The microbial nitrogen cycling potential is impacted by polyaromatic hydrocarbon pollution of marine sediments

Scott, Nicole M.; Hess, Matthias; Bouskill, Nick J.; Mason, Olivia U.; Jansson, Janet K.; Gilbert, Jack A.

doi:10.3389/fmicb.2014.00108

Title: The microbial nitrogen cycling potential is impacted by polyaromatic hydrocarbon pollution of marine sediments

Journal Article · Tue Mar 25 00:00:00 EDT 2014 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2014.00108· OSTI ID:1393979

Scott, Nicole M.; Hess, Matthias; Bouskill, Nick J.; Mason, Olivia U.; Jansson, Janet K.; Gilbert, Jack A.

During hydrocarbon exposure, the composition and functional dynamics of marine microbial communities are altered, favoring bacteria that can utilize this rich carbon source. Initial exposure of high levels of hydrocarbons in aerobic surface sediments can enrich growth of heterotrophic microorganisms having hydrocarbon degradation capacity. As a result, there can be a localized reduction in oxygen potential within the surface layer of marine sediments causing anaerobic zones. We hypothesized that increasing exposure to elevated hydrocarbon concentrations would positively correlate with an increase in denitrification processes and the net accumulation of dinitrogen. This hypothesis was tested by comparing the relative abundance of genes associated with nitrogen metabolism and nitrogen cycling identified in 6 metagenomes from sediments contaminated by polyaromatic hydrocarbons from the Deepwater Horizon (DWH) oil spill in the Gulf of Mexico, and 3 metagenomes from sediments associated with natural oil seeps in the Santa Barbara Channel. An additional 8 metagenomes from uncontaminated sediments from the Gulf of Mexico were analyzed for comparison. We predicted relative changes in metabolite turnover as a function of the differential microbial gene abundances, which showed predicted accumulation of metabolites associated with denitrification processes, including anammox, in the contaminated samples compared to uncontaminated sediments, with the magnitude of this change being positively correlated to the hydrocarbon concentration and exposure duration. These data highlight the potential impact of hydrocarbon inputs on N cycling processes in marine sediments and provide information relevant for system scale models of nitrogen metabolism in affected ecosystems

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE U.S. Department of Energy; Argonne National Laboratory

DOE Contract Number:: AC02-06CH11357

OSTI ID:: 1393979

Journal Information:: Frontiers in Microbiology, Vol. 5; ISSN 1664-302X

Publisher:: Frontiers Research Foundation

Country of Publication:: United States

Language:: English

References (53)

