Expansion of commensal fungus Wallemia mellicola in the gastrointestinal mycobiota enhances the severity of allergic airway disease in mice

PLoS Pathogens

Volumn 14, Issue 9, 2018, Pages

  Skalski, Joseph H ^a,b   Limon, Jose J ^a   Sharma, Purnima ^a   Gargus, Matthew D ^a   Nguyen, Christopher ^a   Tang, Jie ^a   Coelho, Ana Lucia ^a   Hogaboam, Cory M ^a   Crother, Timothy R ^a   Underhill, David M ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; ANTIINFECTIVE AGENT; HOUSE DUST ALLERGEN;

ANIMAL; BASIDIOMYCETES; C57BL MOUSE; DISEASE MODEL; DRUG EFFECT; ENVIRONMENTAL MICROBIOLOGY; FEMALE; GENETICS; GERMFREE ANIMAL; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; INTESTINE FLORA; MICROBIOLOGY; MOUSE; MYCOBIOME; PATHOGENICITY; RESPIRATORY TRACT ALLERGY; SYMBIOSIS;

ALLERGENS; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIGENS, DERMATOPHAGOIDES; BASIDIOMYCOTA; DISEASE MODELS, ANIMAL; ENVIRONMENTAL MICROBIOLOGY; FEMALE; GASTROINTESTINAL MICROBIOME; GERM-FREE LIFE; HUMANS; MICE; MICE, INBRED C57BL; MYCOBIOME; RESPIRATORY HYPERSENSITIVITY; SYMBIOSIS;

EID: 85054406155     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1007260     Document Type: Article

References (54)

