RESUMEN
Ruminants are essential for global food security, but these are major sources of the greenhouse gas methane. Methane yield is controlled by the cycling of molecular hydrogen (H2), which is produced during carbohydrate fermentation and is consumed by methanogenic, acetogenic, and respiratory microorganisms. However, we lack a holistic understanding of the mediators and pathways of H2 metabolism and how this varies between ruminants with different methane-emitting phenotypes. Here, we used metagenomic, metatranscriptomic, metabolomics, and biochemical approaches to compare H2 cycling and reductant disposal pathways between low-methane-emitting Holstein and high-methane-emitting Jersey dairy cattle. The Holstein rumen microbiota had a greater capacity for reductant disposal via electron transfer for amino acid synthesis and propionate production, catalyzed by enzymes such as glutamate synthase and lactate dehydrogenase, and expressed uptake [NiFe]-hydrogenases to use H2 to support sulfate and nitrate respiration, leading to enhanced coupling of H2 cycling with less expelled methane. The Jersey rumen microbiome had a greater proportion of reductant disposal via H2 production catalyzed by fermentative hydrogenases encoded by Clostridia, with H2 mainly taken up through methanogenesis via methanogenic [NiFe]-hydrogenases and acetogenesis via [FeFe]-hydrogenases, resulting in enhanced methane and acetate production. Such enhancement of electron incorporation for metabolite synthesis with reduced methanogenesis was further supported by two in vitro measurements of microbiome activities, metabolites, and public global microbiome data of low- and high-methane-emitting beef cattle and sheep. Overall, this study highlights the importance of promoting alternative H2 consumption and reductant disposal pathways for synthesizing host-beneficial metabolites and reducing methane production in ruminants.
Asunto(s)
Euryarchaeota , Sustancias Reductoras , Bovinos , Ovinos , Animales , Sustancias Reductoras/metabolismo , Metano/metabolismo , Hidrógeno/metabolismo , Rumiantes/metabolismo , Fermentación , Euryarchaeota/metabolismo , Rumen/metabolismoRESUMEN
BACKGROUND: Better utilization of rape straw can provide alternative strategies for sustainable ruminant and food production. The research reported here investigated changes in the carbohydrate composition of rape straw as a result of mixed ensiling with whole-crop corn or inoculated with nitrate, and the consequent effects on ruminal fermentation through in vitro batch culture. The three treatments included: rape straw and corn silage (RSTC), and ensiling treatment of rape straw with whole-crop corn (RSIC) or with calcium nitrate inoculation (RSICN). RESULTS: Ensiling treatment of rape straw and whole-crop corn or plus nitrate enriched lactic acid bacteria and lactate. The treatments broke the fiber surface connections of rape straw, leading to higher neutral detergent soluble (NDS) content and lower fiber content. Ensiling treatments led to greater (P < 0.05) dry matter degradation (DMD), molar proportions of propionate and butyrate, relative abundance of the phylum Bacteroidetes and genus Prevotella, and lower (P < 0.05) methane production in terms of g kg-1 DMD, molar proportions of acetate, and lower acetate to propionate ratio than the RSTC treatment. The RSICN treatment led to the lowest (P < 0.05) hydrogen concentration and methane production among the three treatments. CONCLUSION: Ensiling treatments of rape straw and whole-crop corn destroy the micro-structure of rape straw, promote substrate degradation by enriching the phylum Bacteroidetes and the genus Prevotella, and decrease methane production by favoring propionate and butyrate production. Nitrate inoculation in the ensiling treatment of rape straw and whole-crop corn further decreases methane production without influencing substrate degradation by providing an additional hydrogen sink. © 2023 Society of Chemical Industry.