Dataset Information

Inhibiting Methanogenesis in Rumen Batch Cultures Did Not Increase the Recovery of Metabolic Hydrogen in Microbial Amino Acids.

ABSTRACT: There is an interest in controlling rumen methanogenesis as an opportunity to both decrease the emissions of greenhouse gases and improve the energy efficiency of rumen fermentation. However, the effects of inhibiting rumen methanogenesis on fermentation are incompletely understood even in in vitro rumen cultures, as the recovery of metabolic hydrogen ([H]) in the main fermentation products consistently decreases with methanogenesis inhibition, evidencing the existence of unaccounted [H] sinks. We hypothesized that inhibiting methanogenesis in rumen batch cultures would redirect [H] towards microbial amino acids (AA) biosynthesis as an alternative [H] sink to methane (CH₄). The objective of this experiment was to evaluate the effects of eight inhibitors of methanogenesis on digestion, fermentation and the production of microbial biomass and AA in rumen batch cultures growing on cellulose. Changes in the microbial community composition were also studied using denaturing gradient gel electrophoresis (DGGE). Inhibiting methanogenesis did not cause consistent changes in fermentation or the profile of AA, although the effects caused by the different inhibitors generally associated with the changes in the microbial community that they induced. Under the conditions of this experiment, inhibiting methanogenesis did not increase the importance of microbial AA synthesis as a [H] sink.

SUBMITTER: Ungerfeld EM

PROVIDER: S-EPMC6560395 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Inhibiting Methanogenesis in Rumen Batch Cultures Did Not Increase the Recovery of Metabolic Hydrogen in Microbial Amino Acids.

Ungerfeld Emilio M EM Aedo M Fernanda MF Martínez Emilio D ED Saldivia Marcelo M

Microorganisms 20190427 5

There is an interest in controlling rumen methanogenesis as an opportunity to both decrease the emissions of greenhouse gases and improve the energy efficiency of rumen fermentation. However, the effects of inhibiting rumen methanogenesis on fermentation are incompletely understood even in in vitro rumen cultures, as the recovery of metabolic hydrogen ([H]) in the main fermentation products consistently decreases with methanogenesis inhibition, evidencing the existence of unaccounted [H] sinks. ...[more]

PMID: 31035537

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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:Mitigation of enteric methane (CH4) emissions from ruminant livestock represents an opportunity to improve the sustainability, productivity, and profitability of beef and dairy production. Ruminal methanogenesis can be mitigated via two primary strategies: (1) alternative electron acceptors and (2) enzymatic inhibition of methanogenic pathways. The former utilizes the thermodynamic favorability of certain reactions such as nitrate/nitrite reduction to ammonia (NH3) while the latter targets specific enzymes using structural analogs of CH4 and methanogenic cofactors such as bromochloromethane (BCM). In this study, we investigated the effects of four additives and their combinations on CH4 production by rumen microbes in batch culture. Sodium nitrate (NaNO3), sodium sulfate (Na2SO4), and 3-nitro-1-propionate (3NPA) were included as thermodynamic inhibitors, whereas BCM was included as a enzymatic inhibitor. Individual additives were evaluated at three levels of inclusion in experiments 1 and 2. Highest level of each additive was used to determine the combined effect of NaNO3 + Na2SO4 (NS), NS + 3NPA (NSP), and NSP + BCM (NSPB) in experiments 3 and 4. Experimental diets were high, medium, and low forage diets (HF, MF, and LF, respectively) and consisted of alfalfa hay and a concentrate mix formulated to obtain the following forage to concentrate ratios: 70:30, 50:50, and 30:70, respectively. Diets with additives were placed in fermentation culture bottles and incubated in a water bath (39°C) for 6, 12, or 24h. Microbial DNA was extracted for 16S rRNA and ITS gene amplicon sequencing. In experiments 1 and 2, CH4 concentrations in control cultures decreased in the order of LF, MF, and HF diets, whereas in experiments 3 and 4, CH4 was highest in MF diet followed by HF and LF diets. Culture pH and NH3 in the control decreased in the order of HF, MF, to LF as expected. NaNO3 decreased (p < 0.001) CH4 and butyrate and increased acetate and propionate (p < 0.03 and 0.003, respectively). Cultures receiving NaNO3 had an enrichment of microorganisms capable of nitrate and nitrite reduction. 3NPA also decreased CH4 at 6h with no further decrease at 24 h (p < 0.001). BCM significantly inhibited methanogenesis regardless of inclusion levels as well as in the presence of the thermodynamic inhibitors (p < 0.001) while enriching succinate producers and assimilators as well as propionate producers (p adj < 0.05). However, individual inclusion of BCM decreased total short chain fatty acid (SCFA) concentrations (p < 0.002). Inhibition of methanogenesis with BCM individually and in combination with the other additives increased gaseous H2 concentrations (p < 0.001 individually and 0.028 in combination) while decreasing acetate to propionate ratio (p < 0.001). Only the cultures treated with BCM in combination with other additives significantly (padj < 0.05) decreased the abundance of Methanobrevibacter expressed as log fold change. Overall, the combination of thermodynamic and enzymatic inhibitors presented a promising effect on ruminal fermentation in-vitro, inhibiting methanogenesis while optimizing the other fermentation parameters such as pH, NH3, and SCFAs. Here, we provide a proof of concept that the combination of an electron acceptor and a methane analog may be exploited to improve microbial efficiency via methanogenesis inhibition.

