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

Abstract

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 relatively small one-time injection of air, simulating a small leak into a 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 benzene and all available oxygen. Anaerobic benzene-degrading ORM2 cell numbers plummeted during this time; re-growth and associated recovery of methanogenic benzene degradation took almost one 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 further highlights the importance of including microbial decay in characterizing and modelling and mixed microbial communities. SYNOPSISMethanogenic benzene degradation in a highly enriched anaerobic consortium was inhibited for a year after transient exposure to oxygen, causing mass decay of benzene-fermenting bacteria. GRAPHIC FOR ABSTRACT ART O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY