Acknowledgement
This study was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Science, ICT and Future Planning 2019R1F1A1061930 and 2019R1A4A1024764.
References
- Findley K, Oh J, Yang J, Conlan S, Deming C, Meyer JA, et al. 2013. Topographic diversity of fungal and bacterial communities in human skin. Nature 498: 367-370. https://doi.org/10.1038/nature12171
- Wang LL, Clavaud C, Bar-Hen A, Cui M, Gao J, Liu YY, et al. 2015. Characterization of the major bacterial-fungal populations colonizing dandruff scalps in Shanghai, China, shows microbial disequilibrium. Exp. Dermatol. 24: 398-400. https://doi.org/10.1111/exd.12684
- Saxena R, Mittal P, Clavaud C, Dhakan DB, Hegde P, Veeranagaiah MM, et al. 2018. Comparison of healthy and dandruff scalp microbiome reveals the role of commensals in scalp health. Front. Cell Infect. Microbiol. 8: 346. https://doi.org/10.3389/fcimb.2018.00346
- Wang Q-M, Theelen B, Groenewald M, Bai F-Y, Boekhout T. 2014. Moniliellomycetes and Malasseziomycetes, two new classes in Ustilaginomycotina. Persoonia 33: 41-47 https://doi.org/10.3767/003158514X682313
- Theelen B, Cafarchia C, Gaitanis G, Bassukas ID, Boekhout T, Dawson Jr TL. 2018. Malassezia ecology, pathophysiology, and treatment. Med. Mycol. 56: S10-S25. https://doi.org/10.1093/mmy/myx134
- Tang S, Prem A, Tjokrosurjo J, Sary M, Van Bel MA, Rodrigues-Hoffmann A, et al. 2020. The canine skin and ear microbiome: A comprehensive survey of pathogens implicated in canine skin and ear infections using a novel next-generation-sequencing-based assay. Vet. Microbiol. 247: 108764. https://doi.org/10.1016/j.vetmic.2020.108764
- Gupta AK, Kohli Y. 2004. Prevalence of Malassezia species on various body sites in clinically healthy subjects representing different age groups. Med. Mycol. 42: 35-42. https://doi.org/10.1080/13693780310001610056
- Sugita T, Suzuki M, Goto S, Nishikawa A, Hiruma M, Yamazaki T, et al. 2010. Quantitative analysis of the cutaneous Malassezia microbiota in 770 healthy Japanese by age and gender using a real-time PCR assay. Med. Mycol. 48: 229-233. https://doi.org/10.3109/13693780902977976
- Jo J-H, Deming C, Kennedy EA, Conlan S, Polley EC, Ng W-I, et al. 2016. Diverse human skin fungal communities in children converge in adulthood. J. Invest. Dermatol. 136: 2356-2363. https://doi.org/10.1016/j.jid.2016.05.130
- Wu G, Zhao H, Li C, Rajapakse MP, Wong WC, Xu J, et al. 2015. Genus-wide comparative genomics of Malassezia delineates its phylogeny, physiology, and niche adaptation on human skin. PLoS Genet. 11: e1005614. https://doi.org/10.1371/journal.pgen.1005614
- Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, Kuramae EE, et al. 2007. Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc. Natl. Acad. Sci. USA 104: 18730-18735. https://doi.org/10.1073/pnas.0706756104
