Thermodynamic feasibility of methanogenesis and acetogenesis and associated microbiota abundance in the bovine rumen
Creators: name: van Lingen, Henk J.
Publisher: name: Zenodo
Year: 2025
Subjects: microbial physiology
cattle
hydrogen utilization

description: Fermentation in the ruminal ecosystem of cattle generates a surplus of hydrogen. Hydrogenotrophic methanogenesis, the production of methane from hydrogen and carbon dioxide, is the most common hydrogen-utilizing pathway in the rumen. Methylotrophic methanogenesis, the production of methane from hydrogen and a methyl-containing substrate (e.g. methanol, methylamine), is considered to have a minor but significant contribution to hydrogen utilization. Furthermore, reductive acetogenesis, the production of acetate from hydrogen and carbon dioxide, occurs in anaerobic ecosystems, but the significance of this pathway in the rumen is debatable. Hydrogen partial pressure may largely control the thermodynamic feasibility of reductive acetogenesis, which requires a relatively high threshold of hydrogen partial pressure. Metabolic activity of these pathways may be reflected by the relative abundance of microbiota capable of employing them. The aim is to quantify the thermodynamic feasibility of hydrogenotrophic and methylotrophic methanogenesis and reductive acetogenesis in the rumen, along with identifying the abundance of microbiota employing these three metabolic pathways.

The thermodynamic control of hydrogen partial pressure on hydrogen-utilizing pathways in the rumen was quantified using the thermodynamic potential factor (FT; Jin & Bethke, 2007). This dimensionless factor determines the thermodynamic control exerted on a metabolic conversion by accounting for the difference between the Gibbs energy available through fermentation and the Gibbs energy that may be conserved in ATP. Methanol, methylamine and carbon dioxide concentrations were assumed 1, 1 and 40 mM, respectively, pH 6.5 and methane partial pressure 0.25 bar. Data was taken from a previously published study in which hydrogen partial pressure and microbiota composition in the rumen of cows were monitored at 0, 0.5, 1, 1.5, 2, 3, 4, 6, 8 and 10 h from feeding (Van Lingen et al., 2017). Redundancy analysis was performed for assessing the relationship between microbiota employing the three hydrogen-utilizing pathways and the actual hydrogen partial pressure.

 The FT for methylotrophic methanogenesis approached unity for the ruminal range of hydrogen partial pressure, whereas for hydrogenotrophic methanogenesis and reductive acetogenesis, FT increased from zero to unity, i.e. from complete inhibition to completely feasible, over the ranges of 0.03 to 0.5 and 0.4 to 10 mbar of hydrogen partial pressure, respectively.

Redundancy analysis indicated methanogenic Methanobrevibacter and Methanosphaera genera were correlated to the timepoints at 0.5 and 1 h after supplying feed to the cows that had the highest hydrogen partial pressure, with phylogenetic groupings annotated to the Methanobacteriales order were correlated with the 2 and 3 h timepoints at which hydrogen partial pressure was submaximal. Acetogenic Blautia and Acetitomaculum genera were correlated to the 4 h timepoint, whereas phylogenetic groupings annotated to the Lachnospiraceae family were correlated to the 6 and 10 h timepoints that had lower hydrogen partial pressure.

Reductive acetogenesis is feasible, but only at the higher end ruminal hydrogen partial pressure. Metabolic functionality of the microbiota correlated with the different time points need more thorough exploration, but methanogens were associated with earlier timepoints than microbiota that are considered acetogenic. A possible delay effect in acetogenic abundance relative to timepoints with the highest hydrogen partial pressure requires further investigation.

References

1.    Q. Jin and C.M. Bethke. “The thermodynamics and kinetics of microbial metabolism”. Am. J. Sci. 307:643–677, 2007.

2.    H.J. van Lingen et al., “Diurnal Dynamics of Gaseous and Dissolved Metabolites and Microbiota Composition in the Bovine Rumen”. Front. Microbiol. 8:425, 2017.