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Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill

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Abstract

The Deepwater Horizon (DWH) oil spill in the spring of 2010 resulted in an input of similar to 4.1 million barrels of oil to the Gulf of Mexico; >22% of this oil is unaccounted for, with unknown environmental consequences. Here we investigated the impact of oil deposition on microbial communities in surface sediments collected at 64 sites by targeted sequencing of 16S rRNA genes, shotgun metagenomic sequencing of 14 of these samples and mineralization experiments using C-14-labeled model substrates. The 16S rRNA gene data indicated that the most heavily oil-impacted sediments were enriched in an uncultured Gammaproteobacterium and a Colwellia species, both of which were highly similar to sequences in the DWH deep-sea hydrocarbon plume. The primary drivers in structuring the microbial community were nitrogen and hydrocarbons. Annotation of unassembled metagenomic data revealed the most abundant hydrocarbon degradation pathway encoded genes involved in degrading aliphatic and simple aromatics via butane monooxygenase. The activity of key hydrocarbon degradation pathways by sediment microbes was confirmed by determining the mineralization of C-14-labeled model substrates in the following order: propylene glycol, dodecane, toluene and phenanthrene. Further, analysis of metagenomic sequence data revealed an increase in abundance of genes involved in denitrification pathways in samples that exceeded the Environmental Protection Agency (EPA)'s benchmarks for polycyclic aromatic hydrocarbons (PAHs) compared with those that did not. Importantly, these data demonstrate that the indigenous sediment microbiota contributed an important ecosystem service for remediation of oil in the Gulf. However, PAHs were more recalcitrant to degradation, and their persistence could have deleterious impacts on the sediment ecosystem.

Alteromonadaceae Bacterial Proteins Carbon Radioisotopes Ecosystem Gammaproteobacteria Gene Expression Gulf of Mexico Metagenomics Mixed Function Oxygenases Nitrogen Petroleum Pollution Polycyclic Hydrocarbons Aromatic RNA Bacterial RNA Ribosomal 16S Seawater EC 1.- Mixed Function Oxygenases N762921K75 Nitrogen deep-sea hydrocarbon plume deepwater horizon oil spill deleterious impact Environmental Protection Agency metabolic process metagenomics microbial community water column Eubacteria Bacteria Microorganisms (Bacteria Eubacteria Microorganisms) - Facultatively Anaerobic Gram-Negative Rods [06700] Colwellia genus Microorganisms (Bacteria Eubacteria Microorganisms) - Bacteria [05000] Gammaproteobacterium higher_taxa Colwellia 16S rRNA gene [Facultatively Anaerobic Gram-Negative Rods] Gammaproteobacterium 16S rRNA gene [Bacteria] aromatics butane monooxygenase 9059-16-9 EC 1.14.15.3 carbon-14 14762-75-5 dodecane 112-40-3 toxin water pollutant pollutant genes glycol 107-21-1 toxin water pollutant pollutant hydrocarbons nitrogen 7727-37-9 phenanthrene 85-01-8 toxin water pollutant pollutant polycyclic aromatic hydrocarbons PAHs toxin water pollutant pollutant propylene 115-07-1 toxin water pollutant pollutant toluene 108-88-3 toxin water pollutant pollutant 03502 Genetics - General 03509 Genetics - Population genetics 10060 Biochemistry studies - General 10062 Biochemistry studies - Nucleic acids purines and pyrimidines 22501 Toxicology - General and methods 22506 Toxicology - Environment and industry 31000 Physiology and biochemistry of bacteria 31500 Genetics of bacteria and viruses 37015 Public health - Air water and soil pollution Biochemistry and Molecular Biophysics Population Studies ecosystem remediation applied and field techniques sequencing laboratory techniques genetic techniques Molecular Genetics Pollution Assessment Control and Management Population Genetics Toxicology ECOLOGY MICROBIOLOGY GULF-OF-MEXICO DEGRADING BACTERIA SEQUENCES DIVERSITY TAXONOMY METHANE GROWTH DWH oil spill iTag/Metagenomics microbial community structure sediments METAGENOMICS