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Using dispersants after oil spills: impacts on the composition and activity of microbial communities

Abstract

Dispersants are globally and routinely applied as an emergency response to oil spills in marine ecosystems with the goal of chemically enhancing the dissolution of oil into water, which is assumed to stimulate microbially mediated oil biodegradation. However, little is known about how dispersants affect the composition of microbial communities or their biodegradation activities. The published findings are controversial, probably owing to variations in laboratory methods, the selected model organisms and the chemistry of different dispersant–oil mixtures. Here, we argue that an in-depth assessment of the impacts of dispersants on microorganisms is needed to evaluate the planning and use of dispersants during future responses to oil spills.

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Figure 1: Dispersants and their interaction with oil in sea water.
Figure 2: Hydrocarbon degradation following the Deepwater Horizon oil spill.

References

  1. 1

    Leahy, J. G. & Colwell, R. R. Microbial degradation of hydrocarbons in the environment. Microbiol. Rev. 54, 305–315 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. 2

    Tissot, B. P. & Welte, D. H. Petroleum Formation and Occurrence: A New Approach to Oil and Gas Exploration 2nd edn (Springer, 1984).

    Google Scholar 

  3. 3

    Putscher, R. E. Isolation of olefins from Bradford crude oil. Anal. Chem. 24, 1551–1558 (1952).

    CAS  Google Scholar 

  4. 4

    Kvenvolden, K. A. & Cooper, C. K. Natural seepage of crude oil into the marine environment. Geo-Mar. Lett. 23, 140–146 (2003).

    CAS  Google Scholar 

  5. 5

    National Research Council. Oil in the Sea III: Inputs, Fates, and Effects (National Academies Press, 2003).

  6. 6

    Joye, S. B., Bowles, M. W., Samarkin, V. A., Hunter, K. S. & Niemann, H. Biogeochemical signatures and microbial activity of different cold-seep habitats along the Gulf of Mexico deep slope. Deep-Sea Res. II 57, 1990–2001 (2010).

    CAS  Google Scholar 

  7. 7

    Hazen, T. C. et al. Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330, 204–208 (2010).

    CAS  PubMed  Google Scholar 

  8. 8

    Ziervogel, K. et al. Microbial activities and dissolved organic matter dynamics in oil-contaminated surface seawater from the Deepwater Horizon oil spill site. PLoS ONE 7, e34816 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    Desai, J. D. & Banat, I. M. Microbial production of surfactants and their commercial potential. Microbiol. Mol. Biol. Rev. 61, 47–64 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Passow, U. Formation of rapidly-sinking, oil-associated marine snow. Deep-Sea Res. II http://dx.doi.org/10.1016/j.dsr2.2014.10.001 (2014).

  11. 11

    Joye, S. B., Teske, A. P. & Kostka, J. E. Microbial dynamics following the Macondo oil well blowout across Gulf of Mexico environments. BioScience 64, 766–777 (2014).

    Google Scholar 

  12. 12

    Steen, A. Frequency of dispersant use worldwide. Int. Oil Spill Con. Proc. 2008, 645–650 (2008).

    Google Scholar 

  13. 13

    Bruheim, P., Bredholt, H. & Eimhjellen, K. Effects of surfactant mixtures, including Corexit 9527, on bacterial oxidation of acetate and alkanes in crude oil. Appl. Environ. Microbiol. 65, 1658–1661 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14

    Foght, J. M. & Westlake, D. W. S. Effect of the dispersant Corexit 9527 on the microbial degradation of Prudhoe Bay oil. Can. J. Microbiol. 28, 117–122 (1982).

    CAS  Google Scholar 

  15. 15

    Macias-Zamora, J. V., Meléndez-Sánchez, A. L., Ramírez-Álvarez, N., Gutiérrez-Galindo, E. A. & Orozco-Borbón, M. V. On the effects of the dispersant Corexit 9500© during the degradation process of n-alkanes and PAHs in marine sediments. Environ. Monit. Assess. 186, 1051–1061 (2014).

    CAS  PubMed  Google Scholar 

  16. 16

    Bælum, J. et al. Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill. Environ. Microbiol. 14, 2405–2416 (2012).

    PubMed  Google Scholar 

  17. 17

    Lindstrom, J. E. & Braddock, J. F. Biodegradation of petroleum hydrocarbons at low temperature in the presence of the dispersant Corexit 9500. Mar. Pollut. Bull. 44, 739–747 (2002).

