Skip to main content
Top
Published in: Clinical Reviews in Allergy & Immunology 3/2019

01-12-2019 | Chronic Inflammatory Bowel Disease

Methanogenic Archaea: Emerging Partners in the Field of Allergic Diseases

Authors: Youssouf Sereme, Soraya Mezouar, Ghiles Grine, Jean Louis Mege, Michel Drancourt, Pierre Corbeau, Joana Vitte

Published in: Clinical Reviews in Allergy & Immunology | Issue 3/2019

Login to get access

Abstract

Archaea, which form one of four domains of life alongside Eukarya, Bacteria, and giant viruses, have long been neglected as components of the human microbiota and potential opportunistic infectious pathogens. In this review, we focus on methanogenic Archaea, which rely on hydrogen for their metabolism and growth. On one hand, methanogenic Archaea in the gut are functional associates of the fermentative digestion of dietary fibers, favoring the production of beneficial short-chain fatty acids and likely contributing to the weaning reaction during the neonatal window of opportunity. On the other hand, methanogenic Archaea trigger the activation of innate and adaptive responses and the generation of specific T and B cells in animals and humans. In mouse models, lung hypersensitivity reactions can be induced by inhaled methanogenic Archaea mimicking human professional exposure to organic dust. Changes in methanogenic Archaea of the microbiota are detected in an array of dysimmune conditions comprising inflammatory bowel disease, obesity, malnutrition, anorexia, colorectal cancer, and diverticulosis. At the subcellular level, methanogenic Archaea are activators of the TLR8-dependent NLRP3 inflammasome, modulate the release of antimicrobial peptides and drive the production of proinflammatory, Th-1, Th-2, and Th-17 cytokines. Our objective was to introduce the most recent and major pieces of evidence supporting the involvement of Archaea in the balance between health and dysimmune diseases, with a particular focus on atopic and allergic conditions.
Literature
2.
go back to reference MetaHIT Consortium, Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto J-M, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Doré J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Bork P, Ehrlich SD, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65. https://doi.org/10.1038/nature08821 CrossRefPubMedCentral MetaHIT Consortium, Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto J-M, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Doré J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Bork P, Ehrlich SD, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65. https://​doi.​org/​10.​1038/​nature08821 CrossRefPubMedCentral
12.
go back to reference Borrel G, Harris HMB, Tottey W, Mihajlovski A, Parisot N, Peyretaillade E, Peyret P, Gribaldo S, O’Toole PW, Brugère J-F (2012) Genome sequence of “Candidatus Methanomethylophilus alvus” Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogenic Archaea. J Bacteriol 194:6944–6945. https://doi.org/10.1128/JB.01867-12 CrossRefPubMedPubMedCentral Borrel G, Harris HMB, Tottey W, Mihajlovski A, Parisot N, Peyretaillade E, Peyret P, Gribaldo S, O’Toole PW, Brugère J-F (2012) Genome sequence of “Candidatus Methanomethylophilus alvus” Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogenic Archaea. J Bacteriol 194:6944–6945. https://​doi.​org/​10.​1128/​JB.​01867-12 CrossRefPubMedPubMedCentral
16.
go back to reference Ferrari A, Brusa T, Rutili A, Canzi E, Biavati B (1994) Isolation and characterization of Methanobrevibacter oralis sp. nov. Curr Microbiol 29:7–12CrossRef Ferrari A, Brusa T, Rutili A, Canzi E, Biavati B (1994) Isolation and characterization of Methanobrevibacter oralis sp. nov. Curr Microbiol 29:7–12CrossRef
17.
go back to reference Nguyen-Hieu T, Khelaifia S, Aboudharam G, Drancourt M (2013) Methanogenic archaea in subgingival sites: a review. APMIS Acta Pathol Microbiol Immunol Scand 121:467–477CrossRef Nguyen-Hieu T, Khelaifia S, Aboudharam G, Drancourt M (2013) Methanogenic archaea in subgingival sites: a review. APMIS Acta Pathol Microbiol Immunol Scand 121:467–477CrossRef