1. Belkaid Y, Hand TW, Role of the microbiota in immunity and inflammation. Cell. 2014;157: 121–41. doi: 10.1016/j.cell.2014.03.011 pmid: 24679531
2. Rooks MG, Garrett WS, Gut microbiota, metabolites and host immunity. Nat Rev Immunol. 2016;16: 341–52. doi: 10.1038/nri.2016.42 pmid: 27231050
3. Round JL, Mazmanian SK, The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9: 313–23. doi: 10.1038/nri2515 pmid: 19343057
4. Kim YG, Udayanga KG, Totsuka N, Weinberg JB, Nunez G, Shibuya A, Gut dysbiosis promotes M2 macrophage polarization and allergic airway inflammation via fungi-induced PGE(2). Cell Host Microbe. 2014;15: 95–102. doi: 10.1016/j.chom.2013.12.010 pmid: 24439901
5. Steed AL, Christophi GP, Kaiko GE, Sun L, Goodwin VM, Jain U, et al. The microbial metabolite desaminotyrosine protects from influenza through type I interferon. Science. 2017;357: 498–502. doi: 10.1126/science.aam5336 pmid: 28774928
6. Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med. 2014;20: 159–66. doi: 10.1038/nm.3444 pmid: 24390308
7. Schuijt TJ, Lankelma JM, Scicluna BP, de Sousa e Melo F, Roelofs JJ, de Boer JD, et al. The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia. Gut. 2016;65: 575–83. doi: 10.1136/gutjnl-2015-309728 pmid: 26511795
8. Limon JJ, Skalski JH, Underhill DM, Commensal Fungi in Health and Disease. Cell Host Microbe. 2017;22: 156–65. doi: 10.1016/j.chom.2017.07.002 pmid: 28799901
9. Nash AK, Auchtung TA, Wong MC, Smith DP, Gesell JR, Ross MC, et al. The gut mycobiome of the Human Microbiome Project healthy cohort. Microbiome. 2017;5: 153. doi: 10.1186/s40168-017-0373-4 pmid: 29178920
10. Huffnagle GB, Noverr MC, The emerging world of the fungal microbiome. Trends Microbiol. 2013;21: 334–41. doi: 10.1016/j.tim.2013.04.002 pmid: 23685069
11. Tang J, Iliev ID, Brown J, Underhill DM, Funari VA, Mycobiome: Approaches to analysis of intestinal fungi. J Immunol Methods. 2015;421: 112–21. doi: 10.1016/j.jim.2015.04.004 pmid: 25891793
12. Valero A, Quirce S, Davila I, Delgado J, Dominguez-Ortega J, Allergic respiratory disease: Different allergens, different symptoms. Allergy. 2017;72: 1306–16. doi: 10.1111/all.13141 pmid: 28208220
13. Serrano-Pariente J, Rodrigo G, Fiz JA, Crespo A, Plaza V, High Risk Asthma Research GIdentification and characterization of near-fatal asthma phenotypes by cluster analysis. Allergy. 2015;70: 1139–47. doi: 10.1111/all.12654 pmid: 26011771
14. Fukutomi Y, Taniguchi M, Sensitization to fungal allergens: Resolved and unresolved issues. Allergol Int. 2015;64: 321–31. doi: 10.1016/j.alit.2015.05.007 pmid: 26433528
15. Arrieta MC, Arevalo A, Stiemsma L, Dimitriu P, Chico ME, Loor S, et al. Associations between infant fungal and bacterial dysbiosis and childhood atopic wheeze in a nonindustrialized setting. J Allergy Clin Immunol. 2018;142: 424–34. doi: 10.1016/j.jaci.2017.08.041 pmid: 29241587
16. Noverr MC, Noggle RM, Toews GB, Huffnagle GB, Role of antibiotics and fungal microbiota in driving pulmonary allergic responses. Infect Immun. 2004;72: 4996–5003. doi: 10.1128/IAI.72.9.4996-5003.2004 pmid: 15321991
17. 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: 865–73. doi: 10.1016/j.chom.2016.05.003 pmid: 27237365
18. Botic T, Kuncic MK, Sepcic K, Knez Z, Gunde-Cimerman N, Salt induces biosynthesis of hemolytically active compounds in the xerotolerant food-borne fungus Wallemia sebi. FEMS Microbiol Lett. 2012;326: 40–6. doi: 10.1111/j.1574-6968.2011.02428.x pmid: 22092533
19. Jancic S, Nguyen HD, Frisvad JC, Zalar P, Schroers HJ, Seifert KA, et al. A Taxonomic Revision of the Wallemia sebi Species Complex. PLoS One. 2015;10: e0125933. doi: 10.1371/journal.pone.0125933 pmid: 26017053
