The Deepwater Horizon oil spill triggered a complex cascade of microbial responses that reshaped the dynamics of heterotrophic carbon degradation and the turnover of dissolved organic carbon (DOC) in oil contaminated waters. Our results from 21-day laboratory incubations in rotating glass bottles (roller bottles) demonstrate that microbial dynamics and carbon flux in oil-contaminated surface water sampled near the spill site two weeks after the onset of the blowout were greatly affected by activities of microbes associated with macroscopic oil aggregates. Roller bottles with oil-amended water showed rapid formation of oil aggregates that were similar in size and appearance compared to oil aggregates observed in surface waters near the spill site. Oil aggregates that formed in roller bottles were densely colonized by heterotrophic bacteria, exhibiting high rates of enzymatic activity (lipase hydrolysis) indicative of oil degradation. Ambient waters surrounding aggregates also showed enhanced microbial activities not directly associated with primary oil-degradation (β-glucosidase; peptidase), as well as a twofold increase in DOC. Concurrent changes in fluorescence properties of colored dissolved organic matter (CDOM) suggest an increase in oil-derived, aromatic hydrocarbons in the DOC pool. Thus our data indicate that oil aggregates mediate, by two distinct mechanisms, the transfer of hydrocarbons to the deep sea: a microbially-derived flux of oil-derived DOC from sinking oil aggregates into the ambient water column, and rapid sedimentation of the oil aggregates themselves, serving as vehicles for oily particulate matter as well as oil aggregate-associated microbial communities.
References
[1]
Atlas RM, Hazen TC (2011) Oil biodegradation and bioremediation: A tale of the two worst spills in US history. Environ Sci Technol 45(16): 6709–6715.
[2]
McNutt M, Camilli R, Guthrie G, Hsieh P, Labson V, et al. (2011) Assessment of flow rate estimates for the Deepwater Horizon/Macondo well oil spill. Flow rate technical group report to the national incident command, interagency solutions group, March 10, 2011.
[3]
Diercks AR, Highsmith RC, Asper VL, Joung D, Zhou Z, et al. (2010) Characterization of subsurface polycyclic aromatic hydrocarbons at the Deepwater Horizon site. Geophys Res Lett 37(L20602). doi:10.1029/2010GL045046.
[4]
Reddy CM, Arey JS, Seewald JS, Sylva SP, Lemkau KL, et al. (2011) Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill. Proc Natl Acad Sci U S A. doi:10.1073/pnas.1101242108.
[5]
Camilli R, Reddy CM, Yoerger DR, Van Mooy BAS, Jakuba MV, et al. (2010) Tracking hydrocarbon plume transport and biodegradation at Deepwater Horizon. Science 330: 201–204.
Kessler JD, Valentine DL, Redmond MC, Du M, Chan EW, et al. (2011) A persistent oxygen anomaly reveals the fate of spilled methane in the deep Gulf of Mexico. Science 331: 312–315.
[8]
Redmond MC, Valentine DL (2011) Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill. Proc Natl Acad Sci U S A. doi:10.1073/pnas.1108756108.
[9]
Valentine DL, Kessler JD, Redmond MC, Mendes SD, Heintz MB, et al. (2010) Propane respiration jump-starts microbial response to a deep oil spill. Science 330: 208–211.
[10]
Valentine DL, Mezi？ I, Ma？e？i？ S, ？rnjari？-？ic N, Ivi？ S, et al. (2012) Dynamic autoinoculation and the microbial ecology of a deep water hydrocarbon eruption. Proc Natl Acad Sci U S A. doi:10.1073/pnas.1108820109.
[11]
Head IM, Jones DM, R？ling WFM (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4: 173–182.
[12]
Operational Science Advisory Team (OSAT) (2010) Summary report for fate and effects of remnant oil in the beach environment. Available: http://www.restorethegulf.gov/sites/defa？ult/files/u316/OSAT-2%20Report%20no%20lt？r.pdf. Accessed 2011 September 14.
[13]
Niu H, Li Z, Lee K, Kepkay P, Mullin JV (2011) Modelling the transport of oil–mineral-aggregates (OMAs) in the marine environment and assessment of their potential risks. Environ Model Assess 16: 61–75.
[14]
National Research Council (NRC) (2003) Oil in the sea III: Inputs, fates, and effects. Washington, D.C.: National Academy Press. 265 p.
[15]
Unanue MA, Azua I, Arrieta JM, Herndl GJ, Iriberri J (1998) Laboratory-made particles as a useful approach to analyze microbial processes in marine macroaggregates. FEMS Microbiol Ecol 26: 325–334.
