Transient Oxygen Exposure Causes Profound and Lasting Changes to a Benzene-Degrading Methanogenic Community

We investigated the
impact of oxygen on a strictly anaerobic,
methanogenic
benzene-degrading enrichment culture derived decades ago from oil-contaminated
sediment. The culture includes a benzene fermenter from Deltaproteobacteria candidate clade Sva0485 (referred to as ORM2) and methanogenic archaea.
A one-time injection of 0.1 mL air , simulating a small leak into
30 mL batch culture bottle, had no measurable impact on benzene degradation
rates, although retrospectively, a tiny enrichment of aerobic taxa
was detected. A subsequent 100 times larger injection of air stalled
methanogenesis and caused drastic perturbation of the microbial community.
A benzene-degrading Pseudomonas became highly enriched
and consumed all available oxygen. Anaerobic benzene-degrading ORM2
cell numbers plummeted during this time; re-growth and associated
recovery of methanogenic benzene degradation took almost 1 year. These
results highlight the oxygen sensitivity of this methanogenic culture
and confirm that the mechanism for anaerobic biotransformation of
benzene is independent of oxygen, fundamentally different from established
aerobic pathways, and is carried out by distinct microbial communities.
The study also highlights the importance of including microbial decay
in characterizing and modeling mixed microbial communities.