Marine microorganisms make a meal of oil Head, Ian M.; Jones, D. Martin; Röling, Wilfred F. M. Nature Reviews Microbiology, Vol. 4, Issue 3 https://doi.org/10.1038/nrmicro1348	journal	March 2006
Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill Mason, Olivia U.; Hazen, Terry C.; Borglin, Sharon The ISME Journal, Vol. 6, Issue 9 https://doi.org/10.1038/ismej.2012.59	journal	June 2012
Microbial community response to a simulated hydrocarbon spill in mangrove sediments Taketani, Rodrigo Gouvêa; Franco, Natália Oliveira; Rosado, Alexandre Soares The Journal of Microbiology, Vol. 48, Issue 1 https://doi.org/10.1007/s12275-009-0147-1	journal	February 2010
Biodegradation of Diesel Fuel in Soil Under Various Nitrogen Addition Regimes Brook, Timothy R.; Stiver, Warren H.; Zytner, Richard G. Soil and Sediment Contamination: An International Journal, Vol. 10, Issue 5 https://doi.org/10.1080/20015891109428	journal	September 2001
Microbial Nitrogen Cycling Processes in Oxygen Minimum Zones Lam, Phyllis; Kuypers, Marcel M. M. Annual Review of Marine Science, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-marine-120709-142814	journal	January 2011
Deep-sea nutrient loss inferred from the marine dissolved N ₂ /Ar ratio : DENITRIFICATION FROM GLOBAL N Hamme, Roberta C.; Emerson, Steven R. Geophysical Research Letters, Vol. 40, Issue 6 https://doi.org/10.1002/grl.50275	journal	March 2013
Potential roles of anaerobic ammonium and methane oxidation in the nitrogen cycle of wetland ecosystems Zhu, Guibing; Jetten, Mike S. M.; Kuschk, Peter Applied Microbiology and Biotechnology, Vol. 86, Issue 4 https://doi.org/10.1007/s00253-010-2451-4	journal	February 2010
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Langmead, Ben; Trapnell, Cole; Pop, Mihai Genome Biology, Vol. 10, Issue 3 https://doi.org/10.1186/gb-2009-10-3-r25	journal	January 2009
GenBank Benson, Dennis A.; Cavanaugh, Mark; Clark, Karen Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1195	journal	November 2012
Anaerobic ammonium oxidation (anammox) in the marine environment Dalsgaard, Tage; Thamdrup, Bo; Canfield, Donald E. Research in Microbiology, Vol. 156, Issue 4 https://doi.org/10.1016/j.resmic.2005.01.011	journal	May 2005
Microbial gene functions enriched in the Deepwater Horizon deep-sea oil plume Lu, Zhenmei; Deng, Ye; Van Nostrand, Joy D. The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.91	journal	August 2011
The Evolution and Future of Earth’s Nitrogen Cycle Canfield, Donald E.; Glazer, Alexander N.; Falkowski, Paul G. Science, Vol. 330, Issue 6001 https://doi.org/10.1126/science.1186120	journal	October 2010
Predicted Relative Metabolomic Turnover (PRMT): determining metabolic turnover from a coastal marine metagenomic dataset Larsen, Peter E.; Collart, Frank R.; Field, Dawn Microbial Informatics and Experimentation, Vol. 1, Issue 1 https://doi.org/10.1186/2042-5783-1-4	journal	June 2011
The world's most spectacular marine hydrocarbon seeps (Coal Oil Point, Santa Barbara Channel, California): Quantification of emissions Hornafius, J. Scott; Quigley, Derek; Luyendyk, Bruce P. Journal of Geophysical Research: Oceans, Vol. 104, Issue C9 https://doi.org/10.1029/1999JC900148	journal	September 1999
Subsurface Cycling of Nitrogen and Anaerobic Aromatic Hydrocarbon Biodegradation Revealed by Nucleic Acid and Metabolic Biomarkers Yagi, J. M.; Suflita, J. M.; Gieg, L. M. Applied and Environmental Microbiology, Vol. 76, Issue 10 https://doi.org/10.1128/AEM.00172-10	journal	March 2010
Identification of Nitrogen-Incorporating Bacteria in Petroleum-Contaminated Arctic Soils by Using [ ¹⁵ N]DNA-Based Stable Isotope Probing and Pyrosequencing Bell, Terrence H.; Yergeau, Etienne; Martineau, Christine Applied and Environmental Microbiology, Vol. 77, Issue 12 https://doi.org/10.1128/AEM.00172-11	journal	April 2011
Relating Phylogenetic and Functional Diversity among Denitrifiers and Quantifying their Capacity to Predict Community Functioning Salles, Joana Falcão; Le Roux, Xavier; Poly, Franck Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00209	journal	January 2012
KEGG: Kyoto Encyclopedia of Genes and Genomes Ogata, H.; Goto, S.; Sato, K. Nucleic Acids Research, Vol. 27, Issue 1 https://doi.org/10.1093/nar/27.1.29	journal	January 1999
