicrob Agents Chemother 57:1559–1560

    Article  CAS  Google Scholar 

  31. 31.

    Kelley S, Gilbert J (2013) Studying the microbiology of the indoor environment. Genome Biol 14:202

    PubMed  Article  PubMed Central  Google Scholar 

  32. 32.

    Kembel SW, Jones E, Kline J, Northcutt D, Stenson J, Womack AM, Bohannan BJM, Brown GZ, Green JL (2012) Architectural design influences the diversity and structure of the built environment microbiome. ISME J 6:1469–1479

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  33. 33.

    Klepeis NE, Nelson WC, Ott WR, Robinson JP, Tsang AM, Switzer P, Behar JV, Hern SC, Engelmann WH (2001) The National Human Activity Pattern Survey (NHAPS): a resource for assessing exposure to environmental pollutants. J Expo Anal Environ Epidemiol 11:231–252

    PubMed  Article  CAS  Google Scholar 

  34. 34.

    Leech JA, Nelson WC, Burnett RT, Aaron S, Raizenne ME (2002) It’s about time: a comparison of Canadian and American time-activity patterns. J Expo Anal Environ Epidemiol 12:427–432

    PubMed  Article  Google Scholar 

  35. 35.

    Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102:11070–11075

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  36. 36.

    Lopman B, Gastañaduy P, Park GW, Hall AJ, Parashar UD, Vinjé J (2012) Environmental transmission of norovirus gastroenteritis. Curr Opin Virol 2:96–102

    PubMed  Article  Google Scholar 

  37. 37.

    Mbithi JN, Springthorpe VS, Boulet JR, Sattar SA (1992) Survival of hepatitis A virus on human hands and its transfer on contact with animate and inanimate surfaces. J Clin Microbiol 30:757–763

    PubMed  CAS  PubMed Central  Google Scholar 

  38. 38.

    Meadow JF, Altrichter AE, Kembel SW, Kline J, Mhuireach G, Moriyama M, Northcutt D, O’Connor TK, Womack AM, Brown GZ, Green JL, Bohannan BJM (2014) Indoor airborne bacterial communities are influenced by ventilation, occupancy, and outdoor air source. Indoor Air 24:41–48

    PubMed  Article  CAS  Google Scholar 

  39. 39.

    Mukherjee DV, Cohen B, Bovino ME, Desai S, Whittier S, Larson EL (2012) Survival of influenza virus on hands and fomites in community and laboratory settings. Am J Infect Control 40:590

    PubMed  Article  Google Scholar 

  40. 40.

    Naether A, Foesel BU, Naegele V, Wüst PK, Weinert J, Bonkowski M, Alt F, Oelmann Y, Polle A, Lohaus G (2012) Environmental factors affect acidobacterial communities below the subgroup level in grassland and forest soils. Appl Environ Microbiol 78:7398–7406

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  41. 41.

    Osburn MR, Sessions AL, Pepe-Ranney C, Spear JR (2011) Hydrogen-isotopic variability in fatty acids from Yellowstone National Park hot spring microbial communities. Geochim Cosmochim Acta 75:4830–4845

    Article  CAS  Google Scholar 

  42. 42.

    Patel A, Fischer S, Calfee R, Plante M, Fadale P (2007) Locker room acquired methicillin-resistant Staphylococcus aureus. Orthopedics 30

  43. 43.

    Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner F (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  44. 44.

    Reeder J, Knight R (2010) Rapid denoising of pyrosequencing amplicon data: exploiting the rank-abundance distribution. Nat Methods 7:668

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  45. 45.

    Reynolds CS (2006) The ecology of phytoplankton. Cambridge University Press, Cambridge, p 552

    Google Scholar 

  46. 46.

    Rintala H, Pitkaeranta M, Toivola M, Paulin L, Nevalainen A (2008) Diversity and seasonal dynamics of bacterial community in indoor environment. BMC Microbiol 8:56

    PubMed  Article  PubMed Central  Google Scholar 

  47. 47.

