Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill

Olivia U. Mason, Nicole M. Scott, Antonio Gonzalez, Adam Robbins-Pianka, Jacob Bælum, Jeffrey Kimbrel, Nicholas J. Bouskill, Emmanuel Prestat, Sharon Borglin, Dominique C. Joyner, Julian L. Fortney, Diogo Jurelevicius, William T. Stringfellow, Lisa Alvarez-Cohen, Terry C. Hazen, Rob Knight, Jack A. Gilbert, Janet K. Jansson

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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.
    Original languageEnglish
    JournalI S M E Journal
    Volume8
    Issue number7
    Pages (from-to)1464-1475
    Number of pages12
    ISSN1751-7362
    DOIs
    Publication statusPublished - 2014

    Bibliographical note

    This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/.

    Keywords

    • 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

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