Limits to Dihydrogen Incorporation into Electron Sinks Alternative to Methanogenesis in Ruminal Fermentation.

Emilio M Ungerfeld

doi:10.3389/fmicb.2015.01272

Abstract

Research is being conducted with the objective of decreasing methane (CH4) production in the rumen, as methane emissions from ruminants are environmentally damaging and a loss of digestible energy to ruminants. Inhibiting ruminal methanogenesis generally results in accumulation of dihydrogen (H2), which is energetically inefficient and can inhibit fermentation. It would be nutritionally beneficial to incorporate accumulated H2 into propionate or butyrate production, or reductive acetogenesis. The objective of this analysis was to examine three possible physicochemical limitations to the incorporation of accumulated H2 into propionate and butyrate production, and reductive acetogenesis, in methanogenesis-inhibited ruminal batch and continuous cultures: (i) Thermodynamics; (ii) Enzyme kinetics; (iii) Substrate kinetics. Batch (N = 109) and continuous (N = 43) culture databases of experiments with at least 50% inhibition in CH4 production were used in this meta-analysis. Incorporation of accumulated H2 into propionate production and reductive acetogenesis seemed to be thermodynamically feasible but quite close to equilibrium, whereas this was less clear for butyrate. With regard to enzyme kinetics, it was speculated that hydrogenases of ruminal microorganisms may have evolved toward high-affinity and low maximal velocity to compete for traces of H2, rather than for high pressure accumulated H2. Responses so far obtained to the addition of propionate production intermediates do not allow distinguishing between thermodynamic and substrate kinetics control.

Highlights

Methanogenesis is the main electron sink in ruminal fermentation
This requirement increases variation in the regressor and decreases the proportion of variation in ∆G associated to the experiment effect, resulting in greater power to test the hypotheses of responses of ∆G to methanogenesis inhibition; (iv) Treatments within experiments consisting in combinations of methanogenesis inhibitors and fermentation intermediates or their isomers or analogs were discarded, as intermediates whose concentration was not reported could affect the thermodynamics of the process being studied; Some batch culture studies that did not report net volatile fatty acids (VFA) production were not used in Ungerfeld (2015) meta-analysis but were included in the present study, because only metabolites final concentrations, but not their net production, is necessary to estimate ∆G
Methanogenesis-uninhibited ruminal fermentation, H2 production from reduced cofactors is thermodynamically feasible because H2 concentration is kept very low through rapid removal mainly by methanogenesis (Janssen, 2010)

Summary

INTRODUCTION

Methanogenesis is the main electron sink in ruminal fermentation. Metabolic hydrogen ([H]) released in fermentation is transferred to methanogens mainly as H2 and incorporated into CH4. In a metaanalysis of methanogenesis inhibition in in vitro experiments, incorporation of [H] into propionate production was small for batch culture compared to what the decrease in CH4 production would stoichiometrically allow, and on average non-existent in continuous culture (Ungerfeld, 2015). Propionate and butyrate, and acetate formed through reductive acetogenesis, are nutritionally useful [H] sinks to ruminants as energy and carbon sources. A question of importance is what are the physicochemical limitations to the incorporation of accumulated H2 into propionate and butyrate formation, and reductive acetogenesis, in the methanogenesisinhibited ruminal fermentation. The present analysis calculates thermodynamic limits of the incorporation of accumulated H2 into propionate and butyrate production and reductive acetogenesis, and discusses possible control mechanisms of these processes in the methanogenesisinhibited fermentation

METHODS

RESULTS

DISCUSSION