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.

Novel hydrocarbon-degradation pathways in uncultured bacteria in industrial-impacted ocean waters

“…Dokdonia species have been previously described in hydrocarbon-contaminated areas [60], but this is the rst time members of this genus capable of degrading hydrocarbons have been identi ed and had their genetic oil-degradation mechanisms described. Likewise, Lentibacter is a predominant lineage in the FSC water column [20,[51][52][53] and has been shown to become enriched in the presence of crude oil [54,55]. Here we found they were predominant at the 5 m SIP enrichments, comprising 8% of the metagenome, and we found evidence of their direct involvement in oil degradation.…”

“…2). Interestingly, the most dominant MAG in the SIP enrichment from 700 m -Oleibacterhas not been previously reported in FSC waters [20], suggesting that is likely present at low abundance in the baseline communities. Lentibacter is a predominant genus in the baseline FSC water column [20,[51][52][53] and becomes enriched in the presence of crude oil [54,55], however, alkane degradation pathways have not been previously con rmed.…”

“…The alkane-degrading microbial communities from our enrichments varied by depth. Based on 16S rRNA data and MAG abundances, Alcanivorax dominated the shallow waters, while Oleibacter was the most abundant at 700 m. Similarly, a recent study analyzing the microbial communities in the FSC over a period of two years showed Alcanivorax were signi cantly increased in abundance in the upper water column (< 175 m), and this was more prominent during the spring compared to the fall (from undetectable to 0.1% relative abundance) [20]. The microbial community reconstructed from 5 m is more diverse than the deeper community.…”

“…Previous hexadecane SIP enrichment experiments from the Deepwater Horizon Spill recovered MAGs a liated to Marinobacter, a generalist hydrocarbon-degrader [19]. Marinobacter has been found throughout the water column of the FSC, with up to 0.2% relative abundance [20,62]. We recovered 4 MAGs from these genera evenly distributed among depths but more abundant at 700 m. However, in this study, Alcanivorax and Oleibacter were the most abundant lineages, suggesting that the distribution of the hydrocarbon-degrading bacteria is not homogeneous in the oceans.…”

“…Here, we investigate the active hydrocarbon-degrading bacteria from the Faroe-Shetland Channel (FSC), an area of the northeast Atlantic Ocean that has over a 20-year history of oil exploration and production. Recently, new potential hydrocarbon-degrading bacteria were described in these waters [20]. To understand the metabolic mechanisms of baseline FSC communities, we used SIP-metagenomics.…”