Ruminant livestock are important sources of human food and global greenhouse gas emissions. Feed degradation and methane formation by ruminants rely on metabolic interactions between rumen microbes and affect ruminant productivity. Rumen and camelid foregut microbial community composition was determined in 742 samples from 32 animal species and 35 countries, to estimate if this was influenced by diet, host species, or geography. Similar bacteria and archaea dominated in nearly all samples, while protozoal communities were more variable. The dominant bacteria are poorly characterised, but the methanogenic archaea are better known and highly conserved across the world. This universality and limited diversity could make it possible to mitigate methane emissions by developing strategies that target the few dominant methanogens. Differences in microbial community compositions were predominantly attributable to diet, with the host being less influential. There were few strong co-occurrence patterns between microbes, suggesting that major metabolic interactions are non-selective rather than specific.

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.

Limiting global warming to 1.5°C above pre-industrial levels by 2050 requires achieving net zero emissions of greenhouse gases by 2050 and a strong decrease in methane (CH4) emissions. Our aim was to connect the global need for mitigation of the emissions of greenhouse gases and enteric CH4 from ruminant production to basic research on the biological consequences of inhibiting rumen methanogenesis in order to better design strategies for pronounced mitigation of enteric CH4 production without negative impacts on animal productivity or economic returns. Ruminant production worldwide has the challenge of decreasing its emissions of greenhouse gases while increasing the production of meat and milk to meet consumers demand. Production intensification decreases the emissions of greenhouse gases per unit of product, and in some instances has decreased total emissions, but in other instances has resulted in increased total emissions of greenhouse gases. We propose that decreasing total emission of greenhouse gases from ruminants in the next decades while simultaneously increasing meat and milk production will require strong inhibition of rumen methanogenesis. An aggressive approach to pronounced inhibition of enteric CH4 emissions is technically possible through the use of chemical compounds and/or bromoform-containing algae, but aspects such as safety, availability, government approval, consumer acceptance, and impacts on productivity and economic returns must be satisfactorily addressed. Feeding these additives will increase the cost of ruminant diets, which can discourage their adoption. On the other hand, inhibiting rumen methanogenesis potentially saves energy for the host animal and causes profound changes in rumen fermentation and post-absorptive metabolism. Understanding the biological consequences of methanogenesis inhibition could allow designing strategies to optimize the intervention. We conducted meta-regressions using published studies with at least one treatment with >50% inhibition of CH4 production to elucidate the responses of key rumen metabolites and animal variables to methanogenesis inhibition, and understand possible consequences on post-absorptive metabolism. We propose possible avenues, attainable through the understanding of biological consequences of the methanogenesis inhibition intervention, to increase animal productivity or decrease feed costs when inhibiting methanogenesis.

No abstract

No abstract