Inter- and Intra-Annual Bacterioplankton Community Patterns in a Deepwater Sub-Arctic Region: Persistent High Background Abundance of Putative Oil Degraders

Abstract

Hydrocarbon-degrading bacteria naturally degrade and remove petroleum pollutants, yet baselines do not currently exist for these critical microorganisms in many regions where the oil and gas industry is active. Furthermore, understanding how a baseline community changes across the seasons and its potential to respond to an oil spill event are prerequisites for predicting their response to elevated hydrocarbon exposures. In this study, 16S rRNA gene-based profiling was used to assess the spatiotemporal variability of baseline bacterioplankton community composition in the Faroe-Shetland Channel (FSC), a deepwater sub-Arctic region where the oil and gas industry has been active for the last 40 years. Over a period of 2 years, we captured the diversity of the bacterioplankton community within distinct water masses (defined by their temperature and salinity) that have a distinct geographic origin (Atlantic or Nordic), depth, and direction of flow. We demonstrate that bacterioplankton communities were significantly different across water samples of contrasting origin and depth. Taxa of known hydrocarbon-degrading bacteria were observed at higher-than-anticipated abundances in water masses originating in the Nordic Seas, suggesting these organisms are sustained by an unconfirmed source of oil input in that region. In the event of an oil spill, our results suggest that the response of these organisms is severely hindered by the low temperatures and nutrient levels that are typical for the FSC.IMPORTANCE Oil spills at sea are one of the most disastrous anthropogenic pollution events, with the Deepwater Horizon spill providing a testament to how profoundly the health of marine ecosystems and the livelihood of its coastal inhabitants can be severely impacted by spilled oil. The fate of oil in the environment is largely dictated by the presence and activities of natural communities of oil-degrading bacteria. While a significant effort was made to monitor and track the microbial response and degradation of the oil in the water column in the wake of the Deepwater Horizon spill, the lack of baseline data on the microbiology of the Gulf of Mexico confounded scientists' abilities to provide an accurate assessment of how the system responded relative to prespill conditions. This data gap highlights the need for long-term microbial ocean observatories in regions at high risk of oil spills. Here, we provide the first microbiological baseline established for a subarctic region experiencing high oil and gas industry activity, the northeast Atlantic, but with no apparent oil seepage or spillage. We also explore the presence, relative abundances, and seasonal dynamics of indigenous hydrocarbon-degrading communities. These data will advance the development of models to predict the behavior of such organisms in the event of a major oil spill in this region and potentially impact bioremediation strategies by enhancing the activities of these organisms in breaking down the oil.