The diversity and abundance of fungi and bacteria on the healthy and dandruff affected human scalp
Autoři:
Sally G. Grimshaw aff001; Adrian M. Smith aff002; David S. Arnold aff001; Elaine Xu aff003; Michael Hoptroff aff001; Barry Murphy aff001
Působiště autorů:
Unilever Research & Development, Port Sunlight, England, United Kingdom
aff001; Unilever Research & Development, Colworth, England, United Kingdom
aff002; Unilever Research & Development, Shanghai, China
aff003
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225796
Souhrn
Dandruff is a skin condition that affects the scalp of up to half the world’s population, it is characterised by an itchy, flaky scalp and is associated with colonisation of the skin by Malassezia spp. Management of this condition is typically via antifungal therapies, however the precise role of microbes in the aggravation of the condition are incompletely characterised. Here, a combination of 454 sequencing and qPCR techniques were used to compare the scalp microbiota of dandruff and non-dandruff affected Chinese subjects. Based on 454 sequencing of the scalp microbiome, the two most abundant bacterial genera found on the scalp surface were Cutibacterium (formerly Propionibacterium) and Staphylococcus, while Malassezia was the main fungal inhabitant. Quantitative PCR (qPCR) analysis of four scalp taxa (M. restricta, M. globosa, C. acnes and Staphylococcus spp.) believed to represent the bulk of the overall population was additionally carried out. Metataxonomic and qPCR analyses were performed on healthy and lesional buffer scrub samples to facilitate assessment of whether the scalp condition is associated with differential microbial communities on the sampled skin. Dandruff was associated with greater frequencies of M. restricta and Staphylococcus spp. compared with the healthy population (p<0.05). Analysis also revealed the presence of an unclassified fungal taxon that could represent a novel Malassezia species.
Klíčová slova:
Fungal genomics – Sequence alignment – Bacteria – Staphylococcus – Polymerase chain reaction – Microbiome – Scalp – Staphylococcus epidermidis
Zdroje
1. Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Current opinion in gastroenterology. 2015;31(1):69. doi: 10.1097/MOG.0000000000000139 25394236
2. Fitz-Gibbon S, Tomida S, Chiu B-H, Nguyen L, Du C, Liu M, et al. Propionibacterium acnes strain populations in the human skin microbiome associated with acne. Journal of Investigative Dermatology. 2013;133(9):2152–60. doi: 10.1038/jid.2013.21 23337890
3. Belda-Ferre P, Alcaraz LD, Cabrera-Rubio R, Romero H, Simon-Soro A, Pignatelli M, et al. The oral metagenome in health and disease. ISME J. 2012;6(1):46–56. http://www.nature.com/ismej/journal/v6/n1/suppinfo/ismej201185s1.html. doi: 10.1038/ismej.2011.85 21716308
4. Harding CR, Moore AE, Rogers SJ, Meldrum H, Scott AE, McGlone FP. Dandruff: a condition characterized by decreased levels of intercellular lipids in scalp stratum corneum and impaired barrier function. Archives of dermatological research. 2002;294(5):221–30. doi: 10.1007/s00403-002-0323-1 12115025
5. Elewski BE. Clinical Diagnosis of Common Scalp Disorders. Journal of Investigative Dermatology Symposium Proceedings. 2005;10(3):190–3. http://dx.doi.org/10.1111/j.1087-0024.2005.10103.x.
6. Ranganathan S, Mukhopadhyay T. Dandruff: The most commercially exploited skin disease. Indian Journal of Dermatology. 2010;55(2):130–4. doi: 10.4103/0019-5154.62734 PMC2887514. 20606879
7. Shuster S. The aetiology of dandruff and the mode of action of therapeutic agents. The British journal of dermatology. 1984;111(2):235–42. Epub 1984/08/01. doi: 10.1111/j.1365-2133.1984.tb04050.x 6235835.
8. Manuel F, Ranganathan S. A New Postulate on Two Stages of Dandruff: A Clinical Perspective. International Journal of Trichology. 2011;3(1):3–6. doi: 10.4103/0974-7753.82117 PMC3129121. 21769228
9. Turner GA, Hoptroff M, Harding CR. Stratum corneum dysfunction in dandruff. Int J Cosmet Sci. 2012;34(4):298–306. Epub 2012/04/21. doi: 10.1111/j.1468-2494.2012.00723.x 22515370; PubMed Central PMCID: PMC3494381.
