Abstract

Rumen fermentation affects ruminants productivity and the environmental impact of ruminant production. The release to the atmosphere of methane produced in the rumen is a loss of energy and a cause of climate change, and the profile of volatile fatty acids produced in the rumen affects the post-absorptive metabolism of the host animal. Rumen fermentation is shaped by intracellular and intercellular flows of metabolic hydrogen centered on the production, interspecies transfer, and incorporation of dihydrogen into competing pathways. Factors that affect the growth of methanogens and the rate of feed fermentation impact dihydrogen concentration in the rumen, which in turn controls the balance between pathways that produce and incorporate metabolic hydrogen, determining methane production and the profile of volatile fatty acids. A basic kinetic model of competition for dihydrogen is presented, and possibilities for intervention to redirect metabolic hydrogen from methanogenesis toward alternative useful electron sinks are discussed. The flows of metabolic hydrogen toward nutritionally beneficial sinks could be enhanced by adding to the rumen fermentation electron acceptors or direct fed microbials. It is proposed to screen hydrogenotrophs for dihydrogen thresholds and affinities, as well as identifying and studying microorganisms that produce and utilize intercellular electron carriers other than dihydrogen. These approaches can allow identifying potential microbial additives to compete with methanogens for metabolic hydrogen. The combination of adequate microbial additives or electron acceptors with inhibitors of methanogenesis can be effective approaches to decrease methane production and simultaneously redirect metabolic hydrogen toward end products of fermentation with a nutritional value for the host animal. The design of strategies to redirect metabolic hydrogen from methane to other sinks should be based on knowledge of the physicochemical control of rumen fermentation pathways. The application of new –omics techniques together with classical biochemistry methods and mechanistic modeling can lead to exciting developments in the understanding and manipulation of the flows of metabolic hydrogen in rumen fermentation.

Highlights

  • The complex microbial community that inhabits the rumen allows ruminants to digest and transform fibrous carbohydrates unavailable to humans into useful products such as meat, milk, wool and traction

  • Part of the negative Gibbs energy change ( G) associated with fermentation is used by rumen microbes to generate ATP that can be utilized for microbial growth, active transport of substrates, and motility

  • The terms in the following list are in some cases defined bearing in mind their main significance with regard to rumen energy metabolism, acknowledging that other aspects might be more important in other areas of science

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Summary

Introduction

The complex microbial community that inhabits the rumen allows ruminants to digest and transform fibrous carbohydrates unavailable to humans into useful products such as meat, milk, wool and traction. Carbohydrates are incompletely oxidized to volatile fatty acids (VFA) and gases, with the host animal absorbing and utilizing the VFA as sources and precursors of energy, fat, glucose, and non-essential amino acids (Armstrong and Blaxter, 1957). Part of the negative Gibbs energy change ( G) associated with fermentation is used by rumen microbes to generate ATP that can be utilized for microbial growth, active transport of substrates, and motility. Electron (e−) – a negatively charged sub-atomic particle. Proton (p+ or H+) – a positively charged sub-atomic particle released by acids in aqueous solutions. Metabolic hydrogen ([H]) – the sum of all hydrogen atoms that can be exchanged between molecules in a living cell or a microbial ecosystem, or any other defined living system The terms in the following list are in some cases defined bearing in mind their main significance with regard to rumen energy metabolism, acknowledging that other aspects might be more important in other areas of science.

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