    CAS  PubMed  Google Scholar 

  18. 18

    Chakraborty, R., Borglin, S. E., Dubinsky, E. A., Andersen, G. L. & Hazen, T. C. Microbial response to the MC-252 oil and corexit 9500 in the Gulf of Mexico. Front. Microbiol. 3, 357 (2012).

    PubMed  PubMed Central  Google Scholar 

  19. 19

    Chandrasekar, S., Sorial, G. A. & Weaver, J. W. Dispersant effectiveness on oil spills — impact of salinity. ICES J. Mar. Sci. 63, 1418–1430 (2006).

    CAS  Google Scholar 

  20. 20

    Fingas, M., Wang, Z., Fieldhouse, B. & Smith, P. Chemical characteristics of an oil and the relationship to dispersant effectiveness. BSEE [online], (2003).

    Google Scholar 

  21. 21

    Weaver, J. W. Characteristics of spilled oils, fuels and petroleum products: 3a. Simulation of oil spills and dispersants under conditions of uncertainty. EPA [online], (2004).

    Google Scholar 

  22. 22

    Kuhl, A. J., Nyman, J. A., Kaller, M. D. & Green, C. C. Dispersant and salinity effects on weathering and acute toxicity of South Louisiana crude oil. Environ. Toxicol. Chem. 32, 2611–2620 (2013).

    CAS  PubMed  Google Scholar 

  23. 23

    Jernelöv, A. & Olof, L. Ixtoc I: a case study of the world's largest oil spill. Ambio 10, 299–306 (1981).

    Google Scholar 

  24. 24

    Lewis, A., Crosbie, A., Davies, L. & Lunel, T. Dispersion of Emulsified Oils at Sea (AEA Technology, 1998).

    Google Scholar 

  25. 25

    Gilfillan, E. S. et al. Tidal area dispersant experiment, Searsport Maine: an overview. Int. Oil Spill Con. Proc. 1985, 553–559 (1985).

    Google Scholar 

  26. 26

    Prince, R. C. et al. The primary biodegradation of dispersed crude oil in the sea. Chemosphere 90, 521–526 (2013).

    CAS  PubMed  Google Scholar 

  27. 27

    Moore, C. M. et al. Processes and patterns of oceanic nutrient limitation. Nature Geosci. 6, 701–710 (2013).

    CAS  Google Scholar 

  28. 28

    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).

    Google Scholar 

  29. 29

    Yoshida, A. et al. Microbial responses using denaturing gradient gel electrophoresis to oil and chemical dispersant in enclosed ecosystems. Mar. Pollut. Bull. 52, 89–95 (2006).

    CAS  PubMed  Google Scholar 

  30. 30

    Martha, D. & Mulligan, C. N. Rhamnolipid biosurfactant assisted dispersion and biodegradation of spilled oil on surface waters. Proc. Annu. Conf. Can. Soc. Civil Engineer (2005).

  31. 31

    Zahed, M., Aziz, H., Isa, M. & Mohajeri, L. Effect of initial oil concentration and dispersant on crude oil biodegradation in contaminated seawater. Bull. Environ. Contam. Toxicol. 84, 438–442 (2010).

    CAS  PubMed  Google Scholar 

  32. 32

    Mason, O. U. et al. Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill. ISME J. 8, 1464–1475 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33

    Committee on Understanding Oil Spill Dispersants. Oil Spill Dispersants: Efficacy and Effects (National Academies Press, 2005).

  34. 34

    Pham, P. H., Huang, Y. J., Chen, C. & Bols, N. C. Corexit 9500 inactivates two enveloped viruses of aquatic animals but enhances the infectivity of a nonenveloped fish virus. Appl. Environ. Microbiol. 80, 1035–1041 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. 35

    Fuller, C. et al. Comparative toxicity of oil, dispersant, and oil plus dispersant to several marine species. Environ. Toxicol. Chem. 23, 2941–2949 (2004).

    PubMed  Google Scholar 

  36. 36

    Bulich, A. A. & Isenberg, D. L. Use of the luminescent bacterial system for the rapid assessment of aquatic toxicity. ISA Trans. 20, 29–33 (1981).

