The Deepwater Horizon blowout in the Gulf of Mexico in 2010, one of the largest marine oil spills1, changed bacterial communities in the water column and sediment as they responded to complex hydrocarbon mixtures2–4. Shifts in community composition have been correlated to the microbial degradation and use of hydrocarbons2,5,6, but the full genetic potential and taxon-specific metabolisms of bacterial hydrocarbon degraders remain unresolved. Here, we have reconstructed draft genomes of marine bacteria enriched from sea surface and deep plume waters of the spill that assimilate alkane and polycyclic aromatic hydrocarbons during stable-isotope probing experiments, and we identify genes of hydrocarbon degradation pathways. Alkane degradation genes were ubiquitous in the assembled genomes. Marinobacter was enriched with n-hexadecane, and uncultured Alpha- and Gammaproteobacteria populations were enriched in the polycyclic-aromatic-hydrocarbon-degrading communities and contained a broad gene set for degrading phenanthrene and naphthalene. The repertoire of polycyclic aromatic hydrocarbon use varied among different bacterial taxa and the combined capabilities of the microbial community exceeded those of its individual components, indicating that the degradation of complex hydrocarbon mixtures requires the non-redundant capabilities of a complex oil-degrading community.
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Crone, T. J. & Tolstoy, M. Magnitude of the 2010 Gulf of Mexico oil leak. Science 330, 634–634 (2010).
Hazen, T. C. et al. Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330, 204–208 (2010).
Redmond, M. C. & Valentine, D. L. Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill. Proc. Natl Acad. Sci. USA 109, 20292–20297 (2012).
Yang, T. et al. Pulsed blooms and persistent oil-degrading bacterial populations in the water column during and after the Deepwater Horizon blowout. Deep Sea Res. II http://dx.doi.org/10.1016/j.dsr2.2014.01.014 (2014).
Crespo-Medina, M. et al. The rise and fall of methanotrophy following a deepwater oil-well blowout. Nature Geosci. 7, 423–427 (2014).
Valentine, D. L. et al. Propane respiration jump-starts microbial response to a deep oil spill. Science 330, 208–211 (2010).
Chauhan, A., Oakeshott, J. G. & Jain, R. K. Bacterial metabolism of polycyclic aromatic hydrocarbons: strategies for bioremediation. Indian J. Microbiol. 48, 95–113 (2008).
Kimes, N. E., Callaghan, A. V., Suflita, J. M. & Morris, P. J. Microbial transformation of the Deepwater Horizon oil spill—past, present, and future perspectives. Front. Microbiol. 5, 603 (2014).
Lea-Smith, D. J. et al. Contribution of cyanobacterial alkane production to the ocean hydrocarbon cycle. Proc. Natl Acad. Sci. USA 112, 13591–13596 (2015).
Mason, O. U. et al. Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill. ISME J. 6, 1715–1727 (2012).
Bælum, J. et al. Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill. Environ. Microbiol. 14, 2405–2416 (2012).
Kleindienst, S. et al. Diverse, rare microbial taxa responded to the Deepwater Horizon deep-sea hydrocarbon plume. ISME J. 10, 400–415 (2015).
Gutierrez, T. et al. Hydrocarbon-degrading bacteria enriched by the Deepwater Horizon oil spill identified by cultivation and DNA-SIP. ISME J. 7, 2091–2104 (2013).
Kodama, Y., Stiknowati, L. I., Ueki, A., Ueki, K. & Watanabe, K. Thalassospira tepidiphila sp. nov., a polycyclic aromatic hydrocarbon-degrading bacterium isolated from seawater. Int. J. Syst. Evol. Microbiol. 58, 711–715 (2008).
Schneiker, S. et al. Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nature Biotechnol. 24, 997–1004 (2006).
Lai, Q. et al. Alcanivorax pacificus sp. nov., isolated from a deep-sea pyrene-degrading consortium. Int. J. Syst. Evol. Microbiol. 61, 1370–1374 (2011).
Wang, B., Lai, Q., Cui, Z., Tan, T. & Shao, Z. A pyrene-degrading consortium from deep-sea sediment of the West Pacific and its key member Cycloclasticus sp. P1. Environ. Microbiol. 10, 1948–1963 (2008).
Kleindienst, S. et al. Chemical dispersants can suppress the activity of natural oil-degrading microorganisms. Proc. Natl Acad. Sci. USA 112, 14900–14905 (2015).
Cozzone, A. J. Role of protein phosphorylation on serine/threonine and tyrosine in the virulence of bacterial pathogens. J. Mol. Microbiol. Biotechnol. 9, 198–213 (2005).
