Influence of the Composition of the Cellulolytic Flora on the Development of Hydrogenotrophic Microorganisms, Hydrogen Utilization, and Methane Production in the Rumens of Gnotobiotically Reared Lambs

Abstract

We investigated the influence of the composition of the fibrolytic microbial community on the development and activities of hydrogen-utilizing microorganisms in the rumens of gnotobiotically reared lambs. Two groups of lambs were reared. The first group was inoculated with Fibrobacter succinogenes, a non-H 2 -producing species, as the main cellulolytic organism, and the second group was inoculated with Ruminococcus albus, Ruminococcus flavefaciens, and anaerobic fungi that produce hydrogen. The development of hydrogenotrophic bacterial communities, i.e., acetogens, fumarate and sulfate reducers, was monitored in the absence of methanogens and after inoculation of methanogens. Hydrogen production and utilization and methane production were measured in rumen content samples incubated in vitro in the presence of exogenous hydrogen (supplemented with fumarate or not supplemented with fumarate) or in the presence of ground alfalfa hay as a degradable substrate. Our results show that methane production was clearly reduced when the dominant fibrolytic species was a non-H 2 -producing species, such as Fibrobacter succinogenes, without significantly impairing fiber degradation and fermentations in the rumen. The addition of fumarate to the rumen contents stimulated H 2 utilization only by the ruminal microbiota inoculated with F. succinogenes, suggesting that these communities could play an important role in fumarate reduction in vivo.Hydrogen is a major intermediary metabolite in anaerobic degradation of organic matter. In ruminants, hydrogen is produced by hydrolytic and fermentative microorganisms and is mainly used by methanogenic Archaea to reduce carbon dioxide into methane. These microorganisms represent the main ruminal microbial community implicated in this pathway (33). Hydrogen transfer through methanogenesis is beneficial to the degradation of plant cell wall carbohydrates in the rumen (19,43,46). However, as a result of this process, methane is eructated by ruminants (400 to 500 liters per day per adult animal) and represents a loss of carbon and energy, accounting for 8 to 12% of the gross energy content of the diet (27, 37, 44). The amount of methane produced varies according to the diet (forage or concentrate) and the production system (intensive or extensive) (27,40). The contribution of livestock agriculture to greenhouse gas (GHG) emissions has been estimated to range between 9% and 18% of anthropogenic emissions, with methane representing between 30% and 50% of the total GHG emitted from the livestock sector (34). In that context, various strategies have been suggested in order to mitigate ruminant methane production (27,28,34). Reducing hydrogen production should be achieved without impairing efficacy of feed digestion and fermentation. Inhibition of activity and/or number of methanogens should be done in association with a stimulation of hydrogen-consuming pathways in order to avoid the negative effect of an increased partial pressure of this gas (28).The aim of the present work was to investigate t...

Effect of dietary starch concentration and fish oil supplementation on milk yield and composition, diet digestibility, and methane emissions in lactating dairy cows

“…Based on these results, we could hypothesize that, in the present study, FO might have enhanced the growth of some rumen cellulolytic bacteria that do not produce hydrogen from their fermentations, such as Fibrobacter succinogenes. The results of Chaucheyras-Durand et al (2010) support, at least partly, this hypothesis: those authors noted that, in reared lambs, CH 4 yield was reduced (this was not the case in the present study) when the dominant fibrolytic species was Fibrobacter succinogenes (a non-H 2 -producing species). However, in the study of Chaucheyras-Durand et al (2010), fiber degradation was not impaired by the treatment (non-H 2 -vs. H 2producing rumen bacteria), whereas FO increased NDF digestibility in the present study.…”

Effect of dietary fiber on the methanogen community in the hindgut of Lantang gilts

“…It has been reported that hydrogen transfer through methanogenesis is beneficial to the degradation of plant cell wall carbohydrates in the rumen (Chaucheyras-Durand et al, 2010) and the microbiota in the large intestine of pigs contains all of the predominant ruminal cellulose degrading bacteria, including F. succinogenes (intestinalis), Ruminococcus albus and Rumnococcus flavefaciens (Varel and Yen, 1997). Accordingly, we also quantified some of the abovementioned bacteria and anaerobic fungi in the large intestinal contents, but only F. succinogenes and anaerobic fungi were successfully amplified.…”

“…It has been reported that, in the rumen, among the major cellulolytic communities, anaerobic fungi are the major contributors of H 2 , whereas F. succinogenes does not produce H 2 (Chaucheyras-Durand et al, 2010). Miller (1991) reported that feed ingredients rich in crude fiber stimulate some microbial species within the cellulolytic-methanogen consortium, which serve to couple the degradation of carbohydrates with the use of H 2 for the reduction of CO 2 to methane.…”

Use of Yeast Probiotics in Ruminants: Effects and Mechanisms of Action on Rumen pH, Fibre Degradation, and Microbiota According to the Diet

“…This hydrogen transfer is important for a good functioning of the rumen ecosystem, but at the same time methane formation represents a loss of energy (10-12% of the metabolizable energy of the host animal) and this gas being a potent greenhouse gas, it should be decreased [157]. Studies with gnotobiotically-reared lambs have shown that animals inoculated with F. succinogenes were less prone to produce methane than lambs inoculated with Ruminococci and fungi, without significant modifications of rumen fibre degradability and volatile fatty acid concentrations [158]. The use of microbial solutions to promote F. succinogenes would then appear interesting to be able to mitigate methane emissions by cattle.…”