Transfer of skin microbiota between two dissimilar autologous microenvironments: A pilot study


Autoři: Benji Perin aff001;  Amin Addetia aff002;  Xuan Qin aff002
Působiště autorů: University of Washington Division of Dermatology and Dermatology Residency, Seattle, WA, United States of America aff001;  Seattle Children’s Hospital, Seattle, WA, United States of America aff002;  University of Washington Department of Laboratory Medicine, Seattle, WA, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226857

Souhrn

Dysbiosis of skin microbiota is associated with several inflammatory skin conditions, including atopic dermatitis, acne, and hidradenitis suppurativa. There is a surge of interest by clinicians and the lay public to explore targeted bacteriotherapy to treat these dermatologic conditions. To date, skin microbiota transplantation studies have focused on moving single, enriched strains of bacteria to target sites rather than a whole community. In this prospective pilot study, we examined the feasibility of transferring unenriched skin microbiota communities between two anatomical sites of the same host. We enrolled four healthy volunteers (median age: 28 [range: 24, 36] years; 2 [50%] female) who underwent collection and transfer of skin microbiota from the forearm to the back unidirectionally. Using culture methods and 16S rRNA V1-V3 deep sequencing, we compared baseline and mixed ("transplant") communities, at T = 0 and T = 24 hours. Our ability to detect movement from one site to the other relied on the inherent diversity of the microenvironment of the antecubital fossa relative to the less diverse back. Comparing bacterial species present in the arm and mixed ("transplant") communities that were absent from the baseline back, we saw evidence of transfer of a partial DNA signature; our methods limit conclusions regarding the viability of transferred organisms. We conclude that unenriched transfer of whole cutaneous microbiota is challenging, but our simple technique, intended to move viable skin organisms from one site to another, is worthy of further investigation.

Klíčová slova:

Bacteria – Microbiome – Staphylococcus aureus – Staphylococcus epidermidis – Actinomyces – Corynebacteria – Prevotella


Zdroje

1. Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC, et al. 2009. Topographical and temporal diversity of the human skin microbiome. Science 324:1190–1192. doi: 10.1126/science.1171700 19478181

2. Oh J, Byrd AL, Park M, NISC Comparative Sequencing Program, Kong HH, Segre JA. 2016. Temporal Stability of the Human Skin Microbiome. Cell 165:854–866. doi: 10.1016/j.cell.2016.04.008 27153496

3. Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA, et al. 2012. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22:850–859. doi: 10.1101/gr.131029.111 22310478

4. Dybboe R, Bandier J, Skov L, Engstrand L, Johansen JD. 2017. The role of the skin microbiome in atopic dermatitis: a systematic review. Br J Dermatol.

5. Fitz-Gibbon S, Tomida S, Chiu B-H, Nguyen L, Du C, Liu M, et al. 2013. Propionibacterium acnes strain populations in the human skin microbiome associated with acne. J Invest Dermatol 133:2152–2160. doi: 10.1038/jid.2013.21 23337890

6. Lomholt HB, Scholz CFP, Brüggemann H, Tettelin H, Kilian M. 2017. A comparative study of Cutibacterium (Propionibacterium) acnes clones from acne patients and healthy controls. Anaerobe 47:57–63. doi: 10.1016/j.anaerobe.2017.04.006 28434779

7. Ring HC, Thorsen J, Saunte DM, Lilje B, Bay L, Riis PT, et al. 2017. The Follicular Skin Microbiome in Patients With Hidradenitis Suppurativa and Healthy Controls. JAMA Dermatol 153:897–905. doi: 10.1001/jamadermatol.2017.0904 28538949

8. Kronman MP, Nielson HJ, Adler AL, Giefer MJ, Wahbeh G, Singh N, et al. 2015. Fecal microbiota transplantation via nasogastric tube for recurrent clostridium difficile infection in pediatric patients. J Pediatr Gastroenterol Nutr 60:23–26. doi: 10.1097/MPG.0000000000000545 25162365

9. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, et al. 2013. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 368:407–415. doi: 10.1056/NEJMoa1205037 23323867

10. Nakatsuji T, Chen TH, Narala S, Chun KA, Two AM, Yun T, et al. 2017. Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci Transl Med 9.