    CAS  PubMed  Google Scholar 

  37. 37

    Fernández, A., Tejedor, C., Cabrera, F. & Chordi, A. Assessment of toxicity of river water and effluents by the bioluminescence assay using Photobacterium phosphoreum. Water Res. 29, 1281–1286 (1995).

    Google Scholar 

  38. 38

    Guzzella, L. & Mingazzini, M. Biological assaying of organic compounds in surface waters. Water Sci. Technol. 30, 113–124 (1994).

    CAS  Google Scholar 

  39. 39

    Hao, O. J., Shin, C.-J., Lin, C.-F., Jeng, F.-T. & Chen, Z.-C. Use of microtox tests for screening industrial wastewater toxicity. Water Sci. Technol. 34, 43–50 (1996).

    CAS  Google Scholar 

  40. 40

    Gustavson, K. E., Svenson, A. & Harkin, J. M. Comparison of toxicities and mechanism of action of n-alkanols in the submitochondrial particle and the Vibrio fischeri bioluminescence (Microtox®) bioassay. Environ. Toxicol. Chem. 17, 1917–1921 (1998).

    CAS  Google Scholar 

  41. 41

    Johnson, B. T. & Long, E. R. Rapid toxicity assessment of sediments from estuarine ecosystems: a new tandem in vitro testing approach. Environ. Toxicol. Chem. 17, 1099–1106 (1998).

    CAS  Google Scholar 

  42. 42

    Svenson, A., Edsholt, E., Ricking, M., Remberger, M. & Röttorp, J. Sediment contaminants and microtox toxicity tested in a direct contact exposure test. Environ. Toxicol. Water Qual. 11, 293–300 (1996).

    CAS  Google Scholar 

  43. 43

    Gälli, R., Munz, C. D. & Scholtz, R. Evaluation and application of aquatic toxicity tests: use of the Microtox test for the prediction of toxicity based upon concentrations of contaminants in soil. Hydrobiologia 273, 179–189 (1994).

    Google Scholar 

  44. 44

    Radniecki, T. S., Schneider, M. C. & Semprini, L. The influence of Corexit 9500A and weathering on Alaska North Slope crude oil toxicity to the ammonia oxidizing bacterium, Nitrosomonas europaea. Mar. Pollut. Bull. 68, 64–70 (2013).

    CAS  PubMed  Google Scholar 

  45. 45

    Nelson-Smith, A. Oil Pollution and Marine Ecology (Plenum Press, 1973).

    Google Scholar 

  46. 46

    Nagell, B., Notini, M. & Grahn, O. Toxicity of four oil dispersants to some animals from the Baltic Sea. Mar. Biol. 28, 237–243 (1974).

    CAS  Google Scholar 

  47. 47

    Hamdan, L. & Fulmer, P. Effects of COREXIT®EC9500A on bacteria from a beach oiled by the Deepwater Horizon spill. Aquat. Microb. Ecol. 63, 101–109 (2011).

    Google Scholar 

  48. 48

    Ortmann, A. C. et al. Dispersed oil disrupts microbial pathways in pelagic food webs. PLoS ONE 7, e42548 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 49

    Zuijdgeest, A. & Huettel, M. Dispersants as used in response to the MC252-spill lead to higher mobility of polycyclic aromatic hydrocarbons in oil-contaminated Gulf of Mexico sand. PLoS ONE 7, e50549 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 50

    Johnson, B. T. in Small-scale Freshwater Toxicity Investigations (eds Blaise, C. & Férard, J.-F.) 69–105 (Springer, 2005).

    Google Scholar 

  51. 51

    Rosen, G., Osorio-Robayo, A., Rivera-Duarte, I. & Lapota, D. Comparison of bioluminescent Dinoflagellate (QwikLite) and bacterial (Microtox) rapid bioassays for the detection of metal and ammonia toxicity. Arch. Environ. Contam. Toxicol. 54, 606–611 (2008).

    CAS  PubMed  Google Scholar 

  52. 52

    Paul, J. H. et al. Toxicity and mutagenicity of Gulf of Mexico waters during and after the Deepwater Horizon oil spill. Environ. Sci. Technol. 47, 9651–9659 (2013).

    CAS  PubMed  Google Scholar 

  53. 53

    US Environmental Protection Agency. Alphabetical list of NCP product schedule (products available for use during an oil spill). EPA [online], (2013).

  54. 54

    Singer, M. M. et al. Standardization of the preparation and quantitation of water-accommodated fractions of petroleum for toxicity testing. Mar. Pollut. Bull. 40, 1007–1016 (2000).

