Skip to main content

Microbial Communities Responding to Deep-Sea Hydrocarbon Spills

  • Living reference work entry
  • First Online:
Book cover Microbial Communities Utilizing Hydrocarbons and Lipids: Members, Metagenomics and Ecophysiology

Abstract

The 2010 Deepwater Horizon oil spill in the Gulf of Mexico can be considered the world’s first deep-sea hydrocarbon spill. Deep-sea hydrocarbon spills occur in a different setting than surface oil spills, and the organisms that respond must be adapted to this low-temperature, high-pressure environment. The hydrocarbon composition can also be quite different than at the sea surface, with high concentrations of dissolved hydrocarbons, including natural gas, and suspended droplets of petroleum. We discuss the bacteria that may respond to these spills and factors that affect their abundance, based on data collected during the Deepwater Horizon spill and in microcosm experiments in the following years.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Institutional subscriptions

References

  • Bacosa HP, Erdner DL, Rosenheim BE, Shetty P, Seitz KW, Baker BJ, Liu Z (2018) Hydrocarbon degradation and response of seafloor sediment bacterial community in the northern Gulf of Mexico to light Louisiana sweet crude oil. ISME J. https://doi.org/10.1038/s41396-018-0190-1

    Article  CAS  Google Scholar 

  • Bælum J, Borglin S, Chakraborty R, Fortney JL, Lamendella R, Mason OU, Auer M, Zemla M, Bill M, Conrad ME, Malfatti SA, Tringe SG, Holman H-Y, Hazen TC, Jansson JK (2012) Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill. Environ Microbiol 14:2405–2416

    Article  Google Scholar 

  • Bagby SC, Reddy CM, Aeppli C, Fisher GB, Valentine DL (2017) Persistence and biodegradation of oil at the ocean floor following Deepwater Horizon. Proc Natl Acad Sci 114:E9–E18

    Article  CAS  Google Scholar 

  • Beck DA, Kalyuzhnaya MG, Malfatti S, Tringe SG, del Rio TG, Ivanova N, Lidstrom ME, Chistoserdova L (2013) A metagenomic insight into freshwater methane-utilizing communities and evidence for cooperation between the Methylococcaceae and the Methylophilaceae. PeerJ 1:e23

    Article  Google Scholar 

  • Brakstad OG, Nonstad I, Faksness L-G, Brandvik PJ (2008) Responses of microbial communities in Arctic sea ice after contamination by crude petroleum oil. Microb Ecol 55:540–552

    Article  Google Scholar 

  • Brakstad OG, Throne-Holst M, Netzer R, Stoeckel DM, Atlas RM (2015) Microbial communities related to biodegradation of dispersed Macondo oil at low seawater temperature with Norwegian coastal seawater. Microb Biotechnol 8:989–998

    Article  CAS  Google Scholar 

  • Brakstad OG, Ribicic D, Winkler A, Netzer R (2018) Biodegradation of dispersed oil in seawater is not inhibited by a commercial oil spill dispersant. Mar Pollut Bull 129:555–561

    Article  CAS  Google Scholar 

  • Buchan A, LeCleir GR, Gulvik CA, González JM (2014) Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12:686–698

    Article  CAS  Google Scholar 

  • Campeão ME, Reis L, Leomil L, de Oliveira L, Otsuki K, Gardinali P, Pelz O, Valle R, Thompson FL, Thompson CC (2017) The deep-sea microbial community from the Amazonian Basin associated with oil degradation. Front Microbiol 8:1019

    Article  Google Scholar 

  • Chakraborty R, Borglin SE, Dubinsky EA, Andersen GL, Hazen TC (2012) Microbial response to the MC-252 oil and Corexit 9500 in the Gulf of Mexico. Front Microbiol 3:357

    PubMed  PubMed Central  Google Scholar 

  • Coulon F, McKew B, Osborn A, McGenity T, Timmis K (2007) Effects of temperature and biostimulation on oil-degrading microbial communities in temperate estuarine waters. Environ Microbiol 9:177–189

    Article  CAS  Google Scholar 

  • Crespo-Medina M, Meile C, Hunter K, Diercks A, Asper V, Orphan V, Tavormina P, Nigro L, Battles J, Chanton J (2014) The rise and fall of methanotrophy following a deepwater oil-well blowout. Nat Geosci 7:423–427

