Abstract
Methanogenic archaea occupy a functionally important niche in the gut microbial ecosystem of mammals. Our purpose was to quantitatively characterize the dynamics of methanogenesis by integrating microbiology, thermodynamics and mathematical modelling. For that, in vitro growth experiments were performed with pure cultures of key methanogens from the human and ruminant gut, namely Methanobrevibacter smithii, Methanobrevibacter ruminantium and Methanobacterium formicium. Microcalorimetric experiments were performed to quantify the methanogenesis heat flux. We constructed an energetic-based mathematical model of methanogenesis. Our model captured efficiently the dynamics of methanogenesis with average concordance correlation coefficients of 0.95 for CO2, 0.98 for H2 and 0.97 for CH4. Together, experimental data and model enabled us to quantify metabolism kinetics and energetic patterns that were specific and distinct for each species despite their use of analogous methane-producing pathways. Then, we tested in silico the interactions between these methanogens under an in vivo simulation scenario using a theoretical modelling exercise. In silico simulations suggest that the classical competitive exclusion principle is inapplicable to gut ecosystems and that kinetic information alone cannot explain gut ecological aspects such as microbial coexistence. We suggest that ecological models of gut ecosystems require the integration of microbial kinetics with nonlinear behaviours related to spatial and temporal variations taking place in mammalian guts. Our work provides novel information on the thermodynamics and dynamics of methanogens. This understanding will be useful to construct new gut models with enhanced prediction capabilities and could have practical applications for promoting gut health in mammals and mitigating ruminant methane emissions.
Highlights
Methanogenic archaea inhabit the gastro-intestinal tract of mammals where they have established syntrophic interactions within the microbial community [1,2,3] playing a critical role in the energy balance of the host [4,5]
The microcalorimetry approach we applied revealed that this simplicity is only apparent and that hydrogenotrophic methanogens exhibit energetic and kinetic differences
For M. smithii and M. formicium the main peak was preceded by a small increase in heat flux which translates in a metabolic activity that remains to be elucidated
Summary
Methanogenic archaea inhabit the gastro-intestinal tract of mammals where they have established syntrophic interactions within the microbial community [1,2,3] playing a critical role in the energy balance of the host [4,5]. In the gastrointestinal tract of mammals, major rumen methanogens [13] and the dominant human archaeon M. smithii [14], are hydrogenotrophic archaea without cytochrome (membrane-associated electron transfer proteins). Cytochromelacking methanogens exhibit lower growth yields than archaea with cytochromes [15] This apparent energetic disadvantage has been counterbalanced by a greater adaptation to the environmental conditions prevailing in the gastrointestinal tract [16], and by the establishment of syntrophic interactions with feed fermenting microbes. This syntrophic cooperation centred on hydrogen allows the anaerobic reactions of substrate conversion to proceed close to the thermodynamic equilibrium [17,18] (that is with Gibbs free energy change close to zero)
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