Abstract

The Deepwater Horizon oil spill triggered a complex cascade of microbial responses that reshaped the dynamics of heterotrophic carbon degradation and the turnover of dissolved organic carbon (DOC) in oil contaminated waters. Our results from 21-day laboratory incubations in rotating glass bottles (roller bottles) demonstrate that microbial dynamics and carbon flux in oil-contaminated surface water sampled near the spill site two weeks after the onset of the blowout were greatly affected by activities of microbes associated with macroscopic oil aggregates. Roller bottles with oil-amended water showed rapid formation of oil aggregates that were similar in size and appearance compared to oil aggregates observed in surface waters near the spill site. Oil aggregates that formed in roller bottles were densely colonized by heterotrophic bacteria, exhibiting high rates of enzymatic activity (lipase hydrolysis) indicative of oil degradation. Ambient waters surrounding aggregates also showed enhanced microbial activities not directly associated with primary oil-degradation (β-glucosidase; peptidase), as well as a twofold increase in DOC. Concurrent changes in fluorescence properties of colored dissolved organic matter (CDOM) suggest an increase in oil-derived, aromatic hydrocarbons in the DOC pool. Thus our data indicate that oil aggregates mediate, by two distinct mechanisms, the transfer of hydrocarbons to the deep sea: a microbially-derived flux of oil-derived DOC from sinking oil aggregates into the ambient water column, and rapid sedimentation of the oil aggregates themselves, serving as vehicles for oily particulate matter as well as oil aggregate-associated microbial communities.

Highlights

  • The explosion of the Deepwater Horizon drilling rig in the northern Gulf of Mexico on April 20, 2010, resulted in the largest accident in the history of the U.S petroleum industry [1]

  • We used rotating bottles to simulate the effects of contamination of surface seawater with an oil slick from the Deepwater Horizon spill site

  • Observation of oil aggregate formation and dynamics over a 21 day time course, coupled with measurements of a suite of potential extracellular enzyme activities, demonstrated that oil contamination led to increased microbial activities compared with uncontaminated surface seawater from the spill site

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Summary

Introduction

The explosion of the Deepwater Horizon drilling rig in the northern Gulf of Mexico on April 20, 2010, resulted in the largest accident in the history of the U.S petroleum industry [1]. Plumes enriched in water-soluble components of the spilled petroleum hydrocarbons developed in water depths greater than 1000 m within two weeks after the onset of the spill [3,4] These deep water plumes were found to contain high microbial biomass dominated by heterotrophic bacteria capable of degrading petroleum hydrocarbons [5,6,7,8,9,10]. We investigate bacterial numbers and activities of extracellular enzymes indicative for oil-degrading bacteria in surface seawaters collected near the Deepwater Horizon oil spill site in which oil aggregates were formed. Rates and activities of microbial extracellular enzymes are a good measure for the initial step of carbon cycling in natural microbial communities [18], and are used here as indicators of heterotrophic microbial activities in oil-contaminated seawater

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