    Robertson CE, Baumgartner LK, Harris JK, Peterson KL, Stevens MJ, Frank DN, Pace NR (2013) Culture-independent analysis of aerosol microbiology in a metropolitan subway system. Appl Environ Microbiol 79:3485–3493

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  48. 48.

    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  49. 49.

    Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  50. 50.

    Schoffl V, Morrison A, Kupper T (2011) Risk of transmission of blood borne infections in climbing: consensus statement of UIAA Medcom. Int J Sports Med 32:170–173

    PubMed  Article  CAS  Google Scholar 

  51. 51.

    Stevens DL, Bisno AL, Chambers HF, Everett ED, Dellinger P, Goldstein EJC, Gorbach SL, Hirschmann JV, Kaplan EL, Montoya JG, Wade JC (2005) Practice guidelines for the diagnosis and management of skin and soft-tissue infections. Clin Infect Dis 41:1373–1406

    PubMed  Article  Google Scholar 

  52. 52.

    Tringe SG, Zhang T, Liu XG, Yu YT, Lee WH, Yap J, Yao F, Suan ST, Ing SK, Haynes M, Rohwer F, Wei CL, Tan P, Bristow J, Rubin EM, Ruan YJ (2008) The airborne metagenome in an indoor urban environment. PLoS One 3:e1862

    PubMed  Article  PubMed Central  Google Scholar 

  53. 53.

    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  54. 54.

    Wertheim HFL, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL (2005) The role of nasal carriage in Staphylococcus aureus infections. The Lancet 5:751–762

    PubMed  Article  Google Scholar 

  55. 55.

    Williams M, Domingo J, Meckes M, Kelty C, Rochon H (2004) Phylogenetic diversity of drinking water bacteria in a distribution system simulator. J Appl Microbiol 96:954–964

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

This research was performed, in part, by participants in the MBL Microbial Diversity Course in Woods Hole, MA, and was supported in part by the Howard Hughes Medical Foundation, the Gordon and Betty Moore Foundation (2493), the National Science Foundation (DEB-091799), the US Department of Energy (DE-FG02-10ER13361), and the NASA Astrobiology Institute. We thank Carey (Trey) Snellings for assistance with culturing conducted at Appalachian State University. Finally, we want to acknowledge four anonymous climbing gym facility managers for allowing us to sample holds and climbing routes.

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Author notes

  1. M. J. Carmichael

    Present address: Department of Biology, Wake Forest University, Winston-Salem, NC, 27109, USA

Affiliations

  1. Department of Biology, Appalachian State University, Boone, NC, 28608, USA

    S. L. Bräuer, M. J. Carmichael & A. Strom

  2. Microbial Diversity Summer Course, Marine Biological Laboratory, Woods Hole, MA, 02543, USA

    S. L. Bräuer, D. Vuono, C. Pepe-Ranney, D. H. Buckley & S. H. Zinder

  3. Department of Civil and Environmental Engineering, Colorado School of Mines, Golden, CO, 80401, USA

    D. Vuono

  4. Department of Crop and Soil Science, Cornell University, Ithaca, NY, 14853, USA

    C. Pepe-Ranney & D. H. Buckley

  5. Department of Health, Leisure and Exercise Science, Appalachian State University, Boone, NC, 28608, USA

    E. Rabinowitz

  6. Department of Microbiology, Cornell University, Ithaca, NY, 14853, USA

    S. H. Zinder

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Bräuer, S.L., Vuono, D., Carmichael, M.J. et al. Microbial Sequencing Analyses Suggest the Presence of a Fecal Veneer on Indoor Climbing Wall Holds. Curr Microbiol 69, 681–689 (2014). https://doi.org/10.1007/s00284-014-0643-3

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Keywords

  • Prochlorococcus
  • Fecal Indicator Bacterium
  • Abundant OTUs
  • Climbing Wall
  • Great Sequencing Depth