- Park M, Cho YJ, Lee YW, Jung WH. 2017. Whole genome sequencing analysis of the cutaneous pathogenic yeast Malassezia restricta and identification of the major lipase expressed on the scalp of patients with dandruff. Mycoses 60: 188-197. https://doi.org/10.1111/myc.12586
- Schwartz JR, Messenger AG, Tosti A, Todd G, Hordinsky M, Hay RJ, et al. 2013. A comprehensive pathophysiology of dandruff and seborrheic dermatitis - towards a more precise definition of scalp health. Acta Derm. Venereol. 93: 131-137. https://doi.org/10.2340/00015555-1382
- Heng MC, Henderson CL, Barker DC, Haberfelde G. 1990. Correlation of Pityosporum ovale density with clinical severity of seborrheic dermatitis as assessed by a simplified technique. J. Am. Acad. Dermatol. 23: 82-86. https://doi.org/10.1016/0190-9622(90)70191-J
- Peter RU, Richarz-Barthauer U. 1995. Successful treatment and prophylaxis of scalp seborrhoeic dermatitis and dandruff with 2% ketoconazole shampoo: results of a multicentre, double-blind, placebo-controlled trial. Br. J. Dermatol. 132: 441-445. https://doi.org/10.1111/j.1365-2133.1995.tb08680.x
- Pierard GE, Arrese JE, Pierard-Franchimont C, P DED. 1997. Prolonged effects of antidandruff shampoos - time to recurrence of Malassezia ovalis colonization of skin. Int. J. Cosmet. Sci. 19: 111-117. https://doi.org/10.1111/j.1467-2494.1997.tb00174.x
- DeAngelis YM, Gemmer CM, Kaczvinsky JR, Kenneally DC, Schwartz JR, Dawson TL, Jr. 2005. Three etiologic facets of dandruff and seborrheic dermatitis: Malassezia fungi, sebaceous lipids, and individual sensitivity. J. Investig. Dermatol. Symp. Proc. 10: 295-297. https://doi.org/10.1111/j.1087-0024.2005.10119.x
- Clavaud C, Jourdain R, Bar-Hen A, Tichit M, Bouchier C, Pouradier F, et al. 2013. Dandruff is associated with disequilibrium in the proportion of the major bacterial and fungal populations colonizing the scalp. PLoS One 8: e58203. https://doi.org/10.1371/journal.pone.0058203
- Park T, Kim HJ, Myeong NR, Lee HG, Kwack I, Lee J, et al. 2017. Collapse of human scalp microbiome network in dandruff and seborrhoeic dermatitis. Exp. Dermatol. 26: 835-838. https://doi.org/10.1111/exd.13293
- Lin Q, Panchamukhi A, Li P, Shan W, Zhou H, Hou L, et al. 2020. Malassezia and Staphylococcus dominate scalp microbiome for seborrheic dermatitis. Bioprocess Biosyst Eng. https://doi.org/10.1007/s00449-020-02333-5
- de Groot PW, Bader O, de Boer AD, Weig M, Chauhan N. 2013. Adhesins in human fungal pathogens: glue with plenty of stick. Eukaryot. Cell 12: 470-481. https://doi.org/10.1128/EC.00364-12
- Xu Z, Wang Z, Yuan C, Liu X, Yang F, Wang T, et al. 2016. Dandruff is associated with the conjoined interactions between host and microorganisms. Sci. Rep. 6: 24877. https://doi.org/10.1038/srep24877
- de la O-Escamilla NO, Sidbury R. 2020. Atopic dermatitis: Update on pathogenesis and therapy. Pediatric. Ann. 49: e140-e146.
