The polycyclic aromatic hydrocarbon degradation potential of Gulf of Mexico native coastal microbial communities after the Deepwater Horizon oil spill.

Anthony D. Kappell,Joy D. Van Nostrand,Jizhong Zhou,Sandra L. McLellan,Ryan J. Newton,Krassimira R. Hristova,Yin Wei

doi:10.3389/fmicb.2014.00205

Abstract

The Deepwater Horizon (DWH) blowout resulted in oil transport, including polycyclic aromatic hydrocarbons (PAHs) to the Gulf of Mexico shoreline. The microbial communities of these shorelines are thought to be responsible for the intrinsic degradation of PAHs. To investigate the Gulf Coast beach microbial community response to hydrocarbon exposure, we examined the functional gene diversity, bacterial community composition, and PAH degradation capacity of a heavily oiled and non-oiled beach following the oil exposure. With a non-expression functional gene microarray targeting 539 gene families, we detected 28,748 coding sequences. Of these sequences, 10% were uniquely associated with the severely oil-contaminated beach and 6.0% with the non-oiled beach. There was little variation in the functional genes detected between the two beaches; however the relative abundance of functional genes involved in oil degradation pathways, including polycyclic aromatic hydrocarbons (PAHs), were greater in the oiled beach. The microbial PAH degradation potentials of both beaches, were tested in mesocosms. Mesocosms were constructed in glass columns using sands with native microbial communities, circulated with artificial sea water and challenged with a mixture of PAHs. The low-molecular weight PAHs, fluorene and naphthalene, showed rapid depletion in all mesocosms while the high-molecular weight benzo[α]pyrene was not degraded by either microbial community. Both the heavily oiled and the non-impacted coastal communities showed little variation in their biodegradation ability for low molecular weight PAHs. Massively-parallel sequencing of 16S rRNA genes from mesocosm DNA showed that known PAH degraders and genera frequently associated with oil hydrocarbon degradation represented a major portion of the bacterial community. The observed similar response by microbial communities from beaches with a different recent history of oil exposure suggests that Gulf Coast beach communities are primed for PAH degradation.

Highlights

The destruction of the Deepwater Horizon (DWH) oil rig resulted in the discharge of approximately 4.9 million barrels of light crude oil into Gulf of Mexico marine environments from April 20, 2010 to July 15, 2010, making it the second worst oil spill in US history (Lehr et al, 2010)
While the Orange beach microbial community had a greater relative abundance of genes involved in hydrocarbon and polycyclic aromatic hydrocarbons (PAHs) degradation, these genes were present at the non-impacted beach. These results suggest that the native communities found at these beaches have an innate potential for degradation of hydrocarbons and PAHs released during an oil spill
Our findings suggest that oil contamination lead to enrichment of bacteria harboring functional genes involved in hydrocarbon degradation and related stress responses within the impacted sand microbial community

Summary

Introduction

The destruction of the Deepwater Horizon (DWH) oil rig resulted in the discharge of approximately 4.9 million barrels of light crude oil into Gulf of Mexico marine environments from April 20, 2010 to July 15, 2010, making it the second worst oil spill in US history (Lehr et al, 2010). Crude oil along with added dispersants formed more than a 35 km long plume in the Gulf of Mexico that significantly impacted coastal ecosystems, including native microbial community composition (Camilli et al, 2010) with unknown ecological consequences. The low molecular weight PAH, naphthalene was the dominant PAH in the crude oil followed by the low molecular weight PAHs, phenanthrene and fluorene, while the high-molecular weight PAH, chrysene and other PAHs were minor components (Zhanfei et al, 2012). PAHs, high molecular weight compounds, are one of the major contaminant classes of concern in oil spills because many are toxic and/or carcinogenic to humans and wildlife and are often recalcitrant to degradation in environmental media

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