Fungal Mikrobiyom; Mikobiyom?

Abstract

Bakteriyel mikrobiyom analiz ve araştırmaları, mantar mikrobiyomu kavramı ve çalışmalarının önüne geçmiştir. Tüm insanlar ve laboratuvar hayvanları, sağlıklı olduklarında doğal mantar topluluklarını taşırlar. Mantar mikrobiyomu, bakteriyel mikrobiyomdan önemli ölçüde daha küçüktür. Hastalıkta kofaktör olarak mantar mikrobiyomunun rolü de belirgindir ancak bunca zamanda hafife alınmıştır. Sağlıklı bir derinin fungal mikrobiyomunda yer alan başlıca türler Malassezia ve Candida türleridir. Sağlıklı deride daha fazla maya formu görülürken, etkilenen bölgelerde daha çok hifal formda görülmektedir. Ağız mikrobiyomunun fungi içerdiği kabaca Candida, Aspergillus, Fusarium ve Cryptococcus sp den oluşmaktadır. Sağlıklı akciğerlerin steril olduğu savı da son yıllarda yapılan sekans çalışmaları ile değişmiş, fungal topluluklardan Aspergillus fumigatus başta olmak üzere Ceriporia lacerata, Saccharomyces cerevicae ve Penicillium brevicompactum’un bulunduğunu gösterilmiştir. İnflamatuar bağırsak hastalıklarında belirgin fungal mikrobiyal disbiyoz bulunmuş, Basidiomycota / Ascomycota oranı ve C. albicans’ın arttığı, Saccharomyces cerevisiae oranının ise azalmış olduğu belirlenmiştir. Sonuçta; Bu tür karmaşık ve birbirine bağlı mikrobiyal sistemlerde, mikobiyom, bir dizi hastalığa ve bunların patogenezine katkıda bulunan bir faktör olabilir. İleri çalışmalar kısa sürede bu tür konulara açılım getirecektir.

Keywords

• Fungal mikrobiyom
• mikobiyom
• mantar
• mikrobiyota

Fungal Microbiome; Mycobiome

Abstract

Fungal microbiome concept and studies are dominated by bacterial microbiome analysis and researches. All humans and laboratory animals carry natural fungal
communities when they are healthy. " e fungal microbiome is significantly smaller than the bacterial microbiome. " e role of the fungal microbiome as a cofactor
in disease is also apparent, but has been underestimated in this time. " e main species in the fungal microbiome of a healthy skin are Malassezia and Candida
species. While more yeast forms are seen in healthy skin, it is mostly seen in hyphae form in the a# ected areas. " e oral microbiome consists roughly of Candida,
Aspergillus, Fusarium and Cryptococcus sp. " e argument that healthy lungs are sterile has also changed with the sequence studies carried out in recent years, and it
has been shown that there are fungal communities such as Aspergillus fumigatus, Ceriporia lacerata, Saccharomyces cerevicae and Penicillium brevicompactum. It
was found that significant fungal microbial dysbiosis was found in in$ ammatory bowel diseases, Basidiomycota / Ascomycota ratio and C. albicans increased, and
Saccharomyces cerevisiae ratio decreased. A% er all; In such complex and interconnected microbial systems, the mycobiome can be a contributing factor to a number
of diseases and their pathogenesis. Further studies will open up such issues in a short time.