    Article  CAS  Google Scholar 

  • Crespo-Medina M, Meile CD, Hunter KS, Diercks AR, Asper VL, Orphan VJ, Tavormina PL, Nigro LM, Battles JJ, Chanton JP, Shiller AM, Joung DJ, Amon RMW, Bracco A, Montoya JP, Villareal TA, Wood AM, Joye SB (2015) Addendum: the rise and fall of methanotrophy following a deepwater oil-well blowout. Nat Geosci 8:490

    Article  CAS  Google Scholar 

  • Cui Z, Xu G, Li Q, Gao W, Zheng L (2013) Genome sequence of the pyrene- and fuoranthene-degrading bacterium Cycloclasticus sp. strain PY97M. Genome Announc 1:e00536–e00513

    PubMed  PubMed Central  Google Scholar 

  • D’Ambrosio L, Ziervogel K, MacGregor B, Teske A, Arnosti C (2014) Composition and enzymatic function of particle-associated and free-living bacteria: a coastal/offshore comparison. ISME J 8:2167–2179

    Article  Google Scholar 

  • Delmont TO, Eren AM (2017) Simulations predict microbial responses in the environment? This environment disagrees retrospectively. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1712186114

    Article  CAS  Google Scholar 

  • Dubinsky EA, Conrad ME, Chakraborty R, Bill M, Borglin SE, Hollibaugh JT, Mason OU, Piceno YM, Reid FC, Stringfellow WT (2013) Succession of hydrocarbon-degrading bacteria in the aftermath of the Deepwater Horizon oil spill in the Gulf of Mexico. Environ Sci Technol 47:10860–10867

    Article  CAS  Google Scholar 

  • Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG, Sogin ML, Delmont TO (2015) Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ 3:e1319

    Article  Google Scholar 

  • Gros J, Socolofsky SA, Dissanayake AL, Jun I, Zhao L, Boufadel MC, Reddy CM, Arey JS (2017) Petroleum dynamics in the sea and influence of subsea dispersant injection during Deepwater Horizon. Proc Natl Acad Sci 114:10065–10070

    Article  CAS  Google Scholar 

  • Guibert LM, Loviso CL, Borglin S, Jansson JK, Dionisi HM, Lozada M (2016) Diverse bacterial groups contribute to the alkane degradation potential of chronically polluted subantarctic coastal sediments. Microb Ecol 71:100–112

    Article  CAS  Google Scholar 

  • Gutierrez T, Singleton DR, Berry D, Yang T, Aitken MD, Teske A (2013) Hydrocarbon-degrading bacteria enriched by the Deepwater Horizon oil spill identified by cultivation and DNA-SIP. ISME J 7:2091–2104

    Article  CAS  Google Scholar 

  • Hazen T, Dubinsky E, DeSantis T, Andersen G, Piceno Y, Singh N, Jansson J, Probst A, Borglin S, Fortney J (2010) Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330:204–208

    Article  CAS  Google Scholar 

  • Hu P, Dubinsky EA, Probst AJ, Wang J, Sieber CMK, Tom LM, Gardinali PR, Banfield JF, Atlas RM, Andersen GL (2017) Simulation of Deepwater Horizon oil plume reveals substrate specialization within a complex community of hydrocarbon degraders. Proc Natl Acad Sci 114:7432–7437

    Article  CAS  Google Scholar 

  • Joung D, Shiller AM (2013) Trace element distributions in the water column near the Deepwater Horizon well blowout. Environ Sci Technol 47:2161–2168

    Article  CAS  Google Scholar 

  • Joye SB, Leifer I, MacDonald IR, Chanton JP, Meile CD, Teske AP, Kostka JE, Chistoserdova L, Coffin R, Hollander D, Kastner M, Montoya JP, Rehder G, Solomon E, Treude T, Villareal TA (2011) Comment on “A persistent oxygen anomaly reveals the fate of spilled methane in the deep Gulf of Mexico”. Science 332:1033–1033

    Article  CAS  Google Scholar 

  • Kasai Y, Kishira H, Harayama S (2002) Bacteria belonging to the genus Cycloclasticus play a primary role in the degradation of aromatic hydrocarbons released in a marine environment. Appl Environ Microbiol 68:5625–5633