Nitrogen cycling in coastal marine ecosystems Herbert, R. A. FEMS Microbiology Reviews, Vol. 23, Issue 5 https://doi.org/10.1111/j.1574-6976.1999.tb00414.x	journal	October 1999
Anaerobic ammonium oxidation in deep-sea sediments off the Washington margin Engström, Pia; Penton, C. Ryan; Devola, Allan H. Limnology and Oceanography, Vol. 54, Issue 5 https://doi.org/10.4319/lo.2009.54.5.1643	journal	July 2009
Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill Reddy, C. M.; Arey, J. S.; Seewald, J. S. Proceedings of the National Academy of Sciences, Vol. 109, Issue 50 https://doi.org/10.1073/pnas.1101242108	journal	July 2011
Natural seepage of crude oil into the marine environment Kvenvolden, K. A.; Cooper, C. K. Geo-Marine Letters, Vol. 23, Issue 3-4 https://doi.org/10.1007/s00367-003-0135-0	journal	December 2003
Metagenomic analysis of microbial consortium from natural crude oil that seeps into the marine ecosystem offshore Southern California Hawley, Erik R.; Piao, Hailan; Scott, Nicole M. Standards in Genomic Sciences, Vol. 9, Issue 3 https://doi.org/10.4056/sigs.5029016	journal	January 2014
Microbial hydrocarbon degradation-bioremediation of oil spills Atlas, Ronald M. Journal of Chemical Technology & Biotechnology, Vol. 52, Issue 2 https://doi.org/10.1002/jctb.280520202	journal	January 1991
Anaerobic ammonium oxidation by nitrite (anammox): Implications for N2 production in coastal marine sediments Engström, Pia; Dalsgaard, Tage; Hulth, Stefan Geochimica et Cosmochimica Acta, Vol. 69, Issue 8 https://doi.org/10.1016/j.gca.2004.09.032	journal	April 2005
Structure of bacterial communities along a hydrocarbon contamination gradient in a coastal sediment: Bacterial communities along a hydrocarbon gradient PaissÃ©, Sandrine; Coulon, FrÃ©dÃ©ric; GoÃ±i-Urriza, Marisol FEMS Microbiology Ecology, Vol. 66, Issue 2 https://doi.org/10.1111/j.1574-6941.2008.00589.x	journal	November 2008
Hydrocarbon-degrading bacteria enriched by the Deepwater Horizon oil spill identified by cultivation and DNA-SIP Gutierrez, Tony; Singleton, David R.; Berry, David The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.98	journal	June 2013
Petroleum nitrogen compounds and oxygen compounds Snyder, Lloyd Robert Accounts of Chemical Research, Vol. 3, Issue 9 https://doi.org/10.1021/ar50033a002	journal	September 1970
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes Meyer, F.; Paarmann, D.; D'Souza, M. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-386	journal	September 2008
Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill: Enrichment of oil degraders from Gulf of Mexico Baelum, Jacob; Borglin, Sharon; Chakraborty, Romy Environmental Microbiology, Vol. 14, Issue 9 https://doi.org/10.1111/j.1462-2920.2012.02780.x	journal	May 2012
Comparative phylogenetic analysis of microbial communities in pristine and hydrocarbon-contaminated Alpine soils: Microbial community phylogeny in Alpine soil LabbÃ©, Diane; Margesin, Rosa; Schinner, Franz FEMS Microbiology Ecology, Vol. 59, Issue 2 https://doi.org/10.1111/j.1574-6941.2006.00250.x	journal	February 2007
New Developments in the Marine Nitrogen Cycle Brandes, Jay A.; Devol, Allan H.; Deutsch, Curtis Chemical Reviews, Vol. 107, Issue 2 https://doi.org/10.1021/cr050377t	journal	February 2007
Oxygen Sensitivity of Anammox and Coupled N-Cycle Processes in Oxygen Minimum Zones Kalvelage, Tim; Jensen, Marlene M.; Contreras, Sergio PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0029299	journal	December 2011
Study of nitrogen fixation in microbial communities of oil-contaminated marine sediment microcosms Musat, Florin; Harder, Jens; Widdel, Friedrich Environmental Microbiology, Vol. 8, Issue 10 https://doi.org/10.1111/j.1462-2920.2006.01069.x	journal	October 2006
Deep-Sea Oil Plume Enriches Indigenous Oil-Degrading Bacteria Hazen, Terry C.; Dubinsky, Eric A.; DeSantis, Todd Z. Science, Vol. 330, Issue 6001 https://doi.org/10.1126/science.1195979	journal	August 2010
Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill Mason, Olivia U.; Scott, Nicole M.; Gonzalez, Antonio The ISME Journal, Vol. 8, Issue 7 https://doi.org/10.1038/ismej.2013.254	journal	January 2014
New Developments in the Marine Nitrogen Cycle Brandes, Jay A.; Devol, Allan H.; Deutsch, Curtis ChemInform, Vol. 38, Issue 20 https://doi.org/10.1002/chin.200720269	journal	May 2007