Grammann, K., Volke, A. & Kunte, H. J. New type of osmoregulated solute transporter identified in halophilic members of the bacteria domain: TRAP transporter TeaABC mediates uptake of ectoine and hydroxyectoine in Halomonas elongata DSM 2581T. J. Bacteriol. 184, 3078–3085 (2002).
Edwards, B. R. et al. Rapid microbial respiration of oil from the Deepwater Horizon spill in offshore surface waters of the Gulf of Mexico. Environ. Res. Lett. 6, 035301 (2011).
McKay, L. J., Gutierrez, T. & Teske, A. P. Development of a group-specific 16S rRNA-targeted probe set for the identification of Marinobacter by fluorescence in situ hybridization. Deep Sea Res. II http://dx.doi.org/10.1016/j.dsr2.2013.10.009 (2014).
Lamendella, R. et al. Assessment of the Deepwater Horizon oil spill impact on Gulf coast microbial communities. Aquat. Microbiol. 5, 130 (2014).
Salomon, D. et al. Type VI secretion system toxins horizontally shared between marine bacteria. PLoS Pathogens 11, e1005128 (2015).
Vaysse, P.-J. et al. Proteomic analysis of Marinobacter hydrocarbonoclasticus SP17 biofilm formation at the alkane–water interface reveals novel proteins and cellular processes involved in hexadecane assimilation. Res. Microbiol. 160, 829–837 (2009).
Arnosti, C., Ziervogel, K., Yang, T. & Teske, A. Oil-derived marine aggregates—hot spots of polysaccharide degradation by specialized bacterial communities. Deep Sea Res. II http://dx.doi.org/10.1016/j.dsr2.2014.12.008 (2015).
Baker, B. J., Lesniewski, R. A. & Dick, G. J. Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume. ISME J. 6, 2269–2279 (2012).
Kujawinski, E. B. et al. Fate of dispersants associated with the Deepwater Horizon oil spill. Environ. Sci. Technol. 45, 1298–1306 (2011).
Tillett, D. & Neilan, B. A. Xanthogenate nucleic acid isolation from cultured and environmental cyanobacteria. J. Phycol. 36, 251–258 (2000).
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10–12 (2011).
Sickle v. 1.33 (Joshi, N. & Fass, J., 2011); https://github.com/najoshi/sickle
Peng, Y., Leung, H. C. M., Yiu, S. M. & Chin, F. Y. L. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420–1428 (2012).
Dick, G. J. et al. Community-wide analysis of microbial genome sequence signatures. Genome Biol. 10, R85 (2009).
Baker, B. J. Omic approaches in microbial ecology: charting the unknown. Microbe 8, 353–360 (2013).
Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).
Overbeek, R. et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 42, D206–D214 (2014).
Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).
Darling, A. E. et al. PhyloSift: phylogenetic analysis of genomes and metagenomes. PeerJ 2, e243 (2014).
Sorek, R. et al. Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318, 1449–1452 (2007).
Castelle, C. J. et al. Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr. Biol. 25, 690–701 (2015).
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
Miller, C. S., Baker, B. J., Thomas, B. C., Singer, S. W. & Banfield, J. F. EMIRGE reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol. 12, R44 (2011).
Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004).
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003).
Eren, A. M. et al. Anvi'o: an advanced analysis and visualization platform for ’omics data. PeerJ 3, e1319 (2015).
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at http://arXiv.org/1303.3997 (2013).
Zhao, Y., Tang, H. & Ye, Y. RAPSearch2: a fast and memory-efficient protein similarity search tool for next-generation sequencing data. Bioinformatics 28, 125–126 (2012).
The metagenomic DNA originated from work that was supported by a Marie Curie International Outgoing Fellowship (PIOF-GA-2008-220129) to T.G. within the 7th European Community Framework Programme. Sampling in the Gulf of Mexico and SIP experiments underlying this study were made possible in part by a grant from The Gulf of Mexico Research Initiative and in part by a Marie Curie Fellowship to T.G. A.T. also acknowledges funding from the National Science Foundation (RAPID Response: the microbial response to the Deepwater Horizon Oil Spill; NSF-OCE 1045115). Data are publicly available through the Gulf of Mexico Research Initiative Information & Data Cooperative (GRIIDC) at https://data.gulfresearchinitiative.org (doi:10.7266/N7GH9FZ8). This is ECOGIG contribution 431.
The authors declare no competing financial interests.
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Dombrowski, N., Donaho, J., Gutierrez, T. et al. Reconstructing metabolic pathways of hydrocarbon-degrading bacteria from the Deepwater Horizon oil spill. Nat Microbiol 1, 16057 (2016). https://doi.org/10.1038/nmicrobiol.2016.57
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