Abstract
Anthropogenic nutrient inputs fuel eutrophication and hypoxia ([O2] < 2 mg L−1), threatening coastal and near shore environments across the globe. The world’s second largest anthropogenic coastal hypoxic zone occurs annually along the Louisiana (LA) shelf. Springtime loading of dissolved inorganic nitrogen (DIN) from the Mississippi River, combined with summertime stratification and increased water residence time on the shelf, promotes establishment of an extensive hypoxic zone that persists throughout the summer. We investigated the patterns of pelagic denitrification and methane (CH4) oxidation along the LA shelf. Microbial activity rates were determined along with concentrations of dissolved nutrients and greenhouse gases, nitrous oxide (N2O) and CH4, during summer in 2013, 2015, and 2016. We documented denitrification rates up to 1900 nmol N L−1 d−1 and CH4 oxidation rates as high as 192 nmol L−1 d−1 in hypoxic waters characterized by high concentrations of N2O (range: 1 to 102 nM) and CH4 (range: 3 to 641 nM). Ecosystem scaling estimates suggest that pelagic denitrification could remove between 0.1 and 47% of the DIN input from the Mississippi River, whereas CH4 oxidation does not function as an effective removal process with CH4 escaping to the atmosphere. Denitrification and CH4 oxidizing bacteria within the LA shelf hypoxic zone were largely unable to keep up with the DIN and CH4 inputs to the water column. Rates were variable and physiochemical dynamics appeared to regulate the microbial removal capacity for both nitrate/nitrite and CH4 in this ecosystem.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abril G, Iversen N (2002) Methane dynamics in a shallow non-tidal estuary (Randers Fjord, Denmark). Mar Ecol Prog Ser 203:171–181. https://doi.org/10.3354/meps230171
Alexander RB, Smith RA, Schwarz GE, Boyer EW, Nolan JY (2008) Differences in phosphorus and nitrogen delivery to the Gulf of Mexico from the Mississippi River basin. Environ Sci Technol 42:822–830. https://doi.org/10.1021/es0716103
An S, Gardner WS, Kana T (2001) Simultaneous measurement of denitrification and nitrogen fixation using isotope pairing with Membrane Inlet Mass Spectrometry analysis. Appl Environ Microbiol 67:1171–1178. https://doi.org/10.1128/AEM.67.3.1171
Babbin AR, Keil RG, Devol AH, Ward BB (2014) Organic matter stoichiometry, flux, and oxygen control nitrogen loss in the ocean. Science 344:406–408
Babbin AR, Bianchi D, Jayakumar A, Ward BB (2015) Rapid nitrous oxide cycling in the suboxic ocean. Science 348:1127–1129. https://doi.org/10.1126/science.aaa8380
Bange HW (2006) Nitrous oxide and methane in European coastal waters. Estuar Coast Shelf Sci 70:361–374. https://doi.org/10.1016/j.ecss.2006.05.042
Bange HW, Bergmann K, Hansen HP, Kock A, Koppe R, Malien F, Ostrau C (2010) Dissolved methane during hypoxic events at the Boknis Eck time series station (Eckernförde Bay, SW Baltic Sea). Biogeosci Discuss 6:11463–11477. https://doi.org/10.5194/bgd-6-11463-2009
Berg C, Vandieken V, Thamdrup B, Jürgens K (2015) Significance of archaeal nitrification in hypoxic waters of the Baltic Sea. ISME J 9:1319–1332. https://doi.org/10.1038/ismej.2014.218
Bernard BB, Brooks JM, Sackett WM (1976) Natural gas seepage in the Gulf of Mexico. Earth Planet Sci Lett 31:48–54
Bianchi TS, DiMarco SF, Cowan JH Jr, Hetland RD, Chapman P, Day JW, Allison MA (2010) The science of hypoxia in the Northern Gulf of Mexico: a review. Science Tot Environ 408:1471–1484
Braman RS, Hendrix SA (1989) Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium(III) reduction with chemiluminescence detection. Anal Chem 61:2715–2718. https://doi.org/10.1021/ac00199a007
Breitburg D, Levin LA, Oschlies A, Grégoire M, Chavez FP, Conley DJ, Garcon V, Gilbert D, Gutierrez D, Isensee K, Jacinto GS, Limburg KE, Montes I, Naqvi SWA, Pitcher GC, Rabalais NN, Roman MR, Rose KA, Seibel BA, Telszewski M, Yasuhara M, Zhang J (2018) Declining oxygen in the global ocean and coastal waters. Science. https://doi.org/10.1126/science.aam7240