    Article  CAS  Google Scholar 

  • Kessler JD, Valentine DL, Redmond MC, Du M, Chan EW, Mendes SD, Quiroz EW, Villanueva CJ, Shusta SS, Werra LM (2011) A persistent oxygen anomaly reveals the fate of spilled methane in the deep Gulf of Mexico. Science 331:312–315

    Article  CAS  Google Scholar 

  • King G, Smith C, Tolar B, Hollibaugh J (2013) Analysis of composition and structure of coastal to mesopelagic bacterioplankton communities in the Northern Gulf of Mexico. Front Microbiol 3:438

    Google Scholar 

  • Kleindienst S, Seidel M, Ziervogel K, Grim S, Loftis K, Harrison S, Malkin SY, Perkins MJ, Field J, Sogin ML, Dittmar T, Passow U, Medeiros PM, Joye SB (2015) Chemical dispersants can suppress the activity of natural oil-degrading microorganisms. Proc Natl Acad Sci 112:14900–14905

    Article  CAS  Google Scholar 

  • Kleindienst S, Grim S, Sogin M, Bracco A, Crespo-Medina M, Joye SB (2016a) Diverse, rare microbial taxa responded to the Deepwater Horizon deep-sea hydrocarbon plume. ISME J 10:400–415

    Article  Google Scholar 

  • Kleindienst S, Seidel M, Ziervogel K, Grim S, Loftis K, Harrison S, Malkin SY, Perkins MJ, Field J, Sogin ML, Dittmar T, Passow U, Medeiros P, Joye SB (2016b) Reply to Prince et al.: ability of chemical dispersants to reduce oil spill impacts remains unclear. Proc Natl Acad Sci 113:E1422–E1423

    Article  CAS  Google Scholar 

  • Krause SMB, Johnson T, Samadhi Karunaratne Y, Fu Y, Beck DAC, Chistoserdova L, Lidstrom ME (2017) Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions. Proc Natl Acad Sci 114:358–363

    Article  CAS  Google Scholar 

  • Kujawinski EB, Kido Soule MC, Valentine DL, Boysen AK, Longnecker K, Redmond MC (2011) Fate of dispersants associated with the Deepwater Horizon oil spill. Environ Sci Technol 45:1298–1306

    Article  CAS  Google Scholar 

  • Lai Q, Li W, Wang B, Yu Z, Shao Z (2012) Complete genome sequence of the pyrene-degrading bacterium Cycloclasticus sp. strain P1. J Bacteriol 194:6677

    Article  CAS  Google Scholar 

  • Liu J, Bacosa HP, Liu Z (2017a) Potential environmental factors affecting oil-degrading bacterial populations in deep and surface waters of the Northern Gulf of Mexico. Front Microbiol 7:2131

    Article  Google Scholar 

  • Liu J, Techtmann SM, Woo HL, Ning D, Fortney JL, Hazen TC (2017b) Rapid response of Eastern Mediterranean deep sea microbial communities to oil. Sci Rep 7:5762

    Article  Google Scholar 

  • Lofthus S, Netzer R, Lewin AS, Heggeset TM, Haugen T, Brakstad OG (2018) Biodegradation of n-alkanes on oil–seawater interfaces at different temperatures and microbial communities associated with the degradation. Biodegradation 29:141–157

    Article  CAS  Google Scholar 

  • Lyu L-N, Ding H, Cui Z, Valentine DL (2018) The wax–liquid transition modulates hydrocarbon respiration rates in Alcanivorax borkumensis SK2. Environ Sci Technol Lett 5:277–282

    Article  CAS  Google Scholar 

  • Marietou A, Chastain R, Beulig F, Scoma A, Hazen TC, Bartlett DH (2018) The effect of hydrostatic pressure on enrichments of hydrocarbon degrading microbes from the Gulf of Mexico following the Deepwater Horizon oil spill. Front Microbiol 9:808

    Article  Google Scholar 

  • Maruyama A, Ishiwata H, Kitamura K, Sunamura M, Fujita T, Matsuo M, Higashihara T (2003) Dynamics of microbial populations and strong selection for Cycloclasticus pugetii following the Nakhodka oil spill. Microb Ecol 46:442–453

    Article  CAS  Google Scholar 

  • Mason OU, Hazen TC, Borglin S, Chain PS, Dubinsky EA, Fortney JL, Han J, Holman H-YN, Hultman J, Lamendella R (2012) Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill. ISME J 6:1715–1727