10. Schwartz JR, Messenger AG, Tosti A, Todd G, Hordinsky M, Hay RJ, et al. A comprehensive pathophysiology of dandruff and seborrheic dermatitis—towards a more precise definition of scalp health. Acta dermato-venereologica. 2013;93(2):131–7. Epub 2012/08/10. doi: 10.2340/00015555-1382 22875203.
11. Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, Kuramae EE, et al. Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proceedings of the National Academy of Sciences. 2007;104(47):18730–5. doi: 10.1073/pnas.0706756104 18000048
12. Wu G, Zhao H, Li C, Rajapakse MP, Wong WC, Xu J, et al. Genus-Wide Comparative Genomics of Malassezia Delineates Its Phylogeny, Physiology, and Niche Adaptation on Human Skin. PLoS Genet. 2015;11(11):e1005614. doi: 10.1371/journal.pgen.1005614 26539826
13. Honnavar P, Prasad GS, Ghosh A, Dogra S, Handa S, Rudramurthy SM. Malassezia arunalokei sp. nov., a Novel Yeast Species Isolated from Seborrheic Dermatitis Patients and Healthy Individuals from India. J Clin Microbiol. 2016;54(7):1826–34. Epub 2016/05/06. doi: 10.1128/JCM.00683-16 27147721; PubMed Central PMCID: PMC4922115.
14. Cabanes FJ, Coutinho SD, Puig L, Bragulat MR, Castella G. New lipid-dependent Malassezia species from parrots. Revista iberoamericana de micologia. 2016;33(2):92–9. Epub 2016/05/18. doi: 10.1016/j.riam.2016.03.003 27184440.
15. Lorch JMP J.M.; Vanderwolf K.J.; Schmidt K.Z.; Verant M.L.; Weller T.J.; Blehert D.S. Malassezia vespertilionis sp. nov.: a new cold-tolerant species of yeast isolated from bats. Persoonia. 2018; 41:56–70. doi: 10.3767/persoonia.2018.41.04 30728599
16. Wang L, Clavaud C, Bar-Hen A, Cui M, Gao J, Liu Y, et al. Characterization of the major bacterial-fungal populations colonizing dandruff scalps in Shanghai, China, shows microbial disequilibrium. Experimental dermatology. 2015;24(5):398–400. Epub 2015/03/06. doi: 10.1111/exd.12684 25739873
17. Clavaud C, Jourdain R, Bar-Hen A, Tichit M, Bouchier C, Pouradier F, et al. Dandruff is associated with disequilibrium in the proportion of the major bacterial and fungal populations colonizing the scalp. PloS one. 2013;8(3):e58203. doi: 10.1371/journal.pone.0058203 23483996
18. Gemmer CM, DeAngelis YM, Theelen B, Boekhout T, Dawson TL Jr, Jr. Fast, noninvasive method for molecular detection and differentiation of Malassezia yeast species on human skin and application of the method to dandruff microbiology. J Clin Microbiol. 2002;40(9):3350–7. Epub 2002/08/31. doi: 10.1128/JCM.40.9.3350-3357.2002 12202578; PubMed Central PMCID: PMC130704.
19. Grice EA, Segre JA. The skin microbiome. Nature Reviews Microbiology. 2011;9(4):244–53. doi: 10.1038/nrmicro2537 21407241
20. Chng KR, Tay ASL, Li C, Ng AHQ, Wang J, Suri BK, et al. Whole metagenome profiling reveals skin microbiome-dependent susceptibility to atopic dermatitis flare. Nature Microbiology. 2016;1:16106. doi: 10.1038/nmicrobiol.2016.106 http://www.nature.com/articles/nmicrobiol2016106#supplementary-information. 27562258
21. Prohic A, Jovovic Sadikovic T, Krupalija‐Fazlic M, Kuskunovic‐Vlahovljak S. Malassezia species in healthy skin and in dermatological conditions. International journal of dermatology. 2015.