- Kasperkiewicz M, Schmidt E, Ludwig RJ, Zillikens D. 2018. Targeting IgE antibodies by immunoadsorption in atopic dermatitis. Front. Immunol. 9: 254. https://doi.org/10.3389/fimmu.2018.00254
- Johansson C, Sandstrom M, Bartosik J, Sarnhult T, Christiansen J, Zargari A, et al. 2003. Atopy patch test reactions to Malassezia allergens differentiate subgroups of atopic dermatitis patients. Br. J. Dermatol. 148: 479-488. https://doi.org/10.1046/j.1365-2133.2003.05093.x
- Brodska P, Panzner P, Pizinger K, Schmid-Grendelmeier P. 2014. IgE-mediated sensitization to Malassezia in atopic dermatitis: more common in male patients and in head and neck type. Dermatitis 25: 120-126. https://doi.org/10.1097/DER.0000000000000040
- Glatz M, BuCHNER M, Von Bartenwerffer W, Schmid-Grendelmeier P, Worm M, Hedderich J, et al. 2015. Malassezia spp.-specific immunoglobulin E level is a marker for severity of atopic dermatitis in adults. Acta Derm. Venereol. 95: 191-196. https://doi.org/10.2340/00015555-1864
- Kato H, Sugita T, Ishibashi Y, Nishikawa A. 2006. Detection and quantification of specific IgE antibodies against eight Malassezia species in sera of patients with atopic dermatitis by using an enzyme-linked immunosorbent assay. Microbiol. Immunol. 50: 851-856. https://doi.org/10.1111/j.1348-0421.2006.tb03860.x
- Hiragun T, Ishii K, Hiragun M, Suzuki H, Kan T, Mihara S, et al. 2013. Fungal protein MGL_1304 in sweat is an allergen for atopic dermatitis patients. J. Allergy Clin. Immunol. 132: 608-615. e604. https://doi.org/10.1016/j.jaci.2013.03.047
- Hiragun M, Hiragun T, Ishii K, Suzuki H, Tanaka A, Yanase Y, et al. 2014. Elevated serum IgE against MGL_1304 in patients with atopic dermatitis and cholinergic urticaria. Allergol. Int. 63: 83-93. https://doi.org/10.2332/allergolint.13-OA-0611
- Kohsaka T, Hiragun T, Ishii K, Hiragun M, Kamegashira A, Hide M. 2018. Different hypersensitivities against homologous proteins of MGL_1304 in patients with atopic dermatitis. Allergol. Int. 67: 103-108. https://doi.org/10.1016/j.alit.2017.05.009
- Honnavar P, Dogra S, Handa S, Chakrabarti A, Rudramurthy SM. 2020. Molecular identification and quantification of Malassezia species isolated from pityriasis versicolor. Indian Dermatol. Online J. 11: 167-170. https://doi.org/10.4103/idoj.IDOJ_142_19
- Elshabrawy WO, Saudy N, Sallam M. 2017. Molecular and phenotypic identification and speciation of Malassezia yeasts isolated from Egyptian patients with pityriasis versicolor. J. Clin. Diagn Res. 11: DC12-DC17.
- Vlachos C, Schulte BM, Magiatis P, Adema GJ, Gaitanis G. 2012. Malassezia-derived indoles activate the aryl hydrocarbon receptor and inhibit Toll-like receptor-induced maturation in monocyte-derived dendritic cells. Br. J. Dermatol. 167: 496-505. https://doi.org/10.1111/j.1365-2133.2012.11014.x
- Magiatis P, Pappas P, Gaitanis G, Mexia N, Melliou E, Galanou M, et al. 2013. Malassezia yeasts produce a collection of exceptionally potent activators of the Ah (dioxin) receptor detected in diseased human skin. J. Invest. Dermatol. 133: 2023-2030. https://doi.org/10.1038/jid.2013.92
- Esser C, Bargen I, Weighardt H, Haarmann-Stemmann T, Krutmann J. 2013. Functions of the aryl hydrocarbon receptor in the skin. Semin. Immunopathol. 35: 677-691. https://doi.org/10.1007/s00281-013-0394-4
- Suhr MJ, Banjara N, Hallen-Adams HE. 2016. Sequence-based methods for detecting and evaluating the human gut mycobiome. Lett. Appl. Microbiol. 62: 209-215. https://doi.org/10.1111/lam.12539
- Nash AK, Auchtung TA, Wong MC, Smith DP, Gesell JR, Ross MC, et al. 2017. The gut mycobiome of the Human Microbiome Project healthy cohort. Microbiome 5: 153. https://doi.org/10.1186/s40168-017-0373-4
- Auchtung TA, Fofanova TY, Stewart CJ, Nash AK, Wong MC, Gesell JR, et al. 2018. Investigating colonization of the healthy adult gastrointestinal tract by fungi. MSphere 3: e00092-18.
