Hydrogen utilising bacteria from the forestomach of eastern grey (Macropus giganteus) and red (Macropus rufus) kangaroos

Abstract

Reductive acetogenesis is an alternative to methanogenesis for removing hydrogen produced during enteric fermentation. In Australia, kangaroos have evolved an enlarged forestomach analogous to the rumen of sheep and cattle. However, unlike sheep and cattle, kangaroos produce very little methane from enteric fermentation. From samples of gut contents from five eastern grey and three red kangaroos, we were not able to detect methanogens using a PCR protocol, but did detect the formyltetrahydrofolate synthetase (FTHFS) gene (likely to be used for reductive acetogenesis) in all animals. Isolations to recover acetogens resulted in two different classes of hydrogen consuming bacteria being isolated. The first class consisted of acetogens that possessed the FTHFS gene, which except for Clostridium glycolicum, were not closely related to any previously cultured bacteria. The second class were not acetogens but consisted of enterobacteria (Escherichia coli and Shigella) that did not possess FTHFS genes but did utilise hydrogen and produce acetate. Enumeration of the acetogens containing the FTHFS gene by real-time PCR indicated that bacteria of the taxa designated YE257 were common to all the kangaroos whereas YE266/YE273 were only detected in eastern grey kangaroos. When present, both species occurred at densities above ×106 cell equivalents per mL. C. glycolicum was not detected in the kangaroos and, unlike YE257 and YE266/273, is unlikely to play a major role in reductive acetogenesis in the foregut of kangaroos.

Decreasing methane yield with increasing food intake keeps daily methane emissions constant in two foregut fermenting marsupials, the western grey kangaroo and red kangaroo

“…The nevertheless higher-than-expected CH 4 yield in macropods of the present study seemingly contradicts literature findings of extremely low in vivo CH 4 emission (Kempton et al, 1976;Dellow et al, 1988;Madsen and Bertelsen, 2012; also previously contradicted by von Engelhardt et al, 1978), very small populations of foregut Archaea (Evans et al, 2009;Klieve et al, 2012;Ouwerkerk et al, 2009) and the assumed dominance of reductive acetogens as hydrogen sinks in macropods (Godwin et al, 2014). However, as pointed out by Ouwerkerk et al (2005) and Gulino et al (2013), macropods generally seem to harbour rather unique microbe communities with many as yet undescribed species.…”

“…Ciliate protozoa and fungi were also found in similar density levels to those in the rumen (Dellow et al, 1988). Reductive acetogens that reduce hydrogen to acetate were found to be the main hydrogen sink in macropods, supporting the assumed low CH 4 emissions (Gagen et al, 2010;Godwin et al, 2014;Klieve, 2009;Ouwerkerk et al, 2009). Methanogenic archaea were also present, but in much lower density than in the rumen -that is, up to 1000-fold less (Evans et al, 2009;Klieve et al, 2012).…”

Interactions between microbial consortia in biofilms: a paradigm shift in rumen microbial ecology and enteric methane mitigation

“…The usual reason put forward for this is that the reduction of CO 2 to acetate is thermodynamically less favourable than the reduction of HCO 3 -to CH 4 (McAllister and Newbold 2008). In this connection, however, it is interesting to note that CH 4 is not produced in the fermentative areas in the gut of macropods (Kempton et al 1976) where methanogenesis is apparently replaced by reductive acetogenesis (Ouwerkerk et al 2009).…”

Presence of Novel, Potentially Homoacetogenic Bacteria in the Rumen as Determined by Analysis of Formyltetrahydrofolate Synthetase Sequences from Ruminants

“…Several homoacetogens, including Acetitomaculum ruminis (15), Eubacterium limosum (14,17), Blautia schinkii, and Blautia producta (11), have been isolated from ruminants. Homoacetogens have also been isolated from the kangaroo forestomach, whose function is analogous to that of the rumen, which suggests that homoacetogenesis may play a role in hydrogen removal in the low-methane-emission forestomach (37).…”