    CAS  Google Scholar 

  55. 55

    White, H. K. et al. Long-term persistence of dispersants following the Deepwater Horizon oil spill. Environ. Sci. Technol. Lett. 1, 295–299 (2014).

    CAS  Google Scholar 

  56. 56

    Venkataraman, P. et al. Attachment of a hydrophobically modified biopolymer at the oil-water interface in the treatment of oil spills. ACS Appl. Mater. Interfaces 5, 3572–3580 (2013).

    CAS  PubMed  Google Scholar 

  57. 57

    Yakimov, M. M. et al. Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int. J. Syst. Bacteriol. 48, 339–348 (1998).

    CAS  PubMed  Google Scholar 

  58. 58

    Dyksterhouse, S. E., Gray, J. P., Herwig, R. P., Lara, J. C. & Staley, J. T. Cycloclasticus pugetii gen. nov., sp. nov., an aromatic hydrocarbon-degrading bacterium from marine sediments. Int. J. Syst. Bacteriol. 45, 116–123 (1995).

    CAS  PubMed  Google Scholar 

  59. 59

    Golyshin, P. N. et al. Oleiphilaceae fam. nov., to include Oleiphilus messinensis gen. nov., sp. nov., a novel marine bacterium that obligately utilizes hydrocarbons. Int. J. Syst. Evol. Microbiol. 52, 901–911 (2002).

    CAS  PubMed  Google Scholar 

  60. 60

    Yakimov, M. M. et al. Oleispira antarctica gen. nov., sp. nov., a novel hydrocarbonoclastic marine bacterium isolated from Antarctic coastal sea water. Int. J. Syst. Evol. Microbiol. 53, 779–785 (2003).

    CAS  PubMed  Google Scholar 

  61. 61

    Yakimov, M. M. et al. Thalassolituus oleivorans gen. nov., sp. nov., a novel marine bacterium that obligately utilizes hydrocarbons. Int. J. Syst. Evol. Microbiol. 54, 141–148 (2004).

    CAS  PubMed  Google Scholar 

  62. 62

    Engelhardt, M. A., Daly, K., Swannell, R. P. & Head, I. M. Isolation and characterization of a novel hydrocarbon-degrading, Gram-positive bacterium, isolated from intertidal beach sediment, and description of Planococcus alkanoclasticus sp. nov. J. Appl. Microbiol. 90, 237–247 (2001).

    CAS  PubMed  Google Scholar 

  63. 63

    Kleindienst, S. et al. Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps. ISME J. 8, 2029–2044 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 64

    Kleindienst, S., Ramette, A., Amann, R. & Knittel, K. Distribution and in situ abundance of sulfate-reducing bacteria in diverse marine hydrocarbon seep sediments. Environ. Microbiol. 14, 2689–2710 (2012).

    CAS  PubMed  Google Scholar 

  65. 65

    Orcutt, B. N. et al. Impact of natural oil and higher hydrocarbons on microbial diversity, distribution, and activity in Gulf of Mexico cold-seep sediments. Deep-Sea Res. II 57, 2008–2021 (2010).

    CAS  Google Scholar 

  66. 66

    Shao, Z. & Wang, W. Enzymes and genes involved in aerobic alkane degradation. Front. Microbiol. 4, 116 (2013).

    PubMed  PubMed Central  Google Scholar 

  67. 67

    Sabirova, J. S., Ferrer, M., Regenhardt, D., Timmis, K. N. & Golyshin, P. N. Proteomic insights into metabolic adaptations in Alcanivorax borkumensis induced by alkane utilization. J. Bacteriol. 188, 3763–3773 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68

    Kessler, J. D. et al. A persistent oxygen anomaly reveals the fate of spilled methane in the deep Gulf of Mexico. Science 331, 312–315 (2011).

    CAS  PubMed  Google Scholar 

  69. 69

    Valentine, D. L. et al. Propane respiration jump-starts microbial response to a deep oil spill. Science 330, 208–211 (2010).

    CAS  PubMed  Google Scholar 

  70. 70

    McNutt, M. K. et al. Review of flow rate estimates of the Deepwater Horizon oil spill. Proc. Natl Acad. Sci. USA 109, 20260–20267 (2012).