Bristow LA, Sarode N, Cartee J, Caro-Quintero A, Thamdrup B, Stewart FJ (2015) Biogeochemical and metagenomic analysis of nitrite accumulation in the Gulf of Mexico hypoxic zone. Limnol Oceanogr 60:1733–1750. https://doi.org/10.1002/lno.10130
Brooks JM, Reid DF, Bernard BB (1981) Methane in the upper water column of the northwestern Gulf of Mexico. J Geophys Res Oceans 86:11029–11040
Bugna GC, Chanton JP, Cable JE, Burnett WC, Cable PH (1996) The importance of groundwater discharge to the methane budgets of nearshore and continental shelf waters of the northeastern Gulf of Mexico. Geochim Cosmochim Acta 60:4735–4746
Bulow SE, Rich JJ, Naik HS, Pratihary AK, Ward BB (2010) Denitrification exceeds anammox as a nitrogen loss pathway in the Arabian Sea oxygen minimum zone. Deep Sea Res Part I Oceanogr Res Pap 57:384–393. https://doi.org/10.1016/j.dsr.2009.10.014
Bussmann I, Matousu A, Osudar R, Mau S (2015) Assessment of the radio 3H-CH4 tracer technique to measure aerobic methane oxidation in the water column. Limnol Oceanogr Methods 13:312–327. https://doi.org/10.1002/lom3.10027
Carini S, Bano N, LeCleir G, Joye SB (2005) Aerobic methane oxidation and methanotroph community composition during seasonal stratification in Mono Lake, California (USA). Environ Microbiol 7:1127–1138. https://doi.org/10.1111/j.1462-2920.2005.00786.x
Carini P, White AE, Campbell EO, Giovannoni SJ (2014) Methane production by phosphate-starved SAR11 chemoheterotrophic marine bacteria. Nat Comm 5:4346. https://doi.org/10.1038/ncomms5346
Chang BX, Rich JR, Jayakumar A, Naik H, Pratihary AK, Keil RG, Ward BB, Devol AH (2014) The effect of organic carbon on fixed nitrogen loss in the eastern tropical South Pacific and Arabian Sea oxygen deficient zones. Limnol Oceanogr 59(4):1267–1274. https://doi.org/10.4319/lo.2014.59.4.1267
Chistoserdova L, Kalyuzhnaya MG (2018) Current trends in methylotrophy. Trends Microbiol 26(8):703–714
Chronopoulou PM, Shelley F, Pritchard WJ, Maanoja ST, Trimmer M (2017) Origin and fate of methane in the Eastern Tropical North Pacific oxygen minimum zone. ISME J 11:1386–1399. https://doi.org/10.1038/ismej.2017.6
Cicerone RJ, Oremland RS (1988) Biogeochemical aspects of atmospheric methane. Global Biogeochem Cycles 2:299–327. https://doi.org/10.1029/GB002i004p00299
Cline JD (1969) Spectrophotometric Determination of Hydrogen Sulfide. Limnol Oceanogr 14:454–458. https://doi.org/10.4319/lo.1969.14.3.0454
Codispoti LA, Packard TT (1980) Denitrification rates in the eastern tropical South Pacific. J Mar Res 38:3
Crespo-Medina M, Meile CD, Hunter KS, Diercks AR, Asper VL, Orphan VJ, Tavormina PL, Nigro LM, Battles JJ, Chanton JP, Shiller AM, Joung DJ, Amon RMW, Bracco A, Montoya JP, Villareal TA, Wood AM, Joye SB (2014) The rise and fall of methanotrophy following a deepwater oil-well blowout. Nat Geosci 7:423–427. https://doi.org/10.1038/ngeo2156
Crevecoeur S, Vincent WF, Comte J, Matveev A, Lovejoy C (2017) Diversity and potential activity of methanotrophs in high methane-emitting permafrost thaw ponds. PLoS ONE 12:e0188223. https://doi.org/10.1371/journal.pone.0188223
Crutzen PJ (1970) The influence of nitrogen oxides on the atmospheric ozone content. Quart J R Met Soc 96:320–325. https://doi.org/10.1002/qj.49709640815
Dalsgaard T, Thamdrup B (2002) Factors Controlling Anaerobic Ammonium Oxidation with Nitrite in Marine Sediments. Appl Environ Microbiol 68:3802–3808. https://doi.org/10.1128/AEM.68.8.3802-3808.2002
Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156:457–464. https://doi.org/10.1016/j.resmic.2005.01.011
Dalsgaard T, Thamdrup B, Farías L, Revsbech NP (2012) Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific. Limnol Oceanogr 57:1331–1346. https://doi.org/10.4319/lo.2012.57.5.1331
Dalsgaard T, Stewart FJ, Thamdrup B, De Brabandere L, Revsbech NP, Ulloa O, Canfield DC, Delong EF (2014) Oxygen at nanomolar levels reversibly suppresses process rates and gene expression in anammox and denitrification in the oxygen minimum zone off Northern Chile. mBio 5:1–14. https://doi.org/10.1128/mBio.01966-14
