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Applied and Environmental Microbiology, October 2007, p. 6391-6403, Vol. 73, No. 20
0099-2240/07/$08.00+0     doi:10.1128/AEM.00181-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Establishment and Development of Ruminal Hydrogenotrophs in Methanogen-Free Lambs

Unité de Microbiologie, INRA, Centre de Clermont-Ferrand-Theix, 63177 Aubière Cedex, France,¹ Grasslands Research Centre, AgResearch, Private Bag 11008, Palmerston North 4442, New Zealand²

Received 24 January 2007/ Accepted 24 July 2007

The aim of this work was to determine whether reductive acetogenesis can provide an alternative to methanogenesis in the rumen. Gnotobiotic lambs were inoculated with a functional rumen microbiota lacking methanogens and reared to maturity on a fibrous diet. Lambs with a methanogen-free rumen grew well, and the feed intake and ruminal volatile fatty acid concentrations for lambs lacking ruminal methanogens were lower but not markedly dissimilar from those for conventional lambs reared on the same diet. A high population density (10⁷ to 10⁸ cells g^–1) of ruminal acetogens slowly developed in methanogen-free lambs. Sulfate- and fumarate-reducing bacteria were present, but their population densities were highly variable. In methanogen-free lambs, the hydrogen capture from fermentation was low (28 to 46%) in comparison with that in lambs containing ruminal methanogens (>90%). Reductive acetogenesis was not a significant part of ruminal fermentation in conventional lambs but contributed 21 to 25% to the fermentation in methanogen-free meroxenic animals. Ruminal H₂ utilization was lower in lambs lacking ruminal methanogens, but when a methanogen-free lamb was inoculated with a methanogen, the ruminal H₂ utilization was similar to that in conventional lambs. H₂ utilization in lambs containing a normal ruminal microflora was age dependent and increased with the animal age. The animal age effect was less marked in lambs lacking ruminal methanogens. Addition of fumarate to rumen contents from methanogen-free lambs increased H₂ utilization. These findings provide the first evidence from animal studies that reductive acetogens can sustain a functional rumen and replace methanogens as a sink for H₂ in the rumen.

Published ahead of print on 3 August 2007.