- Raimondi S, Amaretti A, Gozzoli C, Simone M, Righini L, Candeliere F, et al. 2019. Longitudinal survey of fungi in the human gut: ITS profiling, phenotyping and colonization. Front. Microbiol. 10: 1575. https://doi.org/10.3389/fmicb.2019.01575
- Limon JJ, Tang J, Li D, Wolf AJ, Michelsen KS, Funari V, et al. 2019. Malassezia is associated with Crohn's disease and exacerbates colitis in mouse models. Cell Host Microbe 25: 377-388. https://doi.org/10.1016/j.chom.2019.01.007
- Aykut B, Pushalkar S, Chen R, Li Q, Abengozar R, Kim JI, et al. 2019. The fungal mycobiome promotes pancreatic oncogenesis via activation of MBL. Nature 574: 264-267. https://doi.org/10.1038/s41586-019-1608-2
- Coker OO, Nakatsu G, Dai RZ, Wu WKK, Wong SH, Ng SC, et al. 2019. Enteric fungal microbiota dysbiosis and ecological alterations in colorectal cancer. Gut 68: 654-662. https://doi.org/10.1136/gutjnl-2018-317178
- Soret P, Vandenborght L-E, Francis F, Coron N, Enaud R, Avalos M, et al. 2020. Respiratory mycobiome and suggestion of interkingdom network during acute pulmonary exacerbation in cystic fibrosis. Sci. Rep. 10: 3589. https://doi.org/10.1038/s41598-020-60015-4
- Wertz PW. 2018. Lipids and the permeability and antimicrobial barriers of the skin. J. Lipids 2018: 5954034. https://doi.org/10.1155/2018/5954034
- Gupta AK, Kohli Y. 2004. Prevalence of Malassezia species on various body sites in clinically healthy subjects representing different age groups. Med. Mycol. 42: 35-42. https://doi.org/10.1080/13693780310001610056
- Oranges T, Dini V, Romanelli M. 2015. Skin physiology of the neonate and infant: clinical implications. Adv. Wound Care (New Rochelle). 4: 587-595. https://doi.org/10.1089/wound.2015.0642
- Stehr F, Kretschmar M, Kroger C, Hube B, Schafer WJJomcBe. 2003. Microbial lipases as virulence factors. J. Mol. Catal. B Enzym. 22: 347-355. https://doi.org/10.1016/S1381-1177(03)00049-3
- Park M, Do E, Jung WH. 2013. Lipolytic enzymes involved in the virulence of human pathogenic fungi. Mycobiology 41: 67-72. https://doi.org/10.5941/MYCO.2013.41.2.67
- Priya R, Mythili A, Singh YR, Sreekumar H, Manikandan P, Panneerselvam K, et al. 2014. Virulence, speciation and antibiotic susceptibility of ocular coagualase negative Staphylococci (CoNS). J. Clin. Diagn. Res. 8: DC33-37.
