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World J Gastroenterol. Nov 21, 2014; 20(43): 16062-16078
Published online Nov 21, 2014. doi: 10.3748/wjg.v20.i43.16062
Archaea and the human gut: New beginning of an old story
Nadia Gaci, Guillaume Borrel, William Tottey, Paul William O’Toole, Jean-François Brugère
Nadia Gaci, William Tottey, Jean-François Brugère, EA-4678 CIDAM, Clermont Université, Université d’Auvergne, F-63000 Clermont-Ferrand, France
Guillaume Borrel, Paul William O’Toole, School of Microbiology and Alimentary Pharmabiotic Centre, University College Cork, Cork, Ireland
Author contributions: Gaci N and Borrel G contributed equally to this work; Gaci N compiled the data concerning methanogens and several human diseases; Borrel G compiled information about the available genomics data and analyzed the presence of the genes coding MtaA, MtaB, MtaC and BSH; Gaci N, Borrel G, Tottey W, O’Toole PW and Brugère JF wrote the paper.
Supported by PhD Scholarship from the French “Ministère de l’Enseignement Supérieur et de la Recherche” (To Nadia Gaci); Science Foundation Ireland through a postdoctoral grant of the Alimentary Pharmabiotic Centre (to Guillaume Borrel); PhD Scholarship of the European Union (UE) and the Auvergne Council (FEDER) (to William Tottey); Science Foundation Ireland through a Principal Investigator award and by an FHRI award to the ELDERMET project by the Department Agriculture, Fisheries and Marine of the Government of Ireland (to Paul W O’Toole)
Correspondence to: Jean-François Brugère, PhD, EA-4678 CIDAM, Clermont Université, Université d’Auvergne, 28 Place Henri Dunant, BP 10448, F-63000 Clermont-Ferrand, France. jf.brugere@udamail.fr
Telephone: +33-473-178391 Fax: +33-473-178392
Received: March 13, 2014
Revised: May 14, 2014
Accepted: July 22, 2014
Published online: November 21, 2014
Processing time: 251 Days and 23.9 Hours
Abstract

Methanogenic archaea are known as human gut inhabitants since more than 30 years ago through the detection of methane in the breath and isolation of two methanogenic species belonging to the order Methanobacteriales, Methanobrevibacter smithii and Methanosphaera stadtmanae. During the last decade, diversity of archaea encountered in the human gastrointestinal tract (GIT) has been extended by sequence identification and culturing of new strains. Here we provide an updated census of the archaeal diversity associated with the human GIT and their possible role in the gut physiology and health. We particularly focus on the still poorly characterized 7th order of methanogens, the Methanomassiliicoccales, associated to aged population. While also largely distributed in non-GIT environments, our actual knowledge on this novel order of methanogens has been mainly revealed through GIT inhabitants. They enlarge the number of final electron acceptors of the gut metabolites to mono- di- and trimethylamine. Trimethylamine is exclusively a microbiota-derived product of nutrients (lecithin, choline, TMAO, L-carnitine) from normal diet, from which seems originate two diseases, trimethylaminuria (or Fish-Odor Syndrome) and cardiovascular disease through the proatherogenic property of its oxidized liver-derived form. This therefore supports interest on these methanogenic species and its use as archaebiotics, a term coined from the notion of archaea-derived probiotics.

Keywords: Human gut microbiota; Methanogens; Methanomassiliicoccus; Methanomethylophilus; Trimethylaminuria; Trimethylamine; Methane; Cardiovascular disease; Archaebiotics; Probiotics

Core tip: Archaea are naturally occurring components of the human gut microbiota, whose biological significance has been recently reevaluated. In this review, an update of the current knowledge about the archaea from the human gut is provided, integrating the new order of methanogens, Methanomassiliicoccales. By its particular metabolism, this lineage is likely a depleting biological agent of a gut microbiota metabolite from diet implied in cardiovascular disease and trimethylaminuria, trimethylamine. The recent provocative proposal of archaea as a new class of probiotics (archaebiotics) should focus the interest on the third domain of life concerning the gut physiopathology and human health.