Abstract
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.
Highlights
In the rumen, metabolic hydrogen ([2H]) is released during the fermentation of feed by bacteria, protozoa and fungi
Overall total greenhouse gas (GHG) produced was different among treatments (P < 0.001) with NIT and NOP producing less GHG compared to control treatment (CON) and AQ (−73%)
Dissolved H2 concentration differed among treatments, with the greatest concentration recorded for NOP, followed in descending order by CON, NIT and AQ (P < 0.001)
Summary
Metabolic hydrogen ([2H]) is released during the fermentation of feed by bacteria, protozoa and fungi. Metabolic hydrogen transfer to different acceptors ensures the continuity of fermentation by re-oxidizing reduced co-factors. Dihydrogen (H2) is produced when electrons are transferred to protons in reactions catalyzed by hydrogenases (Hegarty and Gerdes, 1999). Hydrogenase activity can be inhibited by an accumulation of H2, with bacterial hydrogenases ([Ni-Fe] hydrogenases) being more sensitive than protozoal hydrogenases ([Fe-Fe] hydrogenases) (Fourmond et al, 2013). Metabolic hydrogen can be incorporated into other pathways, including propionate, methane (CH4) and microbial protein synthesis (Henderson, 1980; Czerkawski, 1986; Asanuma et al, 1999). The flow of [2H] is key to energy metabolism, driving most fermentation pathways (Janssen, 2010), which has a major impact on ruminant nutrition
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