    PubMed  Google Scholar 

  71. 71

    National Commission on the BP Deepwater Horizon Oil Spill and Offshore Drilling. The use of surface and subsea dispersants during the BP Deepwater Horizon oil spill. GPO [online], (2011).

  72. 72

    Camilli, R. et al. Tracking hydrocarbon plume transport and biodegradation at Deepwater Horizon. Science 330, 201–204 (2010).

    CAS  PubMed  Google Scholar 

  73. 73

    Diercks, A.-R. et al. Characterization of subsurface polycyclic aromatic hydrocarbons at the Deepwater Horizon site. Geophys. Res. Lett. 37, L20602 (2010).

    Google Scholar 

  74. 74

    Socolofsky, S. A., Adams, E. E. & Sherwood, C. R. Formation dynamics of subsurface hydrocarbon intrusions following the Deepwater Horizon blowout. Geophys. Res. Lett. 38, L09602 (2011).

    Google Scholar 

  75. 75

    Joye, S. B., MacDonald, I. R., Leifer, I. & Asper, V. Magnitude and oxidation potential of hydrocarbon gases released from the BP oil well blowout. Nature Geosci. 4, 160–164 (2011).

    CAS  Google Scholar 

  76. 76

    Reddy, C. M. et al. Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill. Proc. Natl Acad. Sci. USA 109, 20229–20234 (2012).

    CAS  PubMed  Google Scholar 

  77. 77

    Gray, J. L. et al. Presence of the Corexit component dioctyl sodium sulfosuccinate in Gulf of Mexico waters after the 2010 Deepwater Horizon oil spill. Chemosphere 95, 124–130 (2014).

    CAS  PubMed  Google Scholar 

  78. 78

    Kujawinski, E. B. et al. Fate of dispersants associated with the Deepwater Horizon oil spill. Environ. Sci. Technol. 45, 1298–1306 (2011).

    CAS  PubMed  Google Scholar 

  79. 79

    Atlas, R. M. & Hazen, T. C. Oil biodegradation and bioremediation: a tale of the two worst spills in U. S. history. Environ. Sci. Technol. 45, 6709–6715 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. 80

    Dubinsky, E. A. et al. 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 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. 81

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. 82

    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).

    CAS  PubMed  Google Scholar 

  83. 83

    Valentine, D. L. et al. Dynamic autoinoculation and the microbial ecology of a deep water hydrocarbon irruption. Proc. Natl Acad. Sci. USA 109, 20286–20291 (2012).

    CAS  PubMed  Google Scholar 

  84. 84

    Passow, U., Ziervogel, K., Asper, V. & Diercks, A. Marine snow formation in the aftermath of the Deepwater Horizon oil spill in the Gulf of Mexico. Environ. Res. Lett. 7, 035301 (2012).

    Google Scholar 

  85. 85

    Yin, F., John, G. F., Hayworth, J. S. & Clement, T. P. Long-term monitoring data to describe the fate of polycyclic aromatic hydrocarbons in Deepwater Horizon oil submerged off Alabama's beaches. Sci. Total Environ. 508, 46–56 (2015).

    CAS  PubMed  Google Scholar 

  86. 86

    Lamendella, R. et al. Assessment of the Deepwater Horizon oil spill impact on Gulf coast microbial communities. Front. Microbiol. 5, 130 (2014).

    PubMed  PubMed Central  Google Scholar 

  87. 87

    Widdel, F., Knittel, K. & Galushko, A. in Handbook of Hydrocarbon and Lipid Microbiology Vol. 3 (eds Timmis, K. N. et al.) 1997–2021 (Springer Berlin Heidelberg, 2010).

    Google Scholar 

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Acknowledgements

The authors acknowledge the BP/Gulf of Mexico Research Initiative (GoMRI) for supporting the ECOGIG (Ecosystem Impacts of Oil and Gas Inputs to the Gulf; to S.B.J.) and C-IMAGE (Center for Integrated Modeling and Analysis of Gulf Ecosystems; to J.H.P) consortia. Additional support from the Guy Harvey Ocean Research Foundation (to J.H.P.) is also appreciated. This paper is ECOGIG contribution number 204.

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Correspondence to Samantha B. Joye.

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Kleindienst, S., Paul, J. & Joye, S. Using dispersants after oil spills: impacts on the composition and activity of microbial communities. Nat Rev Microbiol 13, 388–396 (2015). https://doi.org/10.1038/nrmicro3452

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