- Al-Wali WI, Elvin SJ, Mason CM, Clark A, Tranter HS. 1998. Comparative phenotypic characteristics of Staphylococcus aureus isolates from line and non-line associated septicaemia, CAPD peritonitis, bone/joint infections and healthy nasal carriers. J. Med. Microbiol. 47: 265-274. https://doi.org/10.1099/00222615-47-3-265
- Rollof J, Braconier JH, Soderstrom C, Nilsson-Ehle P. 1988. Interference of Staphylococcus aureus lipase with human granulocyte function. Eur. J. Clin. Microbiol. Infect. Dis. 7: 505-510. https://doi.org/10.1007/BF01962601
- Braconier JH, Rollof J. 1991. Influence by staphylococcal lipase on granulocyte metabolism and killing of bacteria. Zentralbl. Bakteriol. 276: 68-72. https://doi.org/10.1016/S0934-8840(11)80220-3
- Chen X, Alonzo F, 3rd. 2019. Bacterial lipolysis of immune-activating ligands promotes evasion of innate defenses. Proc. Natl. Acad. Sci. USA 116: 3764-3773. https://doi.org/10.1073/pnas.1817248116
- Hube B, Stehr F, Bossenz M, Mazur A, Kretschmar M, Schafer W. 2000. Secreted lipases of Candida albicans: cloning, characterisation and expression analysis of a new gene family with at least ten members. Arch. Microbiol. 174: 362-374. https://doi.org/10.1007/s002030000218
- Stehr F, Felk A, Gacser A, Kretschmar M, Mahnss B, Neuber K, et al. 2004. Expression analysis of the Candida albicans lipase gene family during experimental infections and in patient samples. FEMS Yeast Res. 4: 401-408. https://doi.org/10.1016/S1567-1356(03)00205-8
- Gacser A, Stehr F, Kroger C, Kredics L, Schafer W, Nosanchuk JD. 2007. Lipase 8 affects the pathogenesis of Candida albicans. Infect. Immun. 75: 4710-4718. https://doi.org/10.1128/IAI.00372-07
- Neugnot V, Moulin G, Dubreucq E, Bigey F. 2002. The lipase/acyltransferase from Candida parapsilosis: Molecular cloning and characterization of purified recombinant enzymes. Eur. J. Biochem. 269: 1734-1745. https://doi.org/10.1046/j.1432-1327.2002.02828.x
- Toth A, Nemeth T, Csonka K, Horvath P, Vagvolgyi C, Vizler C, et al. 2014. Secreted Candida parapsilosis lipase modulates the immune response of primary human macrophages. Virulence 5: 555-62. https://doi.org/10.4161/viru.28509
- Ro BI, Dawson TL. 2005. The role of sebaceous gland activity and scalp microfloral metabolism in the etiology of seborrheic dermatitis and dandruff. J. Investig. Dermatol. Symp. Proc. 10: 194-197. https://doi.org/10.1111/j.1087-0024.2005.10104.x
- Ran Y, Yoshiike T, Ogawa H. 1993. Lipase of Malassezia furfur: Some properties and their relationship to cell growth. J. Med. Vet. Mycol. 31: 77-85. https://doi.org/10.1080/02681219380000081
- Plotkin LI, Squiquera L, Mathov I, Galimberti R, Leoni J. 1996. Characterization of the lipase activity of Malassezia furfur. J. Med. Vet. Mycol. 34: 43-48. https://doi.org/10.1080/02681219680000071
- Brunke S, Hube B. 2006. MfLIP1, a gene encoding an extracellular lipase of the lipid-dependent fungus Malassezia furfur. Microbiology 152: 547-554. https://doi.org/10.1099/mic.0.28501-0
- Juntachai W, Chaichompoo A, Chanarat S. 2020. Ambient pH regulates secretion of lipases in Malassezia furfur. Microbiology 166: 288-295. https://doi.org/10.1099/mic.0.000879
- Juntachai W, Kajiwara S. 2015. Differential expression of extracellular lipase and protease activities of mycelial and yeast forms in Malassezia furfur. Mycopathologia 180: 143-151. https://doi.org/10.1007/s11046-015-9900-7
- DeAngelis YM, Saunders CW, Johnstone KR, Reeder NL, Coleman CG, Kaczvinsky JR, Jr., et al. 2007. Isolation and expression of a Malassezia globosa lipase gene, LIP1. J. Invest. Dermatol. 127: 2138-2146. https://doi.org/10.1038/sj.jid.5700844
- Juntachai W, Oura T, Kajiwara S. 2011. Purification and characterization of a secretory lipolytic enzyme, MgLIP2, from Malassezia globosa. Microbiology 157: 3492-3499. https://doi.org/10.1099/mic.0.054528-0
- Xu H, Lan D, Yang B, Wang Y. 2015. Biochemical properties and structure analysis of a DAG-Like lipase from Malassezia globosa. Int. J. Mol. Sci. 16: 4865-4879. https://doi.org/10.3390/ijms16034865
- Lan D, Xu H, Xu J, Dubin G, Liu J, Iqbal Khan F, et al. 2017. Malassezia globosa MgMDL2 lipase: Crystal structure and rational modification of substrate specificity. Biochem. Biophys. Res. Commun. 488: 259-265. https://doi.org/10.1016/j.bbrc.2017.04.103
- Sommer B, Overy DP, Haltli B, Kerr RG. 2016. Secreted lipases from Malassezia globosa: recombinant expression and determination of their substrate specificities. Microbiology 162: 1069-1079. https://doi.org/10.1099/mic.0.000299
- Cho Y-J, Park M, Jung WHJMra. 2019. Resequencing the genome of Malassezia restricta strain KCTC 27527. Microbiol. Resour. Announc. 8: e00213-19.