19.
go back to reference Gaci N, Borrel G, Tottey W, O’Toole PW, Brugère JF (2014) Archaea and the human gut: new beginning of an old story. World J Gastroenterol 20:16062–16078CrossRef Gaci N, Borrel G, Tottey W, O’Toole PW, Brugère JF (2014) Archaea and the human gut: new beginning of an old story. World J Gastroenterol 20:16062–16078CrossRef
20.
go back to reference Demonfort Nkamga V, Armstrong N, Drancourt M (2017) In vitro susceptibility of cultured human methanogens to lovastatin. Int J Antimicrob Agents 49:176–182CrossRef Demonfort Nkamga V, Armstrong N, Drancourt M (2017) In vitro susceptibility of cultured human methanogens to lovastatin. Int J Antimicrob Agents 49:176–182CrossRef
21.
go back to reference Koskinen K, Pausan MR, Perras AK, Beck M, Bang C, Mora M, Schilhabel A, Schmitz R, Moissl-Eichinger C (2017) First insights into the diverse human archaeome: specific detection of archaea in the gastrointestinal tract, lung, and nose and on skin. MBio 8(6):Pii: e00824-17. https://doi.org/10.1128/mBio.00824-17 CrossRef Koskinen K, Pausan MR, Perras AK, Beck M, Bang C, Mora M, Schilhabel A, Schmitz R, Moissl-Eichinger C (2017) First insights into the diverse human archaeome: specific detection of archaea in the gastrointestinal tract, lung, and nose and on skin. MBio 8(6):Pii: e00824-17. https://​doi.​org/​10.​1128/​mBio.​00824-17 CrossRef
24.
go back to reference Ishaq SL, Moses PL, Wright A-DG (2016) The pathology of methanogenic archaea in human gastrointestinal tract disease. In: Mozsik G (ed) The Gut Microbiome - Implications for Human Disease. InTech. https://doi.org/10.5772/61423 Ishaq SL, Moses PL, Wright A-DG (2016) The pathology of methanogenic archaea in human gastrointestinal tract disease. In: Mozsik G (ed) The Gut Microbiome - Implications for Human Disease. InTech. https://​doi.​org/​10.​5772/​61423
28.
go back to reference Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogenic Archaea: reevaluation of a unique biological group. Microbiol Rev 43:260–296PubMedPubMedCentral Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogenic Archaea: reevaluation of a unique biological group. Microbiol Rev 43:260–296PubMedPubMedCentral
33.
go back to reference Weaver GA, Krause JA, Miller TL, Wolin MJ (1986) Incidence of methanogenic bacteria in a sigmoidoscopy population: an association of methanogenic bacteria and diverticulosis. Gut 27:698–704CrossRef Weaver GA, Krause JA, Miller TL, Wolin MJ (1986) Incidence of methanogenic bacteria in a sigmoidoscopy population: an association of methanogenic bacteria and diverticulosis. Gut 27:698–704CrossRef
38.
go back to reference Zhang H et al (2009) Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA 106:2365–2370CrossRef Zhang H et al (2009) Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA 106:2365–2370CrossRef
40.
go back to reference Million M, Tidjani Alou M, Khelaifia S, Bachar D, Lagier J-C, Dione N, Brah S, Hugon P, Lombard V, Armougom F, Fromonot J, Robert C, Michelle C, Diallo A, Fabre A, Guieu R, Sokhna C, Henrissat B, Parola P, Raoult D (2016) Increased gut redox and depletion of anaerobic and methanogenic prokaryotes in severe acute malnutrition. Sci Rep 6:26051CrossRef Million M, Tidjani Alou M, Khelaifia S, Bachar D, Lagier J-C, Dione N, Brah S, Hugon P, Lombard V, Armougom F, Fromonot J, Robert C, Michelle C, Diallo A, Fabre A, Guieu R, Sokhna C, Henrissat B, Parola P, Raoult D (2016) Increased gut redox and depletion of anaerobic and methanogenic prokaryotes in severe acute malnutrition. Sci Rep 6:26051CrossRef
52.
go back to reference Ramiro FS, de Lira E, Soares G, Retamal-Valdes B, Feres M, Figueiredo LC, Faveri M (2018) Effects of different periodontal treatments in changing the prevalence and levels of Archaea present in the subgingival biofilm of subjects with periodontitis: a secondary analysis from a randomized controlled clinical trial. Int J Dent Hyg 16:569–575. https://doi.org/10.1111/idh.12347 CrossRefPubMed Ramiro FS, de Lira E, Soares G, Retamal-Valdes B, Feres M, Figueiredo LC, Faveri M (2018) Effects of different periodontal treatments in changing the prevalence and levels of Archaea present in the subgingival biofilm of subjects with periodontitis: a secondary analysis from a randomized controlled clinical trial. Int J Dent Hyg 16:569–575. https://​doi.​org/​10.​1111/​idh.​12347 CrossRefPubMed
