Microbial ecology and biodegradation potential of a sulfolane-contaminated, subarctic aquifer

Abstract

Contaminant biodegradation is one of many ecosystem services aquifer microbiota can provide to humans. Sulfolane is a water-soluble emerging contaminant that is associated with one of the largest contaminated groundwater plumes in the state of Alaska. Despite being widely used, the biodegradation pathways and environmental fate of sulfolane are poorly understood. In this study, we investigated the biodegradation of sulfolane by the microbial community indigenous to this contaminated subarctic aquifer in order to better understand the mechanisms and rates of loss, as well as the environmental factors controlling them. First, we conducted aerobic and anaerobic microcosm studies to assess the biodegradation potential of contaminated subarctic aquifer substrate and concluded that the aquifer microbial community can readily metabolize sulfolane, but only in the presence of oxygen, which is at low concentration in situ. We also investigated the impacts of nutrient limitations and hydrocarbon co-contamination on sulfolane biodegradation rates. To identify exactly which community members were actively degrading sulfolane, we combined DNA-based stable isotope probing (SIP) with genome-resolved metagenomics methods. We found a Rhodoferax sp. to be the primary sulfolane degrading microorganism in this system and obtained a near-complete genomic sequence of this organism, which allowed us to propose a new metabolic model for sulfolane biodegradation. Finally, we assessed the distribution of sulfolane-degrading bacteria throughout the contaminated subarctic aquifer by sequencing 16S rRNA genes from 100 groundwater samples and two sulfolane treatment systems and screening for the sulfolane degrader previously identified using SIP. This assessment revealed that sulfolane biodegradation potential is widespread throughout the aquifer but is not likely occurring under normal conditions. However, the sulfolane-metabolizing Rhodoferax sp. was the most dominant microbe in an effective experimental air-sparge system, suggesting that injecting air into the aquifer can stimulate sulfolane biodegradation in situ. These studies are the first to investigate sulfolane biodegradation potential in a subarctic aquifer. Through this work, we learn there are several important factors limiting biodegradation rates, we expand the known taxonomic distribution of sulfolane biodegradation, and we shed insights into the mechanisms underlying an effective in situ sulfolane remediation system.