De Brabandere L, Thamdrup B, Revsbech NP, Foadi R (2012) A critical assessment of the occurrence and extend of oxygen contamination during anaerobic incubations utilizing commercially available vials. J Microbiol Methods 88:147–154. https://doi.org/10.1016/j.mimet.2011.11.001
Deutsch C, Brix H, Ito T, Frenzel H, Thompson L (2011) Climate-forced variability of ocean hypoxia. Science 333:336–340
Devol AH, Uhlenhopp AG, Naqvi SWA, Brandes JA, Jayakumar DA, Naik H, Gaurin S, Codispoti LA, Yoshinari T (2006) Denitrification rates and excess nitrogen gas concentrations in the Arabian Sea oxygen deficient zone. Deep Sea Res Part I Oceanogr Res Pap 53:1533–1547. https://doi.org/10.1016/j.dsr.2006.07.005
Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929. https://doi.org/10.1126/science.1156401
Dinnel SP, Wiseman WJ (1986) Fresh water on the Louisiana and Texas shelf. Cont Shelf Res 6:765–784. https://doi.org/10.1016/0278-4343(86)90036-1
Dugdale R (1967) Nutrient limitation in the sea: dynamics, identification, and significance. Limnol Oceanogr 12:685–695
Engel A, Galgani L (2015) The organic sea surface microlayer in the upwelling region off Peru and implications for air–sea exchange processes. Biogeosciences 13:989–1007. https://doi.org/10.5194/bg-13-989-2016
Ettwig KF, Butler MK, Le Paslier D et al (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548. https://doi.org/10.1038/nature08883
Galán A, Thamdrup B, Saldías GS, Farías L (2017) Vertical segregation among pathways mediating nitrogen loss (N2 and N2O production) across the oxygen gradient in a coastal upwelling ecosystem. Biogeosci 14:4795–4813. https://doi.org/10.5194/bg-14-4795-2017
Galloway JN, Schlesinger WH, Levy H, Michaels A, Schnoor JL (1995) Nitrogen fixation: anthropogenic enhancement-environmental response. Global Biogeochem Cycles 9:235–252. https://doi.org/10.1029/95GB00158
Ganesh S, Bristow LA, Larsen M, Sarode N, Thamdrup B, Stewart FJ (2015) Size-fraction partitioning of community gene transcription and nitrogen metabolism in a marine oxygen minimum zone. ISME J 9:2682–2696. https://doi.org/10.1038/ismej.2015.44
Gelesh L, Marshall K, Boicourt W, Lapham L (2016) Methane concentrations increase in bottom waters during summertime anoxia in the highly eutrophic estuary, Chesapeake Bay, U.S.A. Limnol Oceanogr 61:S253–S266. https://doi.org/10.1002/lno.10272
Gillies LE, Thrash JC, deRada S, Rabalais NN, Mason OU (2015) Archaeal enrichment in the hypoxic zone in the northern Gulf of Mexico. Environ Microbiol 17:3847–3856. https://doi.org/10.1111/1462-2920.12853
Gillies LE, Thrash JC, Rabalais NN, Mason OU (2019) Extent of the annual Gulf of Mexico hypoxic zone influences microbial community structure. PLoS ONE 14:e0209055. https://doi.org/10.1371/journal.pone.0209055
Glass JB, Kretz CB, Ganesh S, Ranjan P, Seston SL, Buck KN, Landing WM, Morton PL, Moffett JW, Giovannoni SJ, Vergin KL, Stewart FJ (2015) Meta-omic signatures of microbial metal and nitrogen cycling in marine oxygen minimum zones. Front Microbiol 6:998. https://doi.org/10.3389/fmicb.2015.00998
Goreau TJ, Kaplan WA, Wofsy SC, McElroy MB, Valois FW, Watson SW (1980) Production of NO2- and N2O by nitrifying bacteria at reduced concentrations of oxygen. Appl Environ Microbiol 40(3):526–532
Grasshoff K, Ehrhardt M, Kremling K, Almgren T (1983) Methods of Seawater Analysis, 2nd rev. and extended ed. Verlag Chemie.
Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471
Heintz MB, Mau S, Valentine DL (2012) Physical control on methanotrophic potential in waters of the Santa Monica Basin, Southern California. Limnol Oceanogr 57:420–432. https://doi.org/10.4319/lo.2012.57.2.0420
Hietanen S, Jäntti H, Buizert C, Jürgens K, Labrenz M, Voss M, Kuparinen J (2012) Hypoxia and nitrogen processing in the Baltic Sea water column. Limnol Oceanogr 57:325–337. https://doi.org/10.4319/lo.2012.57.1.0325325
IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge; New York, NY: Cambridge University Press.
Jensen MM, Petersen J, Dalsgaard T, Thamdrup B (2009) Pathways, rates, and regulation of N2 production in the chemocline of an anoxic basin, Mariager Fjord, Denmark. Mar Chem 113:102–113. https://doi.org/10.1