Final Report Summary - POLLOX (ANAEROBIC POLLUTANT DEGRADATION WITH OXYGEN)
Two central paradigms are currently understood to control biodegradation of hydrocarbons in groundwater and sediments: (i) Redox gradients and interphases between compartments are ‘hot-spots’ of for contaminant breakdown, and (ii) biodegradation is primarily limited by local electron acceptor availability, in particular that of oxygen. The POLLOX project has embarked on the goal of elucidating a postulated role of novel oxygen-dependent physiologies in what is classically considered as oxygen-independent anaerobic hydrocarbon degradation in aquifer sediments and other contaminated freshwater systems. It focussed on two distinct ecophysiological adaptations of degraders: that of long-distance electron transfer by so-called cable bacteria, capable of conducting electrons from pollutants to oxygen as electron acceptor across redox gradients, and that of an intrinsic oxygenesis by NO-dismutation in non-canonical denitrification of so-called oxygenic hydrocarbon degraders. In an interdisciplinary research endeavour, the POLLOX team has demonstrated that cable bacteria within the Desulfobulbaceae, capable of long-distance electron transfer across redox gradients can actually be found in contaminated aquifers, lake sediments and other anthropogenically impacted freshwater systems. Although a direct involvement of these electrogenic bacteria in pollutant catabolism could not be substantiated, indirect effect of long-distance electron transfer in the stimulation of pollutant breakdown were observed. Moreover, by targeting putative NO-dismutase genes, a wide diversity and surprising abundance of putative oxygenic denitrifiers in anoxic groundwater systems was observed. By targeted 13C-labelling, a previously hypothesized oxygen-activating, nitrate-respiring degradation strategy was revealed, explaining how complex degrader microbiota can increase catabolic efficiencies under limited electron acceptor supply. This was mediated by a novel combination of RNA-stable isotope probing (SIP) and total transcriptome sequencing, allowing for a targeted access to process-relevant gene expression in environmental pollutant-degrading microbiomes. In summary, the POLLOX has opened several intriguing new doors towards a better understanding of the adaptations and ecophysiology of complex pollutant-degrading microbiomes in groundwater, and how microbes can circumvent physical habitat constraints by limited mixing in porous media. Understanding the controls of these emergent microbial capacities may open new routes for modulated pollutant removal in natural and engineered water systems.