Keywords

• Fungal microbiome
• mycobiome
• fungus
• microbiota

References

1. 1- Tiew PY, Mac Aogain M, Ali NABM, Thng KX, Goh K, Lau KJX, Chotirmall SH. The Mycobiome in Health and Disease: Emerging Concepts, Methodologies and Challenges. Mycopathologia. 2020 Apr;185(2):207-231. doi: 10.1007/s11046-019-00413-z
2. 2- Limon, J.J., Skalski, J.H., Underhill, D.M., 2017. Commensal Fungi in Health and Disease. Cell Host & Microbe 22, 156–165.. doi:10.1016/j.chom.2017.07.002 3- Brunetti L, De Caro F, Boccia G, Cavallo P, Capunzo M. Surveillance of nosocomial infections: a preliminary study on yeast carriage on hands of healthcare workers. J Prev Med Hyg. 2008 Jun;49(2):63-8.
3. 4- Paul AA, Hoffman KL, Hagan JL, Sampath V, Petrosino JF, Pammi M. Fungal cutaneous microbiome and host determinants in preterm and term neonates. Pediatr Res. 2020 Aug;88(2):225-233. doi: 10.1038/s41390-019-0719-7.
4. 5- Gupta AK, Kohli Y. Prevalence of Malassezia species on various body sites in clinically healthy subjects representing different age groups. Med Mycol. 2004 Feb;42(1):35-42. doi: 10.1080/13693780310001610056
5. 6- Netea MG, Van Der Graaf CA, Vonk AG, Verschueren I, Van Der Meer JW, Kullberg BJ. The role of toll-like receptor (TLR) 2 and TLR4 in the host defense against disseminated candidiasis. J Infect Dis. 2002 May 15;185(10):1483-9. doi: 10.1086/340511.
6. 7- Kistowska M, Fenini G, Jankovic D, Feldmeyer L, Kerl K, Bosshard P, Contassot E, French LE. Malassezia yeasts activate the NLRP3 inflammasome in antigen-presenting cells via Syk-kinase signalling. Exp Dermatol. 2014 Dec;23(12):884-9. doi: 10.1111/exd.12552.
7. 8- Gresnigt MS, Jaeger M, Subbarao Malireddi RK, Rasid O, Jouvion G, Fitting C, Melchers WJG, Kanneganti TD, Carvalho A, Ibrahim-Granet O, van de Veerdonk FL. The Absence of NOD1 Enhances Killing of Aspergillus fumigatus Through Modulation of Dectin-1 Expression. Front Immunol. 2017 Dec 13;8:1777. doi: 10.3389/fimmu.2017.01777.
8. 9- Oh, J., Freeman, A.F., Park, M., Sokolic, R., Candotti, F., Holland, S.M., Segre, J.A., Kong, H.H., 2013. The altered landscape of the human skin microbiome in patients with primary immunodeficiencies. Genome Research 23, 2103–2114.. doi:10.1101/gr.159467.113