[16]
Ziervogel K, Steen AD, Arnosti C (2011) Changes in the spectrum and rates of extracellular enzyme activities in seawater following aggregate formation. Biogeosciences 7: 1007–1015.
[17]
Weiss MS, Abele U, Weckesser J, Welte W, Schiltz E, et al. (1991) Molecular architecture and electrostatic properties of a bacterial porin. Science 254: 1627–1630.
[18]
Arnosti C (2011) Microbial extracellular enzymes and the marine carbon cycle. Ann Rev Mar Sci 3: 401–425.
[19]
Shanks AL, Edmondson EW (1989) Laboratory-made artificial marine snow: A biological model of the real thing. Mar Biol 101: 463–470.
[20]
Diercks AR, Asper VL, Highsmith RC, Woolsey M, Lohrenz S, et al. (2010) NIUST - deep water horizon oil spill response cruise. Proceedings of the OCEANS 2010 MTS/IEEE Seattle Conference & Exhibition. 978-1-4244-4333-8.
[21]
Hoppe HG (1983) Significance of exoenzymatic activities in the ecology of brackish water - measurements by means of methylumbelliferyl-substrates. Mar Ecol Prog Ser 11: 299–308.
[22]
Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25: 943–948.
[23]
Velji MI, Albright LJ (1986) Microscopic enumeration of attached marine bacteria of seawater, marine sediment, fecal matter, and kelp blade samples following pyrophoshate and ultrasound treatments. Can J Microbiol 32: 121–126.
[24]
Stedmon CA, Markager S, Kaas H (2000) Optical properties and signatures of chromophoric dissolved organic matter (CDOM) in Danish coastal waters. Estuar Coast Shelf Sci 51: 267–278.
[25]
Fingas M, Fieldhouse B (2003) Studies of the formation process of water-in-oil emulsions. Mar Pollut Bull 47: 369–396.
[26]
Woysocki JA, Bianchi TS, Powell RT, Reuss N (2006) Spatial variability in the coupling of organic carbon, nutrients, and phytoplankton pigments in surface waters and sediments of the Mississippi River plume. Estuar Coast Shelf Sci 69: 47–63.
[27]
Coble PG (2007) Marine optical biogeochemistry: The chemistry of the ocean color. Chem Rev 107: 402–418.
[28]
Senesi N, Miano T, Provenzano M, Burnett G (1991) Characterization, differentiation, and classification of humic substances by fluorescence spectroscopy. Soil Sci 152: 259–271.
[29]
Ammerman JW, Glover WB (2000) Continuous underway measurement of microbial ectoenzyme activities in aquatic ecosystems. Mar Ecol Prog Ser 201: 1–12.
[30]
Murrell MC (2003) Bacterioplankton dynamics in a subtropical estuary: Evidence for substrate limitation. Aquat Microb Ecol 32: 239–250.
[31]
Hino S, Watanabe K, Tatkahashi N (1997) Isolation and characterization of slime-producing bacteria capable of utilizing petroleum hydrocarbons as a sole carbon source. J Ferment Bioeng 84: 528–531.
[32]
Gutierrez T, Mulloy B, Black K, Green DH (2007) Glycoprotein emulsifiers from two marine Halomonas species: Chemical and physical characterization. J Appl Microbiol 103: 1716–1727.
[33]
Kasei 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.
[34]
Iwabuchi N, Sunairi M, Urai M, Itoh C, Anzai H, et al. (2002) Extracellular polysaccharides of Rhodococcus rhodochrous S-2 stimulate the degradation of aromatic components in crude oil by indigenous marine bacteria. Appl Environ Microbiol 68: 2337–2343.
[35]
Patton JS, Rigler MW, Boehm PD, Fiest DL (1981) Ixtoc 1 oil spill: Flaking of surface mousse in the Gulf of Mexico. Nature 290: 235–238.
[36]
The Federal Interagency Solution group: Oil Budget Calculator Science and Engineering team (2010) Oil budget calculator technical documentation. Available: http://www.noaanews.noaa.gov/stories2010？/PDFs/OilBudgetCalc_Full_HQ-Print_111110？.pdf. Accessed 2011 September 14.
[37]
Operational Science Advisory Team (OSAT) (2010) Summary report for sub-sea and sub-surface oil and dispersant detection: Sampling and monitoring. Available: http://www.dep.state.fl.us/deepwaterhori？zon/files2/osat_report_17dec.pdf. Accessed 2011 September 13.
[38]
Alldredge AL, Gotschalk C (1988) In situ settling behavior of marine snow. Limnol Oceanogr 33(3): 339–351.