11. Myles IA, Williams KW, Reckhow JD, Jammeh ML, Pincus NB, Sastalla I, et al. 2016. Transplantation of human skin microbiota in models of atopic dermatitis. JCI Insight 1.

12. Myles IA, Earland NJ, Anderson ED, Moore IN, Kieh MD, Williams KW, et al. 2018. First-in-human topical microbiome transplantation with Roseomonas mucosa for atopic dermatitis. JCI Insight 3.

13. Morris BEL, Henneberger R, Huber H, Moissl-Eichinger C. 2013. Microbial syntrophy: interaction for the common good. FEMS Microbiology Reviews.

14. Qin X. 2016. Chronic pulmonary pseudomonal infection in patients with cystic fibrosis: A model for early phase symbiotic evolution. Crit Rev Microbiol 42:144–157. doi: 10.3109/1040841X.2014.907235 24766052

15. Melter O, Radojevič B. 2010. Small colony variants of Staphylococcus aureus—review. Folia Microbiol 55:548–558.

16. van Hoek MJA, Merks RMH. 2017. Emergence of microbial diversity due to cross-feeding interactions in a spatial model of gut microbial metabolism. BMC Syst Biol 11:56. doi: 10.1186/s12918-017-0430-4 28511646

17. Louis P, Flint HJ. 2017. Formation of propionate and butyrate by the human colonic microbiota. Environmental Microbiology.

18. D’hoe K, Vet S, Faust K, Moens F, Falony G, Gonze D, et al. 2018. Integrated culturing, modeling and transcriptomics uncovers complex interactions and emergent behavior in a three-species synthetic gut community. Elife 7.

19. Wyber JA, Andrews J, Gilbert P. 1994. Loss of salt-tolerance and transformation efficiency in Escherichia coli associated with sub-lethal injury by centrifugation. Lett Appl Microbiol 19:312–316. doi: 10.1111/j.1472-765x.1994.tb00463.x 7765444

20. Gohl DM, Vangay P, Garbe J, MacLean A, Hauge A, Becker A, et al. 2016. Systematic improvement of amplicon marker gene methods for increased accuracy in microbiome studies. Nat Biotechnol 34:942–949. doi: 10.1038/nbt.3601 27454739

21. Minot SS, Krumm N, Greenfield NB. 2015. One Codex: A Sensitive and Accurate Data Platform for Genomic Microbial Identification. bioRxiv.

22. Zakrzewski M, Proietti C, Ellis JJ, Hasan S, Brion M-J, Berger B, Krause L. 2017. Calypso: a user-friendly web-server for mining and visualizing microbiome–environment interactions. Bioinformatics 33:782–783. doi: 10.1093/bioinformatics/btw725 28025202

23. Myles IA, Reckhow JD, Williams KW, Sastalla I, Frank KM, Datta SK. 2016. A method for culturing Gram-negative skin microbiota. BMC Microbiol 16:60. doi: 10.1186/s12866-016-0684-9 27052736

24. Qamer S, Sandoe JAT, Kerr KG. 2003. Use of colony morphology to distinguish different enterococcal strains and species in mixed culture from clinical specimens. J Clin Microbiol 41:2644–2646. doi: 10.1128/JCM.41.6.2644-2646.2003 12791893

25. Metcalf JL, Xu ZZ, Bouslimani A, Dorrestein P, Carter DO, Knight R. 2017. Microbiome Tools for Forensic Science. Trends Biotechnol 35:814–823. doi: 10.1016/j.tibtech.2017.03.006 28366290

26. Staley C, Vaughn B, Graiziger C, Singroy S, Hamilton M, Yao D, et al. 2017. Community dynamics drive punctuated engraftment of the fecal microbiome following transplantation using freeze-dried, encapsulated fecal microbiota. J Gut Microbes, 8:3, 276–288.


Článek vyšel v časopise

PLOS One


2019 Číslo 12