Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis

Emilio M Ungerfeld

doi:10.3389/fmicb.2015.00037

Abstract

Maximizing the flow of metabolic hydrogen ([H]) in the rumen away from CH4 and toward volatile fatty acids (VFA) would increase the efficiency of ruminant production and decrease its environmental impact. The objectives of this meta-analysis were: (i) To quantify shifts in metabolic hydrogen sinks when inhibiting ruminal methanogenesis in vitro; and (ii) To understand the variation in shifts of metabolic hydrogen sinks among experiments and between batch and continuous cultures systems when methanogenesis is inhibited. Batch (28 experiments, N = 193) and continuous (16 experiments, N = 79) culture databases of experiments with at least 50% inhibition in CH4 production were compiled. Inhibiting methanogenesis generally resulted in less fermentation and digestion in most batch culture, but not in most continuous culture, experiments. Inhibiting CH4 production in batch cultures resulted in redirection of metabolic hydrogen toward propionate and H2 but not butyrate. In continuous cultures, there was no overall metabolic hydrogen redirection toward propionate or butyrate, and H2 as a proportion of metabolic hydrogen spared from CH4 production was numerically smaller compared to batch cultures. Dihydrogen accumulation was affected by type of substrate and methanogenesis inhibitor, with highly fermentable substrates resulting in greater redirection of metabolic hydrogen toward H2 when inhibiting methanogenesis, and some oils causing small or no H2 accumulation. In both batch and continuous culture, there was a decrease in metabolic hydrogen recovered as the sum of propionate, butyrate, CH4 and H2 when inhibiting methanogenesis, and it is speculated that as CH4 production decreases metabolic hydrogen could be increasingly incorporated into formate, microbial biomass, and perhaps, reductive acetogenesis in continuous cultures. Energetic benefits of inhibiting methanogenesis depended on the inhibitor and its concentration and on the in vitro system.

Highlights

Despite its importance in transforming fibrous plant biomass non-edible by humans into useful products such as meat and milk, ruminant production contributes with between 7 and 18% of total anthropogenic greenhouse gas emissions, with CH4 release from ruminal fermentation being a principal contributor (Martin et al, 2010; Hristov et al, 2013)
In the typical ruminal fermentation, methanogenesis is the main route of co-factor re-oxidation, with [H] transferred from the fermentative microbiota of bacteria, protozoa and fungi to methanogenic Archaea mainly as H2 (Wolin et al, 1997)
In order to be included in this meta-analysis, experiments had to meet all of the following criteria: (i) Production of CH4, H2 accumulation, and net production of individual volatile fatty acids (VFA) was provided or could be calculated; (ii) Initial headspace was H2-free and formate salts or formic acid were not used as substrate; (iii) The experiment included a methanogenesis-uninhibited control treatment; (iv) At least one treatment or level within a treatment resulted in a 50% or greater decrease in CH4 production relative to the control

Summary

Introduction

Despite its importance in transforming fibrous plant biomass non-edible by humans into useful products such as meat and milk, ruminant production contributes with between 7 and 18% of total anthropogenic greenhouse gas emissions, with CH4 release from ruminal fermentation being a principal contributor (Martin et al, 2010; Hristov et al, 2013). Glucose is mainly metabolized through glycolysis to pyruvate in the rumen (Russell and Wallace, 1997). Glycolysis, and pyruvate oxidative decarboxylation to acetyl-CoA, which is the first step in acetate and butyrate formation, both result in the release of metabolic hydrogen ([H]). Reduced co-factors must be re-oxidized for fermentation to continue. In the typical ruminal fermentation, methanogenesis is the main route of co-factor re-oxidation, with [H] transferred from the fermentative microbiota of bacteria, protozoa and fungi to methanogenic Archaea mainly as H2 (Wolin et al, 1997). The production of propionate, a useful fermentation product which is the main glucose precursor for ruminants, competes with CH4 production for [H] (Janssen, 2010) and H2 (Henderson, 1980). Some [H] is incorporated into butyrate production from pyruvate (Miller and Jenesel, 1979); butyrate production from hexoses results www.frontiersin.org

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