9. 10- Velegraki, A., Cafarchia, C., Gaitanis, G., Iatta, R., Boekhout, T., 2015. Malassezia Infections in Humans and Animals: Pathophysiology, Detection, and Treatment. PLOS Pathogens 11, e1004523.. doi:10.1371/journal.ppat.1004523
10. 11- Savolainen J, Lintu P, Kosonen J, Kortekangas-Savolainen O, Viander M, Pène J, Kalimo K, Terho EO, Bousquet J. Pityrosporum and Candida specific and non-specific humoral, cellular and cytokine responses in atopic dermatitis patients. Clin Exp Allergy. 2001 Jan;31(1):125-34. PMID: 11167960.
11. 12- Back, O., Scheynius, A., Johansson, S.G.O., 1995. Ketoconazole in atopic dermatitis: therapeutic response is correlated with decrease in serum IgE. Archives of Dermatological Research 287, 448–451. doi:10.1007/bf00373427
12. 13- Gaitanis G, Magiatis P, Hantschke M, Bassukas ID, Velegraki A. The Malassezia genus in skin and systemic diseases. Clin Microbiol Rev. 2012 Jan;25(1):106-41. doi: 10.1128/CMR.00021-11.
13. 14- Huffnagle GB, Noverr MC. The emerging world of the fungal microbiome. Trends Microbiol. 2013 Jul;21(7):334-41. doi: 10.1016/j.tim.2013.04.002.
14. 15- Zhang E, Tanaka T, Tajima M, Tsuboi R, Nishikawa A, Sugita T. Characterization of the skin fungal microbiota in patients with atopic dermatitis and in healthy subjects. Microbiol Immunol. 2011 Sep;55(9):625-32. doi: 10.1111/j.1348-0421.2011.00364.x.
15. 16- Sonesson A, Bartosik J, Christiansen J, Roscher I, Nilsson F, Schmidtchen A, Bäck O. Sensitization to skin-associated microorganisms in adult patients with atopic dermatitis is of importance for disease severity. Acta Derm Venereol. 2013 May;93(3):340-5. doi: 10.2340/00015555-1465.
16. 17- Chang FY, Lee JH, Yang YH, Yu HH, Wang LC, Lin YT, Chiang BL. Analysis of the serum levels of fungi-specific immunoglobulin E in patients with allergic diseases. Int Arch Allergy Immunol. 2011;154(1):49-56. doi: 10.1159/000319208.
17. 18- Park HK, Ha MH, Park SG, Kim MN, Kim BJ, Kim W. Characterization of the fungal microbiota (mycobiome) in healthy and dandruff-afflicted human scalps. PLoS One. 2012;7(2):e32847. doi: 10.1371/journal.pone.0032847.
18. 19- Theelen, B., Cafarchia, C., Gaitanis, G., Bassukas, I.D., Boekhout, T., Dawson, T.L., 2018. Malassezia ecology, pathophysiology, and treatment. Medical Mycology 56, S10–S25.. doi:10.1093/mmy/myx134
19. 20- Song, Y.C., Hahn, H.J., Kim, J.Y., Ko, J.H., Lee, Y.W., Choe, Y.B., Ahn, K.J., 2011. Epidemiologic Study ofMalasseziaYeasts in Acne Patients by Analysis of 26S rDNA PCR-RFLP. Annals of Dermatology 23, 321.. doi:10.5021/ad.2011.23.3.321
20. 21- Numata S, Akamatsu H, Akaza N, Yagami A, Nakata S, Matsunaga K. Analysis of facial skin-resident microbiota in Japanese acne patients. Dermatology. 2014;228(1):86-92. doi: 10.1159/000356777. Epub 2013 Dec 20. PMID: 24356463.
21. 22- Hu G, Wei YP, Feng J. Malassezia infection: is there any chance or necessity in refractory acne? Chin Med J (Engl). 2010 Mar 5;123(5):628-32.
22. 23- Akaza N, Akamatsu H, Takeoka S, Sasaki Y, Mizutani H, Nakata S, Matsunaga K. Malassezia globosa tends to grow actively in summer conditions more than other cutaneous Malassezia species. J Dermatol. 2012 Jul;39(7):613-6. doi: 10.1111/j.1346-8138.2011.01477.x.
23. 24- Kesavan S, Walters CE, Holland KT, Ingham E. The effects of Malassezia on pro-inflammatory cytokine production by human peripheral blood mononuclear cells in vitro. Med Mycol. 1998 Apr;36(2):97-106.
