Biodegradation of Volatile Hydrocarbons in Estuarine Environments

Benzene, toluene, isoprene, ethane and propane are volatile organic compounds (VOCs) commonly found in estuarine environments. Benzene and toluene are toxic and carcinogenic at varying concentrations. Isoprene, ethane and propane are emitted from marine environments to the atmosphere where they can alter atmospheric chemistry and thus climate in different ways. The identity of microbial communities associated with VOC degradation in estuarine environments is not completely elucidated. Aerobic and anaerobic degradation of these VOCs in the Colne estuary, UK, was investigated using both cultivation-dependent and independent approaches, to understand the effect of VOC-type, concentration and estuarine location on degradation and microbial community composition. Aerobic biodegradation of all VOCs occurred in sediment slurries. More than 80% of the benzene, toluene and isoprene added was degraded within 10 days, while there was more than 40% degradation of ethane and propane within 37 days. Degradation of VOCs correlated positively with the concentration added. Principal component analysis (PCA) of MiSeq-generated 16S rRNA gene sequence data revealed that bacterial communities enriched with ethane, propane or toluene were similar, while those with benzene and isoprene were distinct. The main aerobic genera enriched were: Pseudomonas (benzene), Rhodococcus (isoprene), Amphritea (propane and toluene). In ethane enrichments, Azoarcus and Cycloclasticus dominated at the head and middle of the estuary, respectively. Metabolically versatile Mycobacterium hodleri strain B and Rhodococcus wratislaviensis strain I with putative propane monooxygenase genes were isolated from sediment slurries. Anaerobic degradation of benzene, toluene and propane was observed in sediment slurries but there was no evidence of ethane degradation. Compared with aerobic, anaerobic biodegradation of isoprene was much more equivocal. The bacterial genus primarily enriched with benzene was Pelobacter (95% 16S rRNA identity) along with the archaeal genus Methanomassiliicoccus (83-86% identity) and other novel Euryarchaeota. The main bacterial OTUs enriched on propane had ~90% 16S rRNA identity to Smithella, Rugosimonospora and Desulfatiglans. This study has provided an insight into the bacterial and archaeal populations associated with aerobic and anaerobic degradation of VOCs. It shows that different types of VOCs are consumed by specific taxa, which working together as a community, contribute to carbon cycling in estuarine environments.