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

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.

Urea plus nitrate pretreatment of rice and wheat straws enhances degradation and reduces methane production inin vitroruminal culture

“…Increased hydrogen helps to redirect it into alternative sinks, such as propiogenesis . However, that sink may not efficiently incorporate all released hydrogen from methane inhibition because reactions of reductive propiogenesis have Gibbs energy changes that are similar to those of ATP generation …”

Metabolic Hydrogen Flows in Rumen Fermentation: Principles and Possibilities of Interventions

“…In 48 h batch cultures, there were distinct effects of pH and substrate composition (hay or cracked corn) on H 2 , CH 4 and the acetate to propionate ratio (Russell, 1998), which can also be interpreted as an indication of an effect of the rate of fermentation per se independent of outflow rates or pH. It has also been speculated that the evolution of rumen H 2incorporating hydrogenases in the rumen environment with low H 2 concentration may have resulted in low K m but also low V max for H 2 (Ungerfeld, 2015a). This idea, however, does not agree with the high frequency of genomes of rumen organisms encoding [FeFe]-hydrogenases, and the high abundance of transcripts of various types of [FeFe]-hydrogenases in sheep rumens (Greening et al, 2019), as [FeFe]-hydrogenases have higher V max and K m for H 2 uptake than [NiFe] hydrogenases (Frey, 2002).…”

“…The incorporation of [H] into pathways alternative to methanogenesis can be limited by enzyme or substrate kinetics, or thermodynamics (Ungerfeld, 2015a). The addition of an e − acceptor that can be metabolized to VFA can help removing substrate kinetics or thermodynamic constraints.…”

Phloroglucinol Degradation in the Rumen Promotes the Capture of Excess Hydrogen Generated from Methanogenesis Inhibition

“…Although methanogens are the main H 2 consumers, due to the thermodynamically favorable pathway of CH 4 formation, there are rumen bacteria, which are also able to use H 2 as substrate thus generating alternative end products ( Leng, 2014 ). Thus, when CH 4 production is decreased, [H] might be redirected into alternative sinks nutritionally useful for the ruminant ( Ungerfeld, 2015a ). However, an excessive increase of the H 2 partial pressure in the rumen after methane inhibition might have detrimental effects on rumen function ( Wolin et al, 1997 ).…”