24. 25- Akaza, N., Akamatsu, H., Takeoka, S., Mizutani, H., Nakata, S., Matsunaga, K., 2012. Increased hydrophobicity inMalasseziaspecies correlates with increased proinflammatory cytokine expression in human keratinocytes. Medical Mycology 50, 802–810.. doi:10.3109/13693786.2012.678019
25. 26- Yan D, Issa N, Afifi L, Jeon C, Chang HW, Liao W. The Role of the Skin and Gut Microbiome in Psoriatic Disease. Curr Dermatol Rep. 2017 Jun;6(2):94-103. doi: 10.1007/s13671-017-0178-5.
26. 27- Paulino LC, Tseng CH, Strober BE, Blaser MJ. Molecular analysis of fungal microbiota in samples from healthy human skin and psoriatic lesions. J Clin Microbiol. 2006 Aug;44(8):2933-41. doi: 10.1128/JCM.00785-06.
27. 28- Dowd SE, Delton Hanson J, Rees E, Wolcott RD, Zischau AM, Sun Y, White J, Smith DM, Kennedy J, Jones CE. Survey of fungi and yeast in polymicrobial infections in chronic wounds. J Wound Care. 2011 Jan;20(1):40-7. doi: 10.12968/jowc.2011.20.1.40.
28. 29- Arron ST, Dimon MT, Li Z, Johnson ME, Wood TA,Feeney L, et al. High Rhodotorula sequences in skintranscriptome of patients with diffuse systemic sclerosis.J Invest Dermatol. 2014;134(8):2138–45.
29. 30- Jo J-H, Kennedy EA, Kong HH. Topographical andphysiological differences of the skin mycobiome in healthand disease. Virulence. 2016;8(3):324–33
30. 31- Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, Gillevet PM. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog. 2010 Jan 8;6(1):e1000713. doi: 10.1371/journal.ppat.1000713.
31. 32- Budden KF, Shukla SD, Rehman SF, Bowerman KL,Keely S, Hugenholtz P, et al. Functional effects of themicrobiota in chronic respiratory disease. Lancet RespirMed. 2019;7:907–920.
32. 33- Kong HH, Morris A. The emerging importance and chal-lengesofthehumanmycobiome.Virulence.2017;8(3):310–2.
33. 34- Lyon J. The Lung Microbiome: Key to Respiratory Ills? JAMA. 2017 May 2;317(17):1713-1714. doi: 10.1001/jama.2017.3023.
34. 35- Li X, Leonardi I, Semon A, Doron I, Gao IH, Putzel GG, Kim Y, Kabata H, Artis D, Fiers WD, Ramer-Tait AE, Iliev ID. Response to Fungal Dysbiosis by Gut-Resident CX3CR1+ Mononuclear Phagocytes Aggravates Allergic Airway Disease. Cell Host Microbe. 2018 Dec 12;24(6):847-856.e4. doi: 10.1016/j.chom.2018.11.003.
35. 36- van Woerden HC, Gregory C, Brown R, Marchesi JR, Hoogendoorn B, Matthews IP. Differences in fungi present in induced sputum samples from asthma patients and non-atopic controls: a community based case control study. BMC Infect Dis. 2013 Feb 5;13:69. doi: 10.1186/1471-2334-13-69.
36. 37- Goldman DL, Chen Z, Shankar V, Tyberg M, Vicencio A, Burk R. Lower airway microbiota and mycobiota in children with severe asthma. J Allergy Clin Immunol. 2018 Feb;141(2):808-811.e7. doi: 10.1016/j.jaci.2017.09.018.
37. 38- Mac Aogáin M, Tiew PY, Lim AYH, Low TB, Tan GL, Hassan T, Ong TH, Pang SL, Lee ZY, Gwee XW, Martinus C, Sio YY, Matta SA, Ong TC, Tiong YS, Wong KN, Narayanan S, Au VB, Marlier D, Keir HR, Tee A, Abisheganaden JA, Koh MS, Wang Y, Connolly JE, Chew FT, Chalmers JD, Chotirmall SH. Distinct "Immunoallertypes" of Disease and High Frequencies of Sensitization in Non-Cystic Fibrosis Bronchiectasis. Am J Respir Crit Care Med. 2019 Apr 1;199(7):842-853. doi: 10.1164/rccm.201807-1355OC.