22. Turner GA, Matheson JR, Li GZ, Fei XQ, Zhu D, Baines FL. Enhanced efficacy and sensory properties of an anti-dandruff shampoo containing zinc pyrithione and climbazole. Int J Cosmet Sci. 2013;35(1):78–83. Epub 2012/09/14. doi: 10.1111/ics.12007 22970742.
23. Piérard-Franchimont C, Goffin V, Decroix J, Piérard GE. A Multicenter Randomized Trial of Ketoconazole 2% and Zinc Pyrithione 1% Shampoos in Severe Dandruff and Seborrheic Dermatitis. Skin Pharmacology and Physiology. 2002;15(6):434–41.
24. Schmidt-Rose T, Braren S, Folster H, Hillemann T, Oltrogge B, Philipp P, et al. Efficacy of a piroctone olamine/climbazol shampoo in comparison with a zinc pyrithione shampoo in subjects with moderate to severe dandruff. Int J Cosmet Sci. 2011;33(3):276–82. Epub 2011/01/29. doi: 10.1111/j.1468-2494.2010.00623.x 21272039.
25. Sinclair R, Turner GA, Jones DA, Luo S. Clinical studies in dermatology require a post-treatment observation phase to define the impact of the intervention on the natural history of the complaint. Archives of dermatological research. 2016;308(6):379–87. Epub 2016/03/31. doi: 10.1007/s00403-016-1636-9 27025208.
26. Sandstrom Falk MH, Tengvall Linder M, Johansson C, Bartosik J, Back O, Sarnhult T, et al. The prevalence of Malassezia yeasts in patients with atopic dermatitis, seborrhoeic dermatitis and healthy controls. Acta dermato-venereologica. 2005;85(1):17–23. Epub 2005/04/26. doi: 10.1080/00015550410022276 15848985.
27. Saunders CW, Scheynius A, Heitman J. Malassezia Fungi Are Specialized to Live on Skin and Associated with Dandruff, Eczema, and Other Skin Diseases. PLOS Pathogens. 2012;8(6):e1002701. doi: 10.1371/journal.ppat.1002701 22737067
28. DeAngelis YM, Gemmer CM, Kaczvinsky JR, Kenneally DC, Schwartz JR, Dawson TL Jr. Three etiologic facets of dandruff and seborrheic dermatitis: Malassezia fungi, sebaceous lipids, and individual sensitivity. The journal of investigative dermatology Symposium proceedings / the Society for Investigative Dermatology, Inc [and] European Society for Dermatological Research. 2005;10(3):295–7. Epub 2005/12/31. doi: 10.1111/j.1087-0024.2005.10119.x 16382685.
29. Grice EA, Dawson TL. Host–microbe interactions: Malassezia and human skin. Current Opinion in Microbiology. 2017;40:81–7. doi: 10.1016/j.mib.2017.10.024 29141240
30. Rogers J, Harding C, Mayo A, Banks J, Rawlings A. Stratum corneum lipids: the effect of ageing and the seasons. Archives of dermatological research. 1996;288(12):765–70. Epub 1996/11/01. doi: 10.1007/bf02505294 8950457.
31. Pierard-Franchimont C, Pierard GE, Kligman A. Seasonal modulation of sebum excretion. Dermatologica. 1990;181(1):21–2. Epub 1990/01/01. doi: 10.1159/000247853 2394299.
32. Youn SW, Na JI, Choi SY, Huh CH, Park KC. Regional and seasonal variations in facial sebum secretions: a proposal for the definition of combination skin type. Skin research and technology: official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging (ISSI). 2005;11(3):189–95. Epub 2005/07/07. doi: 10.1111/j.1600-0846.2005.00119.x 15998330.
33. Nam GW, Baek JH, Koh JS, Hwang JK. The seasonal variation in skin hydration, sebum, scaliness, brightness and elasticity in Korean females. Skin research and technology: official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging (ISSI). 2015;21(1):1–8. Epub 2014/02/18. doi: 10.1111/srt.12145 24528115.
