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

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.

SUBMITTER: Ungerfeld EM

PROVIDER: S-EPMC4316778 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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

Ungerfeld Emilio M EM

Frontiers in microbiology 20150204

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 meth ...[more]

PMID: 25699029

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Project description:A decrease in methanogenesis is expected to improve ruminant performance by allocating rumen metabolic hydrogen ([2H]) to more energy-rendering fermentation pathways for the animal. However, decreases in methane (CH4) emissions of up to 30% are not always linked with greater performance. Therefore, the aim of this study was to understand the fate of [2H] when CH4 production in the rumen is inhibited by known methanogenesis inhibitors (nitrate, NIT; 3-nitrooxypropanol, NOP; anthraquinone, AQ) in comparison with a control treatment (CON) with the Rumen Simulation Technique (RUSITEC). Measurements started after 1 week adaptation. Substrate disappearance was not modified by methanogenesis inhibitors. Nitrate mostly seemed to decrease [2H] availability by acting as an electron acceptor competing with methanogenesis. As a consequence, NIT decreased CH4 production (-75%), dissolved dihydrogen (H2) concentration (-30%) and the percentages of reduced volatile fatty acids (butyrate, isobutyrate, valerate, isovalerate, caproate and heptanoate) except propionate, but increased acetate molar percentage, ethanol concentration and the efficiency of microbial nitrogen synthesis (+14%) without affecting gaseous H2. Nitrooxypropanol decreased methanogenesis (-75%) while increasing both gaseous and dissolved H2 concentrations (+81% and +24%, respectively). Moreover, NOP decreased acetate and isovalerate molar percentages and increased butyrate, valerate, caproate and heptanoate molar percentages as well as n-propanol and ammonium concentrations. Methanogenesis inhibition with AQ (-26%) was associated with higher gaseous H2 production (+70%) but lower dissolved H2 concentration (-76%), evidencing a lack of relationship between the two H2 forms. Anthraquinone increased ammonium concentration, caproate and heptanoate molar percentages but decreased acetate and isobutyrate molar percentages, total microbial nitrogen production and efficiency of microbial protein synthesis (-16%). Overall, NOP and AQ increased the amount of reduced volatile fatty acids, but part of [2H] spared from methanogenesis was lost as gaseous H2. Finally, [2H] recovery was similar among CON, NOP and AQ but was largely lower than 100%. Consequently, further studies are required to discover other so far unidentified [2H] sinks for a better understanding of the metabolic pathways involved in [2H] production and utilization.

Project description:BackgroundGrazing mammals rely on their ruminal microbial symbionts to convert plant structural biomass into metabolites they can assimilate. To explore how this complex metabolic system adapts to the host animal's diet, we inferred a microbiome-level metabolic network from shotgun metagenomic data.ResultsUsing comparative genomics, we then linked this microbial network to that of the host animal using a set of interface metabolites likely to be transferred to the host. When the host sheep were fed a grain-based diet, the induced microbial metabolic network showed several critical differences from those seen on the evolved forage-based diet. Grain-based (e.g., concentrate) diets tend to be dominated by a smaller set of reactions that employ metabolites that are nearer in network space to the host's metabolism. In addition, these reactions are more central in the network and employ substrates with shorter carbon backbones. Despite this apparent lower complexity, the concentrate-associated metabolic networks are actually more dissimilar from each other than are those of forage-fed animals. Because both groups of animals were initially fed on a forage diet, we propose that the diet switch drove the appearance of a number of different microbial networks, including a degenerate network characterized by an inefficient use of dietary nutrients. We used network simulations to show that such disparate networks are not an unexpected result of a diet shift.ConclusionWe argue that network approaches, particularly those that link the microbial network with that of the host, illuminate aspects of the structure of the microbiome not seen from a strictly taxonomic perspective. In particular, different diets induce predictable and significant differences in the enzymes used by the microbiome. Nonetheless, there are clearly a number of microbiomes of differing structure that show similar functional properties. Changes such as a diet shift uncover more of this type of diversity.

Project description: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.

Project description:Methane (CH4) formed in the rumen and released to the atmosphere constitutes an energy inefficiency to ruminant production. Redirecting energy in CH4 to fermentation products with a nutritional value to the host animal could increase ruminant productivity and stimulate the adoption of CH4-suppressing strategies. The hypothesis of this research was that inhibiting CH4 formation in the rumen is associated with greater ruminant productivity. The primary objective of this meta-analysis was to evaluate how inhibiting rumen methanogenesis relates with the efficiencies of milk production and growth and fattening. A systematic review of peer-reviewed studies in which rumen methanogenesis was inhibited with chemical compounds was conducted. Experiments were clustered based on research center, year of publication, experimental design, feeding regime, type of animal, production response, inhibitor of CH4 production, and method of CH4 measurement. Response variables were regressed against the random experiment effect nested in its cluster, the random effect of the cluster, the linear and quadratic effects of CH4 production, and the random interaction between CH4 production and the experiment nested in the cluster. When applicable, responses were adjusted by intake of different nutrients included as regressors. Inhibiting rumen methanogenesis tended to associate positively with milk production efficiency, although the relationship was influenced by individual experiments. Likewise, a positive relationship between methanogenesis inhibition and growth and fattening efficiency depended on the inclusion and weighting of individual experiments. Inhibiting rumen methanogenesis negatively associated with dry matter intake. Interpretation of the effects of inhibiting methanogenesis on productivity is limited by the availability of experiments simultaneously reporting energy losses in feces, H2, urine and heat production, as well as net energy partition. It is concluded that inhibiting rumen methanogenesis has not consistently translated into greater animal productivity, and more animal performance experiments are necessary to better characterize the relationships between animal productivity and methanogenesis inhibition in the rumen. A more complete understanding of changes in the flows of nutrients caused by inhibiting rumen methanogenesis and their effect on intake also seems necessary to effectively re-channel energy gained from CH4 suppression toward consistent gains in productivity.

Dataset Information

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

Publications

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

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