    Article  CAS  Google Scholar 

  • McCarren J, Becker JW, Repeta DJ, Shi Y, Young CR, Malmstrom RR, Chisholm SW, DeLong EF (2010) Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci 107:16420–16427

    Article  CAS  Google Scholar 

  • McKew B, Coulon F, Osborn A, Timmis K, McGenity T (2007) Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary, UK. Environ Microbiol 9:165–176

    Article  CAS  Google Scholar 

  • Mendes SD, Redmond MC, Voigritter K, Perez C, Scarlett R, Valentine DL (2015) Marine microbes rapidly adapt to consume ethane, propane, and butane within the dissolved hydrocarbon plume of a natural seep. J Geophys Res Oceans 120:1937–1953

    CAS  Google Scholar 

  • Messina E, Denaro R, Crisafi F, Smedile F, Cappello S, Genovese M, Genovese L, Giuliano L, Russo D, Ferrer M, Golyshin P, Yakimov MM (2016) Genome sequence of obligate marine polycyclic aromatic hydrocarbons-degrading bacterium Cycloclasticus sp. 78-ME, isolated from petroleum deposits of the sunken tanker Amoco Milford Haven, Mediterranean Sea. Mar Genomics 25:11–13

    Article  Google Scholar 

  • Methé B, Nelson K, Deming J, Momen B, Melamud E, Zhang X, Moult J, Madupu R, Nelson W, Dodson R (2005) The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci 102:10913–10918

    Article  Google Scholar 

  • Mishamandani S, Gutierrez T, Aitken M (2014) DNA-based stable isotope probing coupled with cultivation methods implicates Methylophaga in hydrocarbon degradation. Front Microbiol 5:76

    Article  Google Scholar 

  • Powell S, Bowman J, Snape I (2004) Degradation of nonane by bacteria from Antarctic marine sediment. Polar Biol 27:573–578

    Article  Google Scholar 

  • Prince RC, Coolbaugh TS, Parkerton TF (2016a) Oil dispersants do facilitate biodegradation of spilled oil. Proc Natl Acad Sci 113:E1421–E1421

    Article  CAS  Google Scholar 

  • Prince RC, Nash GW, Hill SJ (2016b) The biodegradation of crude oil in the deep ocean. Mar Pollut Bull 111:354–357

    Article  CAS  Google Scholar 

  • Prince RC, Butler JD, Redman AD (2017) The rate of crude oil biodegradation in the sea. Environ Sci Technol 51:1278–1284

    Article  CAS  Google Scholar 

  • Reddy CM, Arey JS, Seewald JS, Sylva SP, Lemkau KL, Nelson RK, Carmichael CA, McIntyre CP, Fenwick J, Ventura GT, Van Mooy BAS, Camilli R (2012) Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill. Proc Natl Acad Sci 109:20229–20234

    Article  CAS  Google Scholar 

  • Redmond MC, Valentine DL (2012) Temperature and natural gas structured the microbial community response to the Deepwater Horizon oil spill. Proc Natl Acad Sci 109:20292–20297

    Article  CAS  Google Scholar 

  • Redmond MC, Valentine DL, Sessions AL (2010) Identification of novel methane-, ethane-, and propane-oxidizing bacteria at marine hydrocarbon seeps by stable isotope probing. Appl Environ Microbiol 76:6412–6422

    Article  CAS  Google Scholar 

  • Ribicic D, Netzer R, Hazen TC, Techtmann SM, Drabløs F, Brakstad OG (2018a) Microbial community and metagenome dynamics during biodegradation of dispersed oil reveals potential key-players in cold Norwegian seawater. Mar Pollut Bull 129:370–378

    Article  CAS  Google Scholar 

  • Ribicic D, Netzer R, Winkler A, Brakstad OG (2018b) Microbial communities in seawater from an Arctic and a temperate Norwegian fjord and their potentials for biodegradation of chemically dispersed oil at low seawater temperatures. Mar Pollut Bull 129:308–317

    Article  CAS  Google Scholar 

  • Rivers AR, Sharma S, Tringe SG, Martin J, Joye SB, Moran MA (2013) Transcriptional response of bathypelagic marine bacterioplankton to the Deepwater Horizon oil spill. ISME J 7:2315–2329