38. 39- Charlson, E.S., Diamond, J.M., Bittinger, K., Fitzgerald, A.S., Yadav, A., Haas, A.R., Bushman, F.D., Collman, R.G., 2012. Lung-enriched Organisms and Aberrant Bacterial and Fungal Respiratory Microbiota after Lung Transplant. American Journal of Respiratory and Critical Care Medicine 186, 536–545.. doi:10.1164/rccm.201204-0693oc
39. 40- Chabé M, Aliouat-Denis CM, Delhaes L, Aliouat el M, Viscogliosi E, Dei-Cas E. Pneumocystis: from a doubtful unique entity to a group of highly diversified fungal species. FEMS Yeast Res. 2011 Feb;11(1):2-17. doi: 10.1111/j.1567-1364.2010.00698.x.
40. 41- Lawani MB, Morris A. The respiratory microbiome of HIV-infected individuals. Expert Rev Anti Infect Ther. 2016 Aug;14(8):719-29. doi: 10.1080/14787210.2016.1206469. 42- Lipuma JJ. The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev. 2010 Apr;23(2):299-323. doi: 10.1128/CMR.00068-09.
41. 43- Delhaes L, Monchy S, Fréalle E, Hubans C, Salleron J, Leroy S, Prevotat A, Wallet F, Wallaert B, Dei-Cas E, Sime-Ngando T, Chabé M, Viscogliosi E. The airway microbiota in cystic fibrosis: a complex fungal and bacterial community--implications for therapeutic management. PLoS One. 2012;7(4):e36313. doi: 10.1371/journal.pone.0036313.
42. 44- Nguyen LD, Viscogliosi E, Delhaes L. The lung mycobiome: an emerging field of the human respiratory microbiome. Front Microbiol. 2015 Feb 13;6:89. doi: 10.3389/fmicb.2015.00089. PMID: 25762987; PMCID: PMC4327734.
43. 45- Carpagnano, G.E., Susca, A., Scioscia, G., Lacedonia, D., Cotugno, G., Soccio, P., Santamaria, S., Resta, O., Logrieco, G., Foschino Barbaro, M.P., 2019. A survey of fungal microbiota in airways of healthy volunteer subjects from Puglia (Apulia), Italy. BMC Infectious Diseases 19.. doi:10.1186/s12879-019-3718-8
44. 46- Li Q, Wang C, Tang C, He Q, Li N, Li J. Dysbiosis of gut fungal microbiota is associated with mucosal inflammation in Crohn’s disease. J Clin Gastroenterol. 2014;48(6):513. 47- Ott SJ, Ku¨hbacher T, Musfeldt M, Rosenstiel P, Hellmig S, Rehman A, et al. Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand J Gastroenterol. 2008;43(7):831–41.
45. 48- Sokol H, Leducq V, Aschard H, Pham H-P, Jegou S, Landman C, et al. Fungal microbiota dysbiosis in IBD. Gut. 2017;66(6):1039–48.
46. 49- Hoarau G, Mukherjee PK, Gower-Rousseau C, Hager C, Chandra J, Retuerto MA, et al. Bacteriome and mycobiome interactions underscore microbial dysbiosis in familial Crohn’s disease. MBio. 2016;7(5):e01250-16.
47. 50- Liguori G, Lamas B, Richard ML, Brandi G, Da Costa G, Hoffmann TW, et al. Fungal dysbiosis in mucosa-associated microbiota of Crohn’s disease patients. J Crohn’s Colitis. 2015;10(3):296–305.
48. 51- Limon JJ, Tang J, Li D, Wolf AJ, Michelsen KS, Funari V, et al. Malassezia is associated with Crohn’s disease and exacerbates colitis in mouse models. Cell Host Microbe. 2019;25(3):377–88 e6.
49. 52- Wheeler ML, Limon JJ, Bar AS, Leal CA, Gargus M, Tang J, et al. Immunological consequences of intestinal fungal dysbiosis. Cell Host Microbe. 2016;19(6):865–73.
50. 53- Sovran B, Planchais J, Jegou S, Straube M, Lamas B, Natividad JM, et al. Enterobacteriaceae are essential for the modulation of colitis severity by fungi. Microbiome. 2018;6(1):152.
51. 54- Scupham, A.J. et al. (2006) Abundant and diverse fungal microbiota in the murine intestine. Appl. Environ. Microbiol. 72, 793–801.