63.
go back to reference Bond JH Jr, Engel RR, Levitt MD Factors influencing pulmonary methane excretion in man. An indirect method of studying the in situ metabolism of the methane-producing colonic bacteria (1971). J Exp Med 133:572–588 Bond JH Jr, Engel RR, Levitt MD Factors influencing pulmonary methane excretion in man. An indirect method of studying the in situ metabolism of the methane-producing colonic bacteria (1971). J Exp Med 133:572–588
69.
go back to reference Bernatchez E, Gold MJ, Langlois A, Blais-Lecours P, Boucher M, Duchaine C, Marsolais D, McNagny KM, Blanchet M-R (2017) Methanosphaera stadtmanae induces a type IV hypersensitivity response in a mouse model of airway inflammation. Physiol rep 5:e13163. Doi: https://doi.org/10.14814/phy2.13163 CrossRef Bernatchez E, Gold MJ, Langlois A, Blais-Lecours P, Boucher M, Duchaine C, Marsolais D, McNagny KM, Blanchet M-R (2017) Methanosphaera stadtmanae induces a type IV hypersensitivity response in a mouse model of airway inflammation. Physiol rep 5:e13163. Doi: https://​doi.​org/​10.​14814/​phy2.​13163 CrossRef
72.
go back to reference Sprott GD, Tolson DL, Patel GB (1997) Archaeosomes as novel antigen delivery systems. FEMS Microbiol Lett 154:17–22CrossRef Sprott GD, Tolson DL, Patel GB (1997) Archaeosomes as novel antigen delivery systems. FEMS Microbiol Lett 154:17–22CrossRef
74.
go back to reference Johansson SG, Hourihane JO, Bousquet J, Bruijnzeel-Koomen C, Dreborg S, Haahtela T, Kowalski ML, Mygind N, Ring J, van Cauwenberge P, van Hage-Hamsten M, Wüthrich B EAACI (the European Academy of Allergology and Cinical Immunology) nomenclature task force (2001) A revised nomenclature for allergy. An EAACI position statement from the EAACI nomenclature task force. Allergy 56:813–824 Review. Erratum in: Allergy 2001 Dec;56(12):1229 Johansson SG, Hourihane JO, Bousquet J, Bruijnzeel-Koomen C, Dreborg S, Haahtela T, Kowalski ML, Mygind N, Ring J, van Cauwenberge P, van Hage-Hamsten M, Wüthrich B EAACI (the European Academy of Allergology and Cinical Immunology) nomenclature task force (2001) A revised nomenclature for allergy. An EAACI position statement from the EAACI nomenclature task force. Allergy 56:813–824 Review. Erratum in: Allergy 2001 Dec;56(12):1229
80.
go back to reference Kummeling I, Thijs C, Huber M, van de Vijver LP, Snijders BE, Penders J, Stelma F, van Ree R, van den Brandt PA, Dagnelie PC (2008) Consumption of organic foods and risk of atopic disease during the first 2 years of life in the Netherlands. Br J Nutr 99:598–605CrossRef Kummeling I, Thijs C, Huber M, van de Vijver LP, Snijders BE, Penders J, Stelma F, van Ree R, van den Brandt PA, Dagnelie PC (2008) Consumption of organic foods and risk of atopic disease during the first 2 years of life in the Netherlands. Br J Nutr 99:598–605CrossRef
85.
go back to reference Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, Blanchard C, Junt T, Nicod LP, Harris NL, Marsland BJ (2014) Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 20:159–166. https://doi.org/10.1038/nm.3444 CrossRefPubMed Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, Blanchard C, Junt T, Nicod LP, Harris NL, Marsland BJ (2014) Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 20:159–166. https://​doi.​org/​10.​1038/​nm.​3444 CrossRefPubMed
Metadata
Title
Methanogenic Archaea: Emerging Partners in the Field of Allergic Diseases
Authors
Youssouf Sereme
Soraya Mezouar
Ghiles Grine
Jean Louis Mege
Michel Drancourt
Pierre Corbeau
Joana Vitte
Publication date
01-12-2019
Publisher
Springer US
Published in
Clinical Reviews in Allergy & Immunology / Issue 3/2019
Print ISSN: 1080-0549
Electronic ISSN: 1559-0267
DOI
https://doi.org/10.1007/s12016-019-08766-5

Other articles of this Issue 3/2019

Clinical Reviews in Allergy & Immunology 3/2019 Go to the issue