34. Xu Z, Wang Z, Yuan C, Liu X, Yang F, Wang T, et al. Dandruff is associated with the conjoined interactions between host and microorganisms. Sci Rep. 2016;6:24877. Epub 2016/05/14. doi: 10.1038/srep24877 27172459; PubMed Central PMCID: PMC4864613.
35. Rogers JS, Moore AE, Meldrum H, Harding CR. Increased scalp skin lipids in response to antidandruff treatment containing zinc pyrithione. Archives of dermatological research. 2003;295(3):127–9. Epub 2003/06/18. doi: 10.1007/s00403-003-0406-7 12811576.
36. Williamson P, Kligman AM. A new method for the quantitative investigation of cutaneous bacteria. J Invest Dermatol. 1965;45(6):498–503. Epub 1965/12/01. doi: 10.1038/jid.1965.164 5321315.
37. Walters WA, Caporaso JG, Lauber CL, Berg-Lyons D, Fierer N, Knight R. PrimerProspector: de novo design and taxonomic analysis of barcoded polymerase chain reaction primers. Bioinformatics. 2011;27(8):1159–61. doi: 10.1093/bioinformatics/btr087 21349862
38. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ. Removing noise from pyrosequenced amplicons. BMC bioinformatics. 2011;12(1):38.
39. Quince C, Lanzen A, Curtis TP, Davenport RJ, Hall N, Head IM, et al. Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods. 2009;6(9):639–41. Epub 2009/08/12. doi: 10.1038/nmeth.1361 19668203.
40. Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584. doi: 10.7717/peerj.2584 27781170
41. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research. 2012;41(D1):D590–D6. doi: 10.1093/nar/gks1219 23193283
42. Cooper P MR. NCBI News: National Center for Biotechnology Information (US) (US); 1991–2012. https://wwwncbinlmnihgov/books/NBK82331/. 2011.
43. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Research. 2013;42(D1):D633–D42. doi: 10.1093/nar/gkt1244 24288368
44. Tateno Y, Imanishi T, Miyazaki S, Fukami-Kobayashi K, Saitou N, Sugawara H, et al. DNA Data Bank of Japan (DDBJ) for genome scale research in life science. Nucleic Acids Research. 2002;30(1):27–30. doi: 10.1093/nar/30.1.27 11752245
45. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72(7):5069–72. Epub 2006/07/06. doi: 10.1128/AEM.03006-05 16820507; PubMed Central PMCID: PMC1489311.
46. Sun S, Chen J, Li W, Altintas I, Lin A, Peltier S, et al. Community cyberinfrastructure for Advanced Microbial Ecology Research and Analysis: the CAMERA resource. Nucleic Acids Research. 2011;39(Database issue):D546–D51. doi: 10.1093/nar/gkq1102 PMC3013694. 21045053
47. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, et al. Introducing EzBioCloud: A taxonomically united database of 16S rRNA and whole genome assemblies. International journal of systematic and evolutionary microbiology. 2016. Epub 2016/12/23. doi: 10.1099/ijsem.0.001755 28005526.
48. Leinonen R, Akhtar R, Birney E, Bower L, Cerdeno-Tárraga A, Cheng Y, et al. The European Nucleotide Archive. Nucleic Acids Research. 2010;39(suppl_1):D28–D31. doi: 10.1093/nar/gkq967 20972220
49. Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, et al. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology. 2013;22(21):5271–7. doi: 10.1111/mec.12481 24112409
50. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nature methods. 2010;7(5):335–6. doi: 10.1038/nmeth.f.303 20383131
51. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008;36(Web Server issue):W465–9. Epub 2008/04/22. doi: 10.1093/nar/gkn180 18424797; PubMed Central PMCID: PMC2447785.
52. Chevenet F, Brun C, Banuls AL, Jacq B, Christen R. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics. 2006;7:439. Epub 2006/10/13. doi: 10.1186/1471-2105-7-439 17032440; PubMed Central PMCID: PMC1615880.
53. Muhire BM, Varsani A, Martin DP. SDT: A Virus Classification Tool Based on Pairwise Sequence Alignment and Identity Calculation. PLOS ONE. 2014;9(9):e108277. doi: 10.1371/journal.pone.0108277 25259891
54. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R, et al. vegan: Community Ecology Package. R package version 2.0–10. 2013. There is no corresponding record for this reference. 2015.