Project description:Strategies to manage metabolic hydrogen ([H]) in the rumen should be considered when reducing ruminant methane (CH4) emissions. However, little is known about the use of dietary treatments to stimulate rumen microorganisms capable of capturing the [H] available when CH4 is inhibited in vivo. The effects of the phenolic compound phloroglucinol on CH4 production, [H] flows and subsequent responses in rumen fermentation and microbial community composition when methanogenesis is inhibited were investigated in cattle. Eight rumen fistulated Brahman steers were randomly allocated in two groups receiving chloroform as an antimethanogenic compound for 21 days. Following that period one group received chloroform + phloroglucinol for another 16 days, whilst the other group received only chloroform during the same period. The chloroform treatment resulted in a decrease in CH4 production and an increase in H2 expelled with a shift in rumen fermentation toward higher levels of propionate and formate and lower levels of acetate at day 21 of treatment. Bacterial operational taxonomic units (OTUs) assigned to Prevotella were promoted whilst Archaea and Synergistetes OTUs were decreased with the chloroform treatment as expected. The shift toward formate coincided with increases in Ruminococcus flavefaciens, Butyrivibrio fibrisolvens, and Methanobrevibacter ruminantium species. The addition of chloroform + phloroglucinol in the rumen resulted in a decrease of H2 expelled (g) per kg of DMI and moles of H2 expelled per mol of CH4 decreased compared with the chloroform only treated animals. A shift toward acetate and a decrease in formate were observed for the chloroform + phloroglucinol-treated animals at day 37. These changes in the rumen fermentation profile were accompanied by a relative increase of OTUs assigned to Coprococcus spp., which could suggest this genus is a significant contributor to the metabolism of this phenolic compound in the rumen. This study demonstrates for the first time in vivo that under methanogenesis inhibition, H2 gas accumulation can be decreased by redirecting [H] toward alternative sinks through the nutritional stimulation of specific microbial groups. This results in the generation of metabolites of value for the host while also helping to maintain a low H2 partial pressure in the methane-inhibited rumen.

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

Inhibiting Methanogenesis in Rumen Batch Cultures Did Not Increase the Recovery of Metabolic Hydrogen in Microbial Amino Acids.

Publications

Inhibiting Methanogenesis in Rumen Batch Cultures Did Not Increase the Recovery of Metabolic Hydrogen in Microbial Amino Acids.

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