Spatiotemporal persistence of multiple, diverse clades and toxins of Corynebacterium diphtheriae Will, Robert C.; Ramamurthy, Thandavarayan; Sharma, Naresh Chand Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21870-5	journal	March 2021
SPOCD1 is an essential executor of piRNA-directed de novo DNA methylation Zoch, Ansgar; Auchynnikava, Tania; Berrens, Rebecca V. Nature, Vol. 584, Issue 7822 https://doi.org/10.1038/s41586-020-2557-5	journal	July 2020
Hydrocarbon-degrading bacteria enriched by the Deepwater Horizon oil spill identified by cultivation and DNA-SIP David, Berry,; D., Aitken, Michael; Tony, Gutierrez, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/4p5s-2q50	text	January 2013
SEED annotated Metagenome data generated from 14 benthic sediment samples taken from the Northern Gulf of Mexico, September to October 2010 Scott, Nicole Harte Research Institute https://doi.org/10.7266/n7d21vmm	dataset	January 2015
16S microbial data generated from sediment and water column samples collected from May 2010 to June 2012 Jack, Scott, Nicole and Gilbert, Harte Research Institute https://doi.org/10.7266/n7ht2m9k	dataset	January 2015
Bioturbation: impact on the marine nitrogen cycle Laverock, Bonnie; Gilbert, Jack A.; Tait, Karen Biochemical Society Transactions, Vol. 39, Issue 1 https://doi.org/10.1042/bst0390315	journal	January 2011
Effects of Heavy Fuel Oil on the Bacterial Community Structure of a Pristine Microbial Mat Bordenave, S.; Goni-Urriza, M. S.; Caumette, P. Applied and Environmental Microbiology, Vol. 73, Issue 19 https://doi.org/10.1128/aem.01352-07	journal	August 2007
Stark Contrast in Denitrification and Anammox across the Deep Norwegian Trench in the Skagerrak Trimmer, Mark; Engström, Pia; Thamdrup, Bo Applied and Environmental Microbiology, Vol. 79, Issue 23 https://doi.org/10.1128/aem.01970-13	journal	September 2013
Changes in Benthic Denitrification, Nitrate Ammonification, and Anammox Process Rates and Nitrate and Nitrite Reductase Gene Abundances along an Estuarine Nutrient Gradient (the Colne Estuary, United Kingdom) Dong, L. F.; Smith, C. J.; Papaspyrou, S. Applied and Environmental Microbiology, Vol. 75, Issue 10 https://doi.org/10.1128/aem.02511-08	journal	March 2009
Free-Living Dinitrogen-Fixing Bacteria Isolated from Petroleum Refinery Oily Sludge Laguerre, Gisele; Bossand, Bernard; Bardin, Rene Applied and Environmental Microbiology, Vol. 53, Issue 7 https://doi.org/10.1128/aem.53.7.1674-1678.1987	journal	January 1987
Nitrification and Autotrophic Nitrifying Bacteria in a Hydrocarbon-Polluted Soil Deni, Jamal; Penninckx, Michel J. Applied and Environmental Microbiology, Vol. 65, Issue 9 https://doi.org/10.1128/aem.65.9.4008-4013.1999	journal	September 1999
Free-Living Heterotrophic Nitrogen-Fixing Bacteria Isolated from Fuel-Contaminated Antarctic Soils Eckford, R.; Cook, F. D.; Saul, D. Applied and Environmental Microbiology, Vol. 68, Issue 10 https://doi.org/10.1128/aem.68.10.5181-5185.2002	journal	October 2002
Robust Hydrocarbon Degradation and Dynamics of Bacterial Communities during Nutrient-Enhanced Oil Spill Bioremediation Roling, W. F. M.; Milner, M. G.; Jones, D. M. Applied and Environmental Microbiology, Vol. 68, Issue 11 https://doi.org/10.1128/aem.68.11.5537-5548.2002	journal	November 2002
Production of N2 through Anaerobic Ammonium Oxidation Coupled to Nitrate Reduction in Marine Sediments Thamdrup, B.; Dalsgaard, T. Applied and Environmental Microbiology, Vol. 68, Issue 3 https://doi.org/10.1128/aem.68.3.1312-1318.2002	journal	March 2002
Bacterial Community Dynamics and Hydrocarbon Degradation during a Field-Scale Evaluation of Bioremediation on a Mudflat Beach Contaminated with Buried Oil Roling, W. F. M.; Milner, M. G.; Jones, D. M. Applied and Environmental Microbiology, Vol. 70, Issue 5 https://doi.org/10.1128/aem.70.5.2603-2613.2004	journal	May 2004
The chemistry of nitrosative stress induced by nitric oxide and reactive nitrogen oxide species. Putting perspective on stressful biological situations Ridnour, L. A.; Thomas, D. D.; Mancardi, D. Biological Chemistry, Vol. 385, Issue 1 https://doi.org/10.1515/bc.2004.001	journal	January 2004

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