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.
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Joung D, Shiller AM (2013) Trace element distributions in the water column near the Deepwater Horizon well blowout. Environ Sci Technol 47:2161–2168
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Powell S, Bowman J, Snape I (2004) Degradation of nonane by bacteria from Antarctic marine sediment. Polar Biol 27:573–578
Prince RC, Coolbaugh TS, Parkerton TF (2016a) Oil dispersants do facilitate biodegradation of spilled oil. Proc Natl Acad Sci 113:E1421–E1421
Prince RC, Nash GW, Hill SJ (2016b) The biodegradation of crude oil in the deep ocean. Mar Pollut Bull 111:354–357
Prince RC, Butler JD, Redman AD (2017) The rate of crude oil biodegradation in the sea. Environ Sci Technol 51:1278–1284
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Yu Z, Chistoserdova L (2017) Communal metabolism of methane and the rare earth element switch. J Bacteriol 199:e00328-17
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DLV was supported by NSF OCE-1756947.
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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
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