Flexible catabolism of monoaromatic hydrocarbons by anaerobic microbiota adapting to oxygen exposure

Abstract

Microbe-mediated anaerobic degradation is a practical method for remediation of the hazardous monoaromatic hydrocarbons (BTEX, including benzene, toluene, ethylbenzene and xylenes) under electron-deficient contaminated sites. However, how do the anaerobic functional microbes adapt to oxygen exposure and flexibly catabolize BTEX remain poorly understood. We investigated the switches of substrate spectrum and bacterial community upon oxygen perturbation in a nitrate-amended anaerobic toluene-degrading microbiota which was dominated by Aromatoleum species. DNA-stable isotope probing demonstrated that Aromatoleum species was involved in anaerobic mineralization of toluene. Metagenome-assembled genome of Aromatoleum species harbored both the nirBD-type genes for nitrate reduction to ammonium coupled with toluene oxidation and the additional meta-cleavage pathway for aerobic benzene catabolism. Once the anaerobic microbiota was fully exposed to oxygen and benzene, 1.05 ± 0.06% of Diaphorobacter species rapidly replaced Aromatoleum species and flourished to 96.72 ± 0.01%. Diaphorobacter sp. ZM was isolated, which was not only able to utilize benzene as the sole carbon source for aerobic growth and but also innovatively reduce nitrate to ammonium with citrate/lactate/glucose as the carbon source under anaerobic conditions. This study expands our understanding of the adaptive mechanism of microbiota for environmental redox disturbance and provides theoretical guidance for the bioremediation of BTEX-contaminated sites.