20. Zalar P, Sybren de Hoog G, Schroers HJ, Frank JM, Gunde-Cimerman N, Taxonomy and phylogeny of the xerophilic genus Wallemia (Wallemiomycetes and Wallemiales, cl. et ord. nov.). Antonie Van Leeuwenhoek. 2005;87: 311–28. doi: 10.1007/s10482-004-6783-x pmid: 15928984
21. Zeng QY, Westermark SO, Rasmuson-Lestander A, Wang XR, Detection and quantification of Wallemia sebi in aerosols by real-time PCR, conventional PCR, and cultivation. Appl Environ Microbiol. 2004;70: 7295–302. doi: 10.1128/AEM.70.12.7295-7302.2004 pmid: 15574929
22. Desroches TC, McMullin DR, Miller JD, Extrolites of Wallemia sebi, a very common fungus in the built environment. Indoor Air. 2014;24: 533–42. doi: 10.1111/ina.12100 pmid: 24471934
23. Wood GM, Mann PJ, Lewis DF, Reid WJ, Moss MO, Studies on a toxic metabolite from the mould Wallemia. Food Addit Contam. 1990;7: 69–77. doi: 10.1080/02652039009373822 pmid: 2106458
24. Frank M, Kingston E, Jeffery JC, Moss MO, Murray M, Simpson TJ, et al. Walleminol and walleminone, novel caryophyllenes from the toxigenic fungus Wallemia sebi. Tetrahedron Lett. 1999;40: 133–6.
25. Sakamoto T, Urisu A, Yamada M, Matsuda Y, Tanaka K, Torii S, Studies on the osmophilic fungus Wallemia sebi as an allergen evaluated by skin prick test and radioallergosorbent test. Int Arch Allergy Appl Immunol. 1989;90: 368–72. pmid: 2613343
26. Vesper SJ, McKinstry C, Yang C, Haugland RA, Kercsmar CM, Yike I, et al. Specific molds associated with asthma in water-damaged homes. J Occup Environ Med. 2006;48: 852–8. doi: 10.1097/01.jom.0000224736.52780.2f pmid: 16902378
27. Mason KL, Erb Downward JR, Falkowski NR, Young VB, Kao JY, Huffnagle GB, Interplay between the gastric bacterial microbiota and Candida albicans during postantibiotic recolonization and gastritis. Infect Immun. 2012;80: 150–8. doi: 10.1128/IAI.05162-11 pmid: 21986629
28. 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. doi: 10.1038/srep07980 pmid: 25613490
29. Mar Rodriguez M, Perez D, Javier Chaves F, Esteve E, Marin-Garcia P, Xifra G, et al. Obesity changes the human gut mycobiome. Sci Rep. 2015;5: 14600. doi: 10.1038/srep14600 pmid: 26455903
30. Botschuijver S, Roeselers G, Levin E, Jonkers DM, Welting O, Heinsbroek SE, et al. Intestinal Fungal Dysbiosis Associates With Visceral Hypersensitivity in Patients With Irritable Bowel Syndrome and Rats. Gastroenterology. 2017;153: 1026–39. doi: 10.1053/j.gastro.2017.06.004 pmid: 28624575
31. Peng XP, Wang Y, Liu PP, Hong K, Chen H, Yin X, et al. Aromatic compounds from the halotolerant fungal strain of Wallemia sebi PXP-89 in a hypersaline medium. Arch Pharm Res. 2011;34: 907–12. doi: 10.1007/s12272-011-0607-0 pmid: 21725811
32. Moore RJ, Stanley D, Experimental design considerations in microbiota/inflammation studies. Clin Transl Immunology. 2016;5: e92. doi: 10.1038/cti.2016.41 pmid: 27525065
33. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12: R60. doi: 10.1186/gb-2011-12-6-r60 pmid: 21702898
34. Clavel T, Gomes-Neto JC, Lagkouvardos I, Ramer-Tait AE, Deciphering interactions between the gut microbiota and the immune system via microbial cultivation and minimal microbiomes. Immunol Rev. 2017;279: 8–22. doi: 10.1111/imr.12578 pmid: 28856739
35. Wymore Brand M, Wannemuehler MJ, Phillips GJ, Proctor A, Overstreet AM, Jergens AE, et al. The Altered Schaedler Flora: Continued Applications of a Defined Murine Microbial Community. ILAR J. 2015;56: 169–78. doi: 10.1093/ilar/ilv012 pmid: 26323627
36. Dewhirst FE, Chien CC, Paster BJ, Ericson RL, Orcutt RP, Schauer DB, et al. Phylogeny of the defined murine microbiota: altered Schaedler flora. Appl Environ Microbiol. 1999;65: 3287–92. pmid: 10427008
37. Miller JD, Sun M, Gilyan A, Roy J, Rand TG, Inflammation-associated gene transcription and expression in mouse lungs induced by low molecular weight compounds from fungi from the built environment. Chem Biol Interact. 2010;183: 113–24. doi: 10.1016/j.cbi.2009.09.023 pmid: 19818335
38. Zhang Z, Li J, Zheng W, Zhao G, Zhang H, Wang X, et al. Peripheral Lymphoid Volume Expansion and Maintenance Are Controlled by Gut Microbiota via RALDH+ Dendritic Cells. Immunity. 2016;44: 330–42. doi: 10.1016/j.immuni.2016.01.004 pmid: 26885858
39. Lappalainen S, Pasanen AL, Reiman M, Kalliokoski P, Serum IgG antibodies against Wallemia sebi and Fusarium species in Finnish farmers. Ann Allergy Asthma Immunol. 1998;81: 585–92. doi: 10.1016/S1081-1206(10)62710-X pmid: 9892031
40. Vanderweil SG, Tsai CL, Pelletier AJ, Espinola JA, Sullivan AF, Blumenthal D, et al. Inappropriate use of antibiotics for acute asthma in United States emergency departments. Acad Emerg Med. 2008;15: 736–43. doi: 10.1111/j.1553-2712.2008.00167.x pmid: 18627585
41. De Boeck K, Vermeulen F, Meyts I, Hutsebaut L, Franckaert D, Proesmans M, Coprescription of antibiotics and asthma drugs in children. Pediatrics. 2011;127: 1022–6. doi: 10.1542/peds.2009-3068 pmid: 21606144
42. Marra F, Marra CA, Richardson K, Lynd LD, Kozyrskyj A, Patrick DM, et al. Antibiotic use in children is associated with increased risk of asthma. Pediatrics. 2009;123: 1003–10. doi: 10.1542/peds.2008-1146 pmid: 19255032
43. Stensballe LG, Simonsen J, Jensen SM, Bonnelykke K, Bisgaard H, Use of antibiotics during pregnancy increases the risk of asthma in early childhood. J Pediatr. 2013;162: 832–8. doi: 10.1016/j.jpeds.2012.09.049 pmid: 23140881
44. Britton RA, Young VB, Interaction between the intestinal microbiota and host in Clostridium difficile colonization resistance. Trends Microbiol. 2012;20: 313–9. doi: 10.1016/j.tim.2012.04.001 pmid: 22595318
45. Liu CM, Kachur S, Dwan MG, Abraham AG, Aziz M, Hsueh PR, et al. FungiQuant: a broad-coverage fungal quantitative real-time PCR assay. BMC Microbiol. 2012;12: 255. doi: 10.1186/1471-2180-12-255 pmid: 23136846
46. Stevens WW, Kim TS, Pujanauski LM, Hao X, Braciale TJ, Detection and quantitation of eosinophils in the murine respiratory tract by flow cytometry. J Immunol Methods. 2007;327: 63–74. doi: 10.1016/j.jim.2007.07.011 pmid: 17716680
47. Zaiss MM, Rapin A, Lebon L, Dubey LK, Mosconi I, Sarter K, et al. The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation. Immunity. 2015;43: 998–1010. doi: 10.1016/j.immuni.2015.09.012 pmid: 26522986
48. Zeki AA, Bratt JM, Rabowsky M, Last JA, Kenyon NJ, Simvastatin inhibits goblet cell hyperplasia and lung arginase in a mouse model of allergic asthma: a novel treatment for airway remodeling?Transl Res. 2010;156: 335–49. doi: 10.1016/j.trsl.2010.09.003 pmid: 21078495
49. Zhang J, Hung GC, Nagamine K, Li B, Tsai S, Lo SC, Development of Candida-Specific Real-Time PCR Assays for the Detection and Identification of Eight Medically Important Candida Species. Microbiol Insights. 2016;9: 21–8. doi: 10.4137/MBI.S38517 pmid: 27103821
50. Sarma-Rupavtarm RB, Ge Z, Schauer DB, Fox JG, Polz MF, Spatial distribution and stability of the eight microbial species of the altered schaedler flora in the mouse gastrointestinal tract. Appl Environ Microbiol. 2004;70: 2791–800. doi: 10.1128/AEM.70.5.2791-2800.2004 pmid: 15128534
51. McHardy IH, Goudarzi M, Tong M, Ruegger PM, Schwager E, Weger JR, et al. Integrative analysis of the microbiome and metabolome of the human intestinal mucosal surface reveals exquisite inter-relationships. Microbiome. 2013;1: 17. doi: 10.1186/2049-2618-1-17 pmid: 24450808
52. Martin M, Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal. 2011;17: 10–12.
53. 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: 335–6. doi: 10.1038/nmeth.f.303 pmid: 20383131
54. McMurdie PJ, Holmes S, phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8: e61217. doi: 10.1371/journal.pone.0061217 pmid: 23630581