Advertisement

Toward a Predictive Understanding of the Benthic Microbial Community Response to Oiling on the Northern Gulf of Mexico Coast

  • Joel E. KostkaEmail author
  • Will A. Overholt
  • Luis M. Rodriguez-R
  • Markus Huettel
  • Kostas Konstantinidis
Chapter

Abstract

Benthic ecosystems often act as a repository for oil contamination that washes ashore or is deposited onto sediments following a major oil spill. Sedimentary microorganisms mediate central ecosystem services on the coast, such as carbon and nutrient cycling, and these services may be adversely impacted by oil perturbation. Thus, during the response to the Deepwater Horizon (DWH) oil discharge in the Gulf of Mexico, considerable effort went into characterizing the response of benthic microbial communities to oil deposition on shorelines of the Northern Gulf where oil came ashore. Oil perturbation elicited a pronounced microbial response in coastal ecosystems, altering the abundance, diversity, and community composition of sedimentary microorganisms. Next-generation gene sequencing and metagenomic approaches, which were not available during previous large oil spills, have revolutionized the field of microbiology, providing new insights into the microbial response after the DWH discharge. This review centers on a case study of the fate of oil contamination in Pensacola Beach sands, which sheds light on the mechanisms of microbially mediated hydrocarbon degradation and the impacts of oiling to ecosystem functions. Analysis of field and laboratory results is discussed along with the technological advances that made these observations possible. Metagenomics enabled the application of ecological theory, thereby building a stronger foundation for the effective prediction of baseline microbial community structure/function and response to oiling. Oil perturbation was shown to resemble a press ecosystem disturbance according to the disturbance-specialization hypothesis. Benthic microbial communities were shown to be resilient, maintained ecosystem functions, and recovered quickly after oil disturbance.

Keywords

Sediment Nearshore Gulf of Mexico Microorganisms Petroleum hydrocarbons Bacteria Benthic Deepwater Horizon 

Notes

Funding Information

This research was made possible by grants from The Gulf of Mexico Research Initiative through its consortia: The Center for the Integrated Modeling and Analysis of the Gulf Ecosystem (C-IMAGE), Deep Sea to Coast Connectivity in the Eastern Gulf of Mexico (Deep-C). This research was also supported by grants from the National Science Foundation (to MH, JEK, WAO), the Florida Institute of Oceanography (to MH and JEK), and the Northern Gulf Institute (to MH and JEK).

