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Title: Metabolic and spatio-taxonomic response of uncultivated seafloor bacteria following the Deepwater Horizon oil spill

Journal Article · · The ISME Journal

The release of 700 million liters of oil into the Gulf of Mexico over a few months in 2010 produced dramatic changes in the microbial ecology of the water and sediment. Here, we reconstructed the genomes of 57 widespread uncultivated bacteria from post-spill deep-sea sediments, and recovered their gene expression pattern across the seafloor. These genomes comprised a common collection of bacteria that were enriched in heavily affected sediments around the wellhead. Although rare in distal sediments, some members were still detectable at sites up to 60 km away. Many of these genomes exhibited phylogenetic clustering indicative of common trait selection by the environment, and within half we identified 264 genes associated with hydrocarbon degradation. Alkane degradation ability was near ubiquitous among candidate hydrocarbon degraders, whereas just three harbored elaborate gene inventories for the degradation of alkanes and aromatic and polycyclic aromatic hydrocarbons (PAHs). Differential gene expression profiles revealed a spill-promoted microbial sulfur cycle alongside gene upregulation associated with PAH degradation. Gene expression associated with alkane degradation was widespread, although active alkane degrader identities changed along the pollution gradient. Analyses suggest that a broad metabolic capacity to respond to oil inputs exists across a large array of usually rare indigenous deep-sea bacteria.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
USDOE
DOE Contract Number:
AC05-76RL01830
OSTI ID:
1406694
Report Number(s):
PNNL-SA-125408
Journal Information:
The ISME Journal, Vol. 11, Issue 11; ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English

References (81)

