Evaluation of Nanaerobic Digestion as a Mechanism to Explain Surplus Methane Production in Animal Rumina and Engineered Digesters

Nanaerobes are a
newly described class of microorganisms that use
a unique cytochrome bd oxidase to achieve nanaerobic
respiration at <2 μM dissolved oxygen (∼1% of atmospheric
oxygen) but are not viable above this value due to the lack of other
terminal oxidases. Although sharing an overlapping ecological niche
with methanogenic archaea, the role of nanaerobes in methanogenic
systems has not been studied so far. To explore their occurrence and
significance, we re-analyzed published meta-omic datasets from animal
rumina and waste-to-energy digesters, including conventional anaerobic
digesters and anaerobic digesters with ultra-low oxygenation. Results
show that animal rumina share broad similarities in the microbial
community and system performance with oxygenated digesters, rather
than with conventional anaerobic digesters, implying that trace levels
of oxygen drive the efficient digestion in ruminants. The rumen system
serves as an ideal model for the newly named nanaerobic digestion,
as it relies on the synergistic co-occurrence of nanaerobes and methanogens
for methane yield enhancement. The most abundant ruminal bacterial
family Prevotellaceae contains many nanaerobes, which
perform not only anaerobic fermentation but also nanaerobic respiration
using cytochrome bd oxidase. These nanaerobes generally
accompany hydrogenotrophic methanogens to constitute a thermodynamically
and physiologically consistent framework for efficient methane generation.
Our findings provide new insights into ruminal methane emissions and
strategies to enhance methane generation from biomass.