Abstract

BackgroundMethane is an end product of microbial fermentation in the human gastrointestinal tract. This gas is solely produced by an archaeal subpopulation of the human microbiome. Increased methane production has been associated with abdominal pain, bloating, constipation, IBD, CRC or other conditions. Twenty percent of the (healthy) Western populations innately exhale substantially higher amounts (>5 ppm) of this gas. The underlying principle for differential methane emission and its effect on human health is not sufficiently understood.ResultsWe assessed the breath methane content, the gastrointestinal microbiome, its function and metabolome, and dietary intake of one-hundred healthy young adults (female: n = 52, male: n = 48; mean age =24.1). On the basis of the amount of methane emitted, participants were grouped into high methane emitters (CH4 breath content 5–75 ppm) and low emitters (CH4 < 5 ppm).The microbiomes of high methane emitters were characterized by a 1000-fold increase in Methanobrevibacter smithii. This archaeon co-occurred with a bacterial community specialized on dietary fibre degradation, which included members of Ruminococcaceae and Christensenellaceae. As confirmed by metagenomics and metabolomics, the biology of high methane producers was further characterized by increased formate and acetate levels in the gut. These metabolites were strongly correlated with dietary habits, such as vitamin, fat and fibre intake, and microbiome function, altogether driving archaeal methanogenesis.ConclusionsThis study enlightens the complex, multi-level interplay of host diet, genetics and microbiome composition/function leading to two fundamentally different gastrointestinal phenotypes and identifies novel points of therapeutic action in methane-associated disorders.E5uGhR_nPwQ9UQbMdGiGq3Video

Highlights

  • Methane is an end product of microbial fermentation in the human gastrointestinal tract

  • Based on the amount of methane emitted, participants were grouped into high-methane emitters (HE; CH4 value: 5–75 ppm) and low emitters (LE; CH4 value < 5 ppm)

  • Fifteen percent of the participants were categorized as HEs (Supplementary Table 2), with the percentage in congruence with known levels of methane emission of young adult European cohorts [9]

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Summary

Introduction

Methane is an end product of microbial fermentation in the human gastrointestinal tract. This gas is solely produced by an archaeal subpopulation of the human microbiome. Methane is the metabolic end-product of a non-bacterial sub-population of the gastrointestinal microbiome, namely the archaeome [1]. Methane is not utilized by the human itself, elevated methane levels, measured in breath, have been linked with small intestinal bacterial overgrowth, colorectal cancer, diverticulosis and other gastrointestinal disorders (summarized in [2]). Methane-forming archaea (‘methanogens’) in the gastrointestinal tract (GIT) were first observed long ago—through the detection of methane in the human breath and flatus (see [5, 6]). The role of methanogens per se in health and disease is not yet clear, and analyses suffer from methodological pitfalls to correctly detect and characterize the human archaeome as well as the contradictory information that appears in the literature (reviewed in [1])

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