A Tale of Two Spills: Novel Science and Policy Implications of an Emerging New Oil Spill Model journal May 2012
Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill journal June 2012
Sustained deposition of contaminants from the Deepwater Horizon spill journal May 2016
The soluble methane mono-oxygenase of Methylococcus capsulatus (Bath). Its ability to oxygenate n-alkanes, n-alkenes, ethers, and alicyclic, aromatic and heterocyclic compounds journal August 1977
Mats of psychrophilic thiotrophic bacteria associated with cold seeps of the Barents Sea journal January 2012
Cutadapt removes adapter sequences from high-throughput sequencing reads journal May 2011
Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2 journal February 2012
Oil Biodegradation and Bioremediation: A Tale of the Two Worst Spills in U.S. History journal August 2011
Oil spill bioremediation: experiences, lessons and results from the Exxon Valdez oil spill in Alaska journal January 1992
IMG/M: the integrated metagenome data management and comparative analysis system journal November 2011
Natural and unnatural oil slicks in the G ulf of M exico journal December 2015
Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization journal August 2012
Substrate specificity of the alkane hydroxylase system of Pseudomonas oleovorans GPo1 journal October 1994
Tracking Hydrocarbon Plume Transport and Biodegradation at Deepwater Horizon journal August 2010
Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill journal January 2014
Metatranscriptomic Analysis of Diminutive Thiomargarita-Like Bacteria (“Candidatus Thiopilula” spp.) from Abyssal Cold Seeps of the Barbados Accretionary Prism journal February 2015
Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses journal July 2013
Trimmomatic: a flexible trimmer for Illumina sequence data journal April 2014
Community-wide analysis of microbial genome sequence signatures journal January 2009
Mapping and quantifying mammalian transcriptomes by RNA-Seq journal May 2008
Characterization of a Naphthalene Dioxygenase Endowed with an Exceptionally Broad Substrate Specificity toward Polycyclic Aromatic Hydrocarbons journal October 2006
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy journal June 2007
EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data journal May 2011
Hydrocarbon-degrading bacteria: the oil-spill clean-up crew journal November 2009
Phylogenetic Clustering and Overdispersion in Bacterial Communities journal July 2006
Oxidation of Ammonia by Methane-oxidizing Bacteria and the Effects of Ammonia on Methane Oxidation journal June 1977
Microbial community successional patterns in beach sands impacted by the Deepwater Horizon oil spill journal February 2015
Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill journal October 2011
Aquifer environment selects for microbial species cohorts in sediment and groundwater journal February 2015
Single-cell Sequencing of Thiomargarita Reveals Genomic Flexibility for Adaptation to Dynamic Redox Conditions journal June 2016
Complete Genome Sequence of the Pyrene-Degrading Bacterium Cycloclasticus sp. Strain P1 journal November 2012
Microbial communities acclimate to recurring changes in soil redox potential status: Fluctuating redox microbial communities journal December 2010
Reconstructing metabolic pathways of hydrocarbon-degrading bacteria from the Deepwater Horizon oil spill journal May 2016
Search and clustering orders of magnitude faster than BLAST journal August 2010
The microbial nitrogen cycling potential is impacted by polyaromatic hydrocarbon pollution of marine sediments journal March 2014
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs journal February 2008
Ecological Impacts of the Deepwater Horizon Oil Spill: Implications for Immunotoxicity journal November 2011
The RAST Server: Rapid Annotations using Subsystems Technology journal January 2008
Porticoccus hydrocarbonoclasticus sp. nov., an Aromatic Hydrocarbon-Degrading Bacterium Identified in Laboratory Cultures of Marine Phytoplankton journal December 2011
CDD: NCBI's conserved domain database journal November 2014
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth journal April 2012
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools journal November 2012
Copper-dependent reciprocal transcriptional regulation of methane monooxygenase genes in Methylococcus capsulatus and Methylosinus trichosporium journal July 1997
Microbial Dynamics Following the Macondo Oil Well Blowout across Gulf of Mexico Environments journal August 2014
Cytochrome P450 Alkane Hydroxylases of the CYP153 Family Are Common in Alkane-Degrading Eubacteria Lacking Integral Membrane Alkane Hydroxylases journal January 2006
Characterization of five genes in the upper-pathway operon of TOL plasmid pWW0 from Pseudomonas putida and identification of the gene products. journal September 1989
Fallout plume of submerged oil from Deepwater Horizon journal October 2014
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
Analysis of Composition and Structure of Coastal to Mesopelagic Bacterioplankton Communities in the Northern Gulf of Mexico journal January 2013
Distribution of hydrocarbons released during the 2010 MC252 oil spill in deep offshore waters journal February 2013
HTSeq--a Python framework to work with high-throughput sequencing data journal September 2014
Accelerated Profile HMM Searches journal October 2011
Denitrification versus respiratory ammonification: environmental controls of two competing dissimilatory NO3−/NO2− reduction pathways in Shewanella loihica strain PV-4 journal October 2014
Assessment of the Deepwater Horizon oil spill impact on Gulf coast microbial communities journal April 2014
Towards a Genome-Based Taxonomy for Prokaryotes journal September 2005
Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes journal May 2013
Purification and Characterization of an Arene cis-Dihydrodiol Dehydrogenase Endowed with Broad Substrate Specificity toward Polycyclic Aromatic Hydrocarbon Dihydrodiols journal July 2006
SmoXYB1C1Z of Mycobacterium sp. Strain NBB4: a Soluble Methane Monooxygenase (sMMO)-Like Enzyme, Active on C 2 to C 4 Alkanes and Alkenes journal July 2014
Stable isotope evidence for alternative bacterial carbon sources in the Gulf of Mexico journal December 1998
Single-cell genomics reveals features of a Colwellia species that was dominant during the Deepwater Horizon oil spill journal July 2014
Metagenomic analysis and metabolite profiling of deep–sea sediments from the Gulf of Mexico following the Deepwater Horizon oil spill journal January 2013
The environmental controls that govern the end product of bacterial nitrate respiration journal August 2014
Fast gapped-read alignment with Bowtie 2 journal March 2012
Transcriptional response of bathypelagic marine bacterioplankton to the Deepwater Horizon oil spill journal August 2013
Succession of Hydrocarbon-Degrading Bacteria in the Aftermath of the Deepwater Horizon Oil Spill in the Gulf of Mexico journal September 2013
Regiospecificity of Two Multicomponent Monooxygenases from Pseudomonas stutzeri OX1: Molecular Basis for Catabolic Adaptation of This Microorganism to Methylated Aromatic Compounds journal August 2005
Why Orange Guaymas Basin Beggiatoa spp. Are Orange: Single-Filament-Genome-Enabled Identification of an Abundant Octaheme Cytochrome with Hydroxylamine Oxidase, Hydrazine Oxidase, and Nitrite Reductase Activities journal December 2012
Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community journal November 2012
Exxon Valdez Vs. Deepwater Horizon: ES&T’s Top Feature Article 2011 journal March 2012
Big Bacteria journal October 2001
Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill: Enrichment of oil degraders from Gulf of Mexico journal May 2012
A Persistent Oxygen Anomaly Reveals the Fate of Spilled Methane in the Deep Gulf of Mexico journal January 2011
The Sequence Alignment/Map format and SAMtools journal June 2009
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0 journal October 2013
Alkane degradation under anoxic conditions by a nitrate-reducing bacterium with possible involvement of the electron acceptor in substrate activation: Alkane degradation with nitrate journal February 2011
Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage journal December 2011
Deep-Sea Oil Plume Enriches Indigenous Oil-Degrading Bacteria journal August 2010
Analysis of the Novel Benzylsuccinate Synthase Reaction for Anaerobic Toluene Activation Based on Structural Studies of the Product journal January 1998
Genome Sequence of the Pyrene- and Fluoranthene-Degrading Bacterium Cycloclasticus sp. Strain PY97M journal June 2013
Isolation of Marine Polycyclic Aromatic Hydrocarbon (PAH)-Degrading Cycloclasticus Strains from the Gulf of Mexico and Comparison of Their PAH Degradation Ability with That of Puget Sound Cycloclasticus Strains journal December 1998
Nitrate ammonification by Nautilia profundicola AmH: experimental evidence consistent with a free hydroxylamine intermediate journal January 2013

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