Abstract

Abstract Microorganisms are central and cross-cutting to oil spill response strategies. Biodegradation mediated by indigenous microbial communities is the ultimate fate of the majority of petroleum (oil and gas) that enters the marine environment. Key ecosystem services provided by microbes, such as organic matter and nutrient cycling, may be adversely affected by oil contamination. The Deepwater Horizon (DWH) oil spill was the first large scale environmental disaster to which the methods of genomics were applied to determine microbial response to a major perturbation. Here we present a case study on coastal ecosystems to highlight the knowledge gained by application of genomics tools to interrogate mechanisms of petroleum hydrocarbon degradation and to elucidate impacts of oil exposure on ecosystem health and functioning. At Pensacola Beach, results showed that oiling led to a large increase in the growth of indigenous microbes in the form of a series of bacterial blooms. Oil contamination strongly selected for microbial groups capable of hydrocarbon degradation. Oil was degraded and benthic microbial communities returned to near baseline levels approximately one year after oil came ashore. These results indicate that when small particles (< 1 cm) of weathered light oil are buried in the coastal zone, biodegradation by indigenous microbial communities is sufficient for the rapid mitigation of oil contamination after a major spill, whereas larger sand-oil-aggregates take longer to completely degrade because of their unfavorable surface to volume ratio. “Operation Deep Clean” removed these aggregates and enhanced biodegradation insofar as many larger oil aggregates were broken down into smaller ones thereby increasing the surface area available for microbial attack. For environmental managers, these results suggest that biodegradation in beach sands is relatively rapid because oxygen can easily penetrate to the buried oil, and resources may be better placed elsewhere in environments where degradation is limited by oxygen availability or microbial access to hydrocarbons. While specialist microbial groups such as nitrifiers show promise as bioindicators of oil contamination in coastal ecosystems, more work is needed to further validate these biomarkers. Despite substantial progress, a predictive understanding of the fate and impacts of oil spills remains hampered by challenges in interpreting the in situ activity and ecosystem response of benthic microbial populations. To advance this understanding, a dedicated funding mechanism is needed to support fundamental research. A polyphasic approach is encouraged that employs metagenomics in the field along with cultivation and microcosm or mesocosm experiments in the laboratory. Further, research during future disasters would be greatly facilitated by improved coordination between the emergency responders directing mitigation efforts and scientists investigating the success of those efforts.

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