References

  1. American Academy of Microbiology (2011) FAQ: microbes & oil spills. http://www.asmscience.org/content/report/faq?order=date
  2. Atlas RM (1995) Petroleum biodegradation and oil spill bioremediation. Mar Pollut Bull 31:178–182CrossRefGoogle Scholar
  3. Atlas RM, Hazen TC (2011) Oil biodegradation and bioremediation: a tale of the two worst spills in U.S. history. Environ Sci Technol 45(16):6709–6715.  https://doi.org/10.1021/es2013227CrossRefGoogle Scholar
  4. Barbato M, Scoma A, Mapelli F, De Smet R, Banat IM, Daffonchio D, Boon N, Borin S (2016) Hydrocarbonoclastic alcanivorax isolates exhibit different physiological and expression responses to n-dodecane. Front Microbiol 7:2056CrossRefGoogle Scholar
  5. Boufadel MC, Abdollahi-Nasab A, Geng X, Galt J, Torlapati J (2014) Simulation of the landfall of the Deepwater Horizon oil on the shorelines of the Gulf of Mexico. Environ Sci Technol 48(16):9496–9505CrossRefGoogle Scholar
  6. Brooks GR, Larson RA, Schwing PT, Romero I, Moore C, Reichart GJ, Jilbert T, Chanton JP, Hastings DW, Overholt WA, Marks KP, Kostka JE, Holmes CW, Hollander D (2015) Sedimentation pulse in the NE Gulf of Mexico following the 2010 DWH blowout. PLoS One 10(7):e0132341CrossRefGoogle Scholar
  7. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267CrossRefGoogle Scholar
  8. Dalyander PS, Long JW, Plant NG, Thompson DM (2014) Assessing mobility and redistribution patterns of sand and oil agglomerates in the surf zone. Mar Pollut Bull 80(1–2):200–209CrossRefGoogle Scholar
  9. 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:e1319CrossRefGoogle Scholar
  10. Gihring TM, Humphrys M, Mills HJ, Huette M, Kostka JE (2009) Identification of phytodetritus-degrading microbial communities in sublittoral Gulf of Mexico sands. Limnol Oceanogr 54(4):1073–1083CrossRefGoogle Scholar
  11. Gobet A, Böer SI, Huse SM, Van Beusekom JE, Quince C, Sogin ML, Boetius A, Ramette A (2012) Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISME J 6(3):542CrossRefGoogle Scholar
  12. Hayworth JS, Clement TP (2011) BP's operation deep clean-could dilution be the solution to beach pollution? Environ Sci Technol 45:4201–4202CrossRefGoogle Scholar
  13. Head IM, Jones DM, Roling WFM (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4:173–182CrossRefGoogle Scholar
  14. Huettel M, Berg P, Kostka JE (2014) Benthic exchange and biogeochemical cycling in permeable sediments. Annu Rev Mar Sci 6(1):23–51CrossRefGoogle Scholar
  15. Huettel M, Overholt WA, Kostka JE, Hagan C, Kaba J, Wells WB, Dudley S (2018) Degradation of Deepwater Horizon oil buried in a Florida beach influenced by tidal pumping. Mar Pollut Bull 126:488–500CrossRefGoogle Scholar
  16. Hunter EM, Mills HJ, Kostka JE (2006) Microbial community diversity associated with carbon and nitrogen cycling in permeable shelf sediments. Appl Environ Microbiol 72(9):5689–5701CrossRefGoogle Scholar
  17. Joye SB, Kleindienst S, Gilbert JA, Handley KM, Weisenhorn P, Overholt WA, Kostka JE (2016) Responses of microbial communities to hydrocarbon exposures. Oceanography 29(3):136–149CrossRefGoogle Scholar
  18. King GM, Kostka JE, Hazen TC, Sobecky PA (2015) Microbial responses to the Deepwater Horizon oil spill: from coastal wetlands to the deep sea. Annu Rev Mar Sci 7:377–401CrossRefGoogle Scholar
  19. Kostka JE, Prakash O, Overholt WA, Green S, Freyer G, Canion A, Delgardio J, Norton N, Hazen TC, Huettel M (2011) Hydrocarbon-degrading bacteria and the bacterial community response in Gulf of Mexico beach sands impacted by the Deepwater Horizon oil spill. Appl Environ Microbiol: AEM 77:7962–7974.  https://doi.org/10.1128/AEM.05402-11CrossRefGoogle Scholar
  20. Lamendella R, Strutt S, Borglin SE, Chakraborty R, Tas N, Mason OU, Hultman J, Prestat E, Hazen TC, Jansson JK (2014) Assessment of the Deepwater Horizon oil spill impact on Gulf coast microbial communities. Front Microbiol 5:130CrossRefGoogle Scholar
  21. Leahy JG, Colwell RR (1990) Microbial-degradation of hydrocarbons in the environment. Microbiol Rev 54:305–315Google Scholar
  22. Lea-Smith DJ, Biller SJ, Davey MP, Cotton CA, Sepulveda BMP, Turchyn AV, Scanlan DJ, Smith AG, Chisholm SW, Howe CJ (2015) Contribution of cyanobacterial alkane production to the ocean hydrocarbon cycle. Proc Natl Acad Sci 112(44):13591–13596CrossRefGoogle Scholar
  23. Louchouarn P, Yeager KM, Brunner CA, Briggs K, Guo L, Asper V, Coney N, Fortner C, Prouhet J, Schindler KJ, Martin KM, Zhou Z, Loeffler J, Jung A, Cruz V (2011) Deepwater Horizon: coastal ocean to Marsh margin sediment impacts. Abstracts of Papers of the American Chemical Society 241Google Scholar
  24. Lubchenco J, McNutt MK, Dreyfus G, Murawski SA, Kennedy DM, Anastas PT, Chu S, Hunter T (2012) Science in support of the Deepwater Horizon response. Proc Natl Acad Sci 109(50):20212–20221CrossRefGoogle Scholar
  25. McNutt MK, Chu S, Lubchenco J, Hunter T, Dreyfus G, Murawski SA, Kennedy DM (2012) Applications of science and engineering to quantify and control the Deepwater Horizon oil spill. Proc Natl Acad Sci 109(50):20222–20228CrossRefGoogle Scholar
  26. Michel J, Owens EH, Zengel S, Graham A, Nixon Z, Allard T, Holton W, Reimer PD, Lamarche A, White M, Rutherford N (2013) Extent and degree of shoreline oiling: Deepwater Horizon oil spill, Gulf of Mexico, USA. PloS One 8(6):e65087CrossRefGoogle Scholar