52. 55- Yamaguchi, N. et al. (2006) Gastrointestinal Candida colonisation promotes sensitisation against food antigens by affecting the mucosal barrier in mice. Gut 55, 954–960.
53. 56- Iliev, I.D. et al. (2012) Interactions between commensal fungi and the Ctype lectin receptor Dectin-1 influence colitis. Science 336, 1314–1.
54. 57- Mukhopadhya I, Hansen R, Meharg C, Thomson J, Russell R, Berry S, et al. The fungal microbiota of de-novo paediatric inflammatory bowel disease. Microbes Infect. 2015;17(4):304–10.
55. 58- Chehoud C, Albenberg LG, Judge C, Hoffmann C, Grunberg S, Bittinger K, et al. Fungal signature in the gut microbiota of pediatric patients with inflammatory bowel disease. Inflamm Bowel Dis. 2015;21(8):1948–56.
56. 59- Van der Waaij, D. and Van der Waaij, B.D. (1990) The colonization resistance of the digestive tract in different animal species and in man; a comparative study. Epidemiol. Infect. 105, 237–243.
57. 60- Gu Y, Zhou G, Qin X, Huang S, Wang B, Cao H. The potential role of gut mycobiome in irritable bowel syndrome. Front Microbiol. 2019;10:1894.
58. 61- Botschuijver S, Roeselers G, Levin E, Jonkers DM, Welting O, Heinsbroek SEM, et al. Intestinal fungal dysbiosis is associated with visceral hypersensitivity in patients with irritable bowel syndrome and rats. Gastroenterology. 2017;153(4):1026–39.
59. 62- Aykut B, Pushalkar S, Chen R, Li Q, Abengozar R, Kim JI, et al. The fungal mycobiome promotes pancreatic oncogenesis via activation of MBL. Nature. 2019;574:264–7.
60. 63- Coker OO, Nakatsu G, Dai RZ, Wu WKK, Wong SH, Ng SC, et al. Enteric fungal microbiota dysbiosis and ecological alterations in colorectal cancer. Gut. 2019;68(4):654–62.
61. 64- Luan C, Xie L, Yang X, Miao H, Lv N, Zhang R, et al. Dysbiosis of fungal microbiota in the intestinal mucosa of patients with colorectal adenomas. Sci Rep. 2015;5:7980.
62. 65- Budden KF, Shukla SD, Rehman SF, Bowerman KL, Keely S, Hugenholtz P, et al. Functional effects of the microbiota in chronic respiratory disease. Lancet Respir Med. 2019;7:907–920.
63. 66- Bacher P, Hohnstein T, Beerbaum E, Rocker M, Blango MG, Kaufmann S, et al. Human anti-fungal Th17 immunity and pathology rely on cross-reactivity against Candida albicans. Cell. 2019;176(6):1340–55 e15.
64. 67- Severance EG, Alaedini A, Yang S, Halling M, Gressitt KL, Stallings CR, et al. Gastrointestinal inflammation and associated immune activation in schizophrenia. Schizophr Res. 2012;138(1):48–53.
65. 68- Strati F, Cavalieri D, Albanese D, De Felice C, Donati C, Hayek J, et al. New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome. 2017;5(1):24.
66. 69- Dinan TG, Cryan JF. The microbiome–gut–brain axis in health and disease. Gastroenterol Clin N Am. 2017;46(1):77–89.
67. 70- Thijssen AY, Jonkers DM, Leue C, van der Veek PP, Vidakovic-Vukic M, van Rood YR, et al. Dysfunctional cognitions, anxiety and depression in irritable bowel syndrome. J Clin Gastroenterol. 2010;44(10):e236–41.
68. 71- Bacher P, Hohnstein T, Beerbaum E, Rocker M, Blango MG, Kaufmann S, et al. Human anti-fungal Th17 immu- nity and pathology rely on cross-reactivity against Candida albicans. Cell. 2019;176(6):1340–55 e15.
69. 72- Wheeler ML, Limon JJ, Underhill DM. Immunity to commensal fungi: detente and disease. Ann Rev Pathol. 2017;12:359–85.