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

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Scenarios and Responses to Future Deep Oil Spills

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.

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References

  • American Academy of Microbiology (2011) FAQ: microbes & oil spills. http://www.asmscience.org/content/report/faq?order=date

  • Atlas RM (1995) Petroleum biodegradation and oil spill bioremediation. Mar Pollut Bull 31:178–182

    Article  CAS  Google Scholar 

  • 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/es2013227

    Article  CAS  Google Scholar 

  • 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 7:2056

    Article  Google Scholar 

  • 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):9496–9505

    Article  CAS  Google Scholar 

  • 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):e0132341

    Article  Google Scholar 

  • 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 26:266–267

    Article  CAS  Google Scholar 

  • 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):200–209

    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 

  • 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):1073–1083

    Article  CAS  Google Scholar 

  • 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):542

    Article  Google Scholar 

  • Hayworth JS, Clement TP (2011) BP's operation deep clean-could dilution be the solution to beach pollution? Environ Sci Technol 45:4201–4202

    Article  CAS  Google Scholar 

  • Head IM, Jones DM, Roling WFM (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4:173–182

    Article  CAS  Google Scholar 

  • Huettel M, Berg P, Kostka JE (2014) Benthic exchange and biogeochemical cycling in permeable sediments. Annu Rev Mar Sci 6(1):23–51

    Article  Google Scholar 

  • 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 126:488–500

    Article  CAS  Google Scholar 

  • 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):5689–5701

    Article  CAS  Google Scholar 

  • 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):136–149

    Article  Google Scholar 

  • 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 7:377–401

    Article  CAS  Google Scholar 

  • 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.05402-11

    Article  CAS  Google Scholar 

  • 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 5:130

    Article  Google Scholar 

  • Leahy JG, Colwell RR (1990) Microbial-degradation of hydrocarbons in the environment. Microbiol Rev 54:305–315

    CAS  Google Scholar 

  • 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):13591–13596

    Article  CAS  Google Scholar 

  • 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 241

    Google Scholar 

  • 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):20212–20221

    Article  CAS  Google Scholar 

  • 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):20222–20228

    Article  CAS  Google Scholar 

  • 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):e65087

    Article  CAS  Google Scholar 

  • 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):4440–4453

    Article  CAS  Google Scholar 

  • 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:e74265

    Article  CAS  Google Scholar 

  • 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. USCG

    Google Scholar 

  • 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.01015-13

    Article  Google Scholar 

  • 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):518–527

    Article  CAS  Google Scholar 

  • 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 36:996–1004

    Article  CAS  Google Scholar 

  • 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):035301

    Article  Google Scholar 

  • Prince RC (2010) Bioremediation of marine oil spills. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin Heidelberg, pp 2618–2626

    Google Scholar 

  • Prosser JI (2012) Ecosystem processes and interactions in a morass of diversity. FEMS Microbiol Ecol 81(3):507–519

    Article  CAS  Google Scholar 

  • 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):384

    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 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):20229–20234

    Article  CAS  Google Scholar 

  • 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 9:1928–1940

    Article  Google Scholar 

  • 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.00072-06

    Article  CAS  Google Scholar 

  • 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.x

    Article  CAS  Google Scholar 

  • 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/nbt1232

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Urbano M, Elango V, Pardue JH (2013) Biogeochemical characterization of MC252 oil:sand aggregates on a coastal headland beach. Mar Pollut Bull 77:183–191

    Article  CAS  Google Scholar 

  • 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/s00253-006-0748-0

    Article  CAS  Google Scholar 

  • Vázquez DP, Simberloff D (2002) Ecological specialization and susceptibility to disturbance: conjectures and refutations. Am Nat 159:606–623

    Article  Google Scholar 

  • Wang W, Shao Z (2014) The long-chain alkane metabolism network of Alcanivorax dieselolei. Nat Commun 5:5755

    Article  CAS  Google Scholar 

  • Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotechnol 18:257–266

    Article  CAS  Google Scholar 

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Funding

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).

Author information

Authors and Affiliations

  1. Georgia Institute of Technology, Schools of Biological and Earth and Atmospheric Sciences, Atlanta, GA, USA

    Joel E. Kostka & Will A. Overholt

  2. Friedrich Schiller University, Institute of Biodiversity, Jena, Germany

    Will A. Overholt

  3. Georgia Institute of Technology, School of Civil and Environmental Engineering, Atlanta, GA, USA

    Luis M. Rodriguez-R & Kostas Konstantinidis

  4. Florida State University, Department of Earth, Ocean and Atmospheric Science, Tallahassee, FL, USA

    Markus Huettel

Authors
  1. Joel E. Kostka
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  2. Will A. Overholt
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  3. Luis M. Rodriguez-R
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  4. Markus Huettel
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  5. Kostas Konstantinidis
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Corresponding author

Correspondence to Joel E. Kostka .

Editor information

Editors and Affiliations

  1. College of Marine Science, University of South Florida, St. Petersburg, FL, USA

    Steven A. Murawski

  2. College of Marine Science, University of South Florida, St. Petersburg, FL, USA

    Cameron H. Ainsworth

  3. College of Marine Science, University of South Florida, St. Petersburg, FL, USA

    Sherryl Gilbert

  4. College of Marine Science, University of South Florida, St. Petersburg, FL, USA

    David J. Hollander

  5. Rosenstiel School of Marine & Atmospheric Science, University of Miami, Miami, FL, USA

    Claire B. Paris

  6. Hamburg University of Technology, Hamburg, Germany

    Michael Schlüter

  7. Mote Marine Laboratory, Sarasota, FL, USA

    Dana L. Wetzel

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Kostka, J.E., Overholt, W.A., Rodriguez-R, L.M., Huettel, M., Konstantinidis, K. (2020). Toward a Predictive Understanding of the Benthic Microbial Community Response to Oiling on the Northern Gulf of Mexico Coast. In: Murawski, S., et al. Scenarios and Responses to Future Deep Oil Spills. Springer, Cham. https://doi.org/10.1007/978-3-030-12963-7_11

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