    Article  CAS  Google Scholar 

  • Rubin-Blum M, Antony CP, Borowski C, Sayavedra L, Pape T, Sahling H, Bohrmann G, Kleiner M, Redmond MC, Valentine DL, Dubilier N (2017) Short-chain alkanes fuel mussel and sponge Cycloclasticus symbionts from deep-sea gas and oil seeps. Nat Microbiol 2:17093

    Article  CAS  Google Scholar 

  • Ryerson TB, Camilli R, Kessler JD, Kujawinski EB, Reddy CM, Valentine DL, Atlas E, Blake DR, de Gouw J, Meinardi S (2012) Chemical data quantify Deepwater Horizon hydrocarbon flow rate and environmental distribution. Proc Natl Acad Sci 109:20246–20253

    Article  CAS  Google Scholar 

  • Scoma A, Barbato M, Hernandez-Sanabria E, Mapelli F, Daffonchio D, Borin S, Boon N (2016) Microbial oil-degradation under mild hydrostatic pressure (10 MPa): which pathways are impacted in piezosensitive hydrocarbonoclastic bacteria? Sci Rep 6:23526

    Article  CAS  Google Scholar 

  • Shiller AM, Chan EW, Joung DJ, Redmond MC, Kessler JD (2017) Light rare earth element depletion during Deepwater Horizon blowout methanotrophy. Sci Rep 7:10389

    Article  CAS  Google Scholar 

  • Techtmann SM, Zhuang M, Campo P, Holder E, Elk M, Hazen TC, Conmy R, Santo Domingo JW (2017) Corexit 9500 enhances oil biodegradation and changes active bacterial community structure of oil-enriched microcosms. Appl Environ Microbiol 83:e03462–e03416

    Article  CAS  Google Scholar 

  • Valentine DL, Kessler JD, Redmond MC, Mendes SD, Heintz MB, Farwell C, Hu L, Kinnaman FS, Yvon-Lewis S, Du M (2010) Propane respiration jump-starts microbial response to a deep oil spill. Science 330:208–211

    Article  CAS  Google Scholar 

  • Valentine DL, Mezic I, Maćešić S, Črnjarić-Žic N, Ivic S, Hogand P, Fonoberov VA, Loire S (2012) Dynamic auto-inoculation and the microbial ecology of a deep water hydrocarbon irruption. Proc Natl Acad Sci 109:20286–20291

    Article  CAS  Google Scholar 

  • Wang B, Lai Q, Cui Z, Tan T, Shao Z (2008) A pyrene-degrading consortium from deep-sea sediment of the West Pacific and its key member Cycloclasticus sp. P1. Environ Microbiol 10:1948–1963

    Article  CAS  Google Scholar 

  • Yakimov MM, Gentile G, Bruni V, Cappello S, D’Auria G, Golyshin PN, Giuliano L (2004) Crude oil-induced structural shift of coastal bacterial communities of rod bay (Terra Nova Bay, Ross Sea, Antarctica) and characterization of cultured cold-adapted hydrocarbonoclastic bacteria. FEMS Microbiol Ecol 49:419–432

    Article  CAS  Google Scholar 

  • Yang T, Nigro LM, Gutierrez T, D’Ambrosio L, Joye SB, Highsmith R, Teske A (2016) Pulsed blooms and persistent oil-degrading bacterial populations in the water column during and after the Deepwater Horizon blowout. Deep-Sea Res II Top Stud Oceanogr 129:282–291

    Article  CAS  Google Scholar 

  • Yu Z, Chistoserdova L (2017) Communal metabolism of methane and the rare earth element switch. J Bacteriol 199:e00328-17

    Google Scholar 

Download references

Acknowledgments

DLV was supported by NSF OCE-1756947.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Molly C. Redmond .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this entry

Check for updates. Verify currency and authenticity via CrossMark

Cite this entry

Redmond, M.C., Valentine, D.L. (2019). Microbial Communities Responding to Deep-Sea Hydrocarbon Spills. In: McGenity, T. (eds) Microbial Communities Utilizing Hydrocarbons and Lipids: Members, Metagenomics and Ecophysiology . Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-60063-5_12-1

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-60063-5_12-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-60063-5

  • Online ISBN: 978-3-319-60063-5

  • eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences

Publish with us

Policies and ethics