55. Hothorn T, Buehlmann P, Dudoit S, Molinaro A, Laan MVD. R Package Party. Survival Ensembles. Biostatistics2006. p. 355–73. doi: 10.1093/biostatistics/kxj011 16344280
56. La Rosa PS DE, Shands B, Shannon WD. HMP: Hypothesis Testing and Power Calculations for Comparing Metagenomic Samples from HMPR package. 1.3.1 ed. http://CRAN.R-project.org/package=HMP2013.
57. Sas Institute Inc CNC. JMP. 9.0 ed.
58. Soares RC, Zani MB, Arruda ACBB, Arruda LHFd, Paulino LC. Malassezia Intra-Specific Diversity and Potentially New Species in the Skin Microbiota from Brazilian Healthy Subjects and Seborrheic Dermatitis Patients. PLoS ONE. 2015;10(2):e0117921. doi: 10.1371/journal.pone.0117921 25695430
59. Coates R, Moran J, Horsburgh MJ. Staphylococci: colonizers and pathogens of human skin. Future Microbiol. 2014;9(1):75–91. Epub 2013/12/18. doi: 10.2217/fmb.13.145 24328382.
60. Bergeron M, Dauwalder O, Gouy M, Freydiere AM, Bes M, Meugnier H, et al. Species identification of staphylococci by amplification and sequencing of the tuf gene compared to the gap gene and by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. European journal of clinical microbiology & infectious diseases: official publication of the European Society of Clinical Microbiology. 2011;30(3):343–54. Epub 2010/10/23. doi: 10.1007/s10096-010-1091-z 20967479.
61. Vandecasteele SJ, Peetermans WE, R RM, Rijnders BJ, Van Eldere J. Reliability of the ica, aap and atlE genes in the discrimination between invasive, colonizing and contaminant Staphylococcus epidermidis isolates in the diagnosis of catheter-related infections. Clinical microbiology and infection: the official publication of the European Society of Clinical Microbiology and Infectious Diseases. 2003;9(2):114–9. Epub 2003/02/18. doi: 10.1046/j.1469-0691.2003.00544.x 12588331.
62. Sivadon V, Rottman M, Quincampoix JC, Prunier E, Le Moal M, de Mazancourt P, et al. Partial atlE sequencing of Staphylococcus epidermidis strains from prosthetic joint infections. J Clin Microbiol. 2009;47(7):2321–4. Epub 2009/05/22. doi: 10.1128/JCM.01971-08 19458175; PubMed Central PMCID: PMC2708500.
63. Soares RC, Camargo-Penna PH, de Moraes VCS, De Vecchi R, Clavaud C, Breton L, et al. Dysbiotic Bacterial and Fungal Communities Not Restricted to Clinically Affected Skin Sites in Dandruff. Frontiers in Cellular and Infection Microbiology. 2016;6(157). doi: 10.3389/fcimb.2016.00157 27909689
64. Mills KJ, Hu P, Henry J, Tamura M, Tiesman JP, Xu J. Dandruff/seborrhoeic dermatitis is characterized by an inflammatory genomic signature and possible immune dysfunction: transcriptional analysis of the condition and treatment effects of zinc pyrithione. The British journal of dermatology. 2012;166 Suppl 2:33–40. Epub 2012/06/15. doi: 10.1111/j.1365-2133.2012.10863.x 22670617.
65. Saxena R, Mittal P, Clavaud C, Dhakan DB, Hegde P, Veeranagaiah MM, et al. Comparison of Healthy and Dandruff Scalp Microbiome Reveals the Role of Commensals in Scalp Health. Frontiers in Cellular and Infection Microbiology. 2018;8(346). doi: 10.3389/fcimb.2018.00346 30338244
66. Pasolli E, Asnicar F, Manara S, Zolfo M, Karcher N, Armanini F, et al. Extensive Unexplored Human Microbiome Diversity Revealed by Over 150,000 Genomes from Metagenomes Spanning Age, Geography, and Lifestyle. Cell. 2019;176(3):649–62.e20. doi: 10.1016/j.cell.2019.01.001 30661755
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