- Sommer B, Overy DP, Kerr RG. 2015. Identification and characterization of lipases from Malassezia restricta, a causative agent of dandruff. FEMS Yeast Res. 15: fov078. https://doi.org/10.1093/femsyr/fov078
- Park M, Jung WH, Han SH, Lee YH, Lee YW. 2015. Characterisation and expression analysis of MrLip1, a class 3 family lipase of Malassezia restricta. Mycoses 58: 671-678. https://doi.org/10.1111/myc.12412
- Park M, Lee JS, Jung WH, Lee YW. 2020. pH-dependent expression, stability, and activity of Malassezia restricta MrLip5 Lipase. Ann. Dermatol. 32: 473-480. https://doi.org/10.5021/ad.2020.32.6.473
- Eberlein-Konig B, Schafer T, Huss-Marp J, Darsow U, Mohrenschlager M, Herbert O, et al. 2000. Skin surface pH, stratum corneum hydration, trans-epidermal water loss and skin roughness related to atopic eczema and skin dryness in a population of primary school children. Acta Derm. Venereol. 80: 188-191. https://doi.org/10.1080/000155500750042943
- Moalli R, Meyers RS, Ultsch GR, Jackson DC. 1981. Acid-base balance and temperature in a predominantly skin-breathing salamander, Cryptobranchus alleganiensis. Respir. Physiol. 43: 1-11. https://doi.org/10.1016/0034-5687(81)90083-9
- Jung YC, Kim EJ, Cho JC, Suh KD, Nam GW. 2013. Effect of skin pH for wrinkle formation on Asian: Korean, Vietnamese and Singaporean. J. Eur. Acad. Dermatol. Venereol. 27: e328-332. https://doi.org/10.1111/j.1468-3083.2012.04660.x
- Park M, Cho YJ, Lee YW, Jung WH. 2018. Understanding the mechanism of action of the anti-dandruff agent zinc pyrithione against Malassezia restricta. Sci. Rep. 8: 12086. https://doi.org/10.1038/s41598-018-30588-2
- Ianiri G, Averette AF, Kingsbury JM, Heitman J, Idnurm A. 2016. Gene function analysis in the ubiquitous human commensal and pathogen Malassezia genus. mBio 7: e01853-16.
- Celis AM, Vos AM, Triana S, Medina CA, Escobar N, Restrepo S, et al. 2017. Highly efficient transformation system for Malassezia furfur and Malassezia pachydermatis using Agrobacterium tumefaciens-mediated transformation. J. Microbiol. Methods 134: 1-6. https://doi.org/10.1016/j.mimet.2017.01.001
- Gioti A, Nystedt B, Li W, Xu J, Andersson A, Averette AF, et al. 2013. Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis. mBio 4: e00572-00512.