  27. Mills HJ, Hunter E, Humphrys M, Kerkhof L, McGuinness L, Huettel M, Kostka JE (2008) Characterization of nitrifying, denitrifying, and overall bacterial communities in permeable marine sediments of the northeastern Gulf of Mexico. Appl Environ Microbiol 74(14):4440–4453CrossRefGoogle Scholar
  28. Newton RJ, Huse SM, Morrison HG, Peake CS, Sogin ML, McLellan SL (2013) Shifts in the microbial community composition of Gulf Coast beaches following beach oiling. PLoS One 8:e74265CrossRefGoogle Scholar
  29. OSAT (2011) Summary report for fate and effects of remnant oil in the beach environment, Operational Science Advisory Team (OSAT-2). Team, Gulf Coast Incident Management Team. In: OSAT reports. USCGGoogle Scholar
  30. Overholt WA, Green SJ, Marks KP, Venkatraman R, Prakash O, Kostka JE (2013) Draft genome sequences for oil-degrading bacterial strains from beach sands impacted by the Deepwater Horizon oil spill. Genome Announc 1(6):e01015–e01013.  https://doi.org/10.1128/genomeA.01015-13CrossRefGoogle Scholar
  31. Overholt WA, Marks KP, Romero IC, Hollander DJ, Snell TW, Kostka JE (2016) Hydrocarbon-degrading bacteria exhibit a species-specific response to dispersed oil while moderating ecotoxicity. Appl Environ Microbiol 82(2):518–527CrossRefGoogle Scholar
  32. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil PA, Hugenholtz P (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36:996–1004CrossRefGoogle Scholar
  33. Passow U, Ziervogel K, Asper V, Diercks A (2012) Marine snow formation in the aftermath of the Deepwater Horizon oil spill in the Gulf of Mexico. Environ Res Lett 7(3):035301CrossRefGoogle Scholar
  34. Prince RC (2010) Bioremediation of marine oil spills. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin Heidelberg, pp 2618–2626Google Scholar
  35. Prosser JI (2012) Ecosystem processes and interactions in a morass of diversity. FEMS Microbiol Ecol 81(3):507–519CrossRefGoogle Scholar
  36. Prosser JI, Bohannan BJ, Curtis TP, Ellis RJ, Firestone MK, Freckleton RP, Green JL, Green LE, Killham K, Lennon JJ, Osborn AM (2007) The role of ecological theory in microbial ecology. Nat Rev Microbiol 5(5):384CrossRefGoogle Scholar
  37. Reddy CM, Arey JS, Seewald JS, Sylva SP, Lemkau KL, Nelson RK, Carmichael CA, McIntyre CP, Fenwick J, Ventura GT, Van Mooy B (2012) Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill. Proc Natl Acad Sci 109(50):20229–20234CrossRefGoogle Scholar
  38. Rodriguez-R LM, Overholt WA, Hagan C, Huettel M, Kostka JE, Konstantinidis KT (2015) Microbial community successional patterns in beach sands impacted by the Deepwater Horizon oil spill. ISME J 9:1928–1940CrossRefGoogle Scholar
  39. Sabirova JS, Ferrer M, Regenhardt D, Timmis KN, Golyshin PN (2006) Proteomic insights into metabolic adaptations in Alcanivorax borkumensis induced by alkane utilization. J Bacteriol 188(11):3763–3773.  https://doi.org/10.1128/JB.00072-06CrossRefGoogle Scholar
  40. Sabirova JS, Becker A, Lünsdorf H, Nicaud J-M, Timmis KN, Golyshin PN (2011) Transcriptional profiling of the marine oil-degrading bacterium Alcanivorax borkumensis during growth on n-alkanes. FEMS Microbiol Lett 319(2):160–168.  https://doi.org/10.1111/j.1574-6968.2011.02279.xCrossRefGoogle Scholar
  41. Schneiker S, dos Santos VAM, Bartels D, Bekel T, Brecht M, Buhrmester J, Chernikova TN, Denaro R, Ferrer M, Gertler C, Goesmann A, Golyshina OV, Kaminski F, Khachane AM, Lang S, Linke B, McHardy AC, Meyer F, Mechitaylo T, Pühler A, Regenhardt D, Rupp O, Sabirova JS, Selbitschka W, Yakimov MM, Timmis KN, Jorhӧlter FJ, Weidner S, Kaiser O, Golyshin PN (2006) Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nat Biotechnol 24(8):997–1004.  https://doi.org/10.1038/nbt1232CrossRefGoogle Scholar
  42. Shao Z, Wang W (2013) Enzymes and genes involved in aerobic alkane degradation. Front Microbiol 4:116Google Scholar
  43. Urbano M, Elango V, Pardue JH (2013) Biogeochemical characterization of MC252 oil:sand aggregates on a coastal headland beach. Mar Pollut Bull 77:183–191CrossRefGoogle Scholar
  44. van Beilen JB, Funhoff EG (2007) Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biotechnol 74(1):13–21.  https://doi.org/10.1007/s00253-006-0748-0CrossRefGoogle Scholar
  45. Vázquez DP, Simberloff D (2002) Ecological specialization and susceptibility to disturbance: conjectures and refutations. Am Nat 159:606–623CrossRefGoogle Scholar
  46. Wang W, Shao Z (2014) The long-chain alkane metabolism network of Alcanivorax dieselolei. Nat Commun 5:5755CrossRefGoogle Scholar
  47. Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotechnol 18:257–266CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Joel E. Kostka
    • 1
    Email author
  • Will A. Overholt
    • 1
    • 2
  • Luis M. Rodriguez-R
    • 3
  • Markus Huettel
    • 4
  • Kostas Konstantinidis
    • 3
  1. 1.Georgia Institute of Technology, Schools of Biological and Earth and Atmospheric SciencesAtlantaUSA
  2. 2.Friedrich Schiller University, Institute of BiodiversityJenaGermany
  3. 3.Georgia Institute of Technology, School of Civil and Environmental EngineeringAtlantaUSA
  4. 4.Florida State University, Department of Earth, Ocean and Atmospheric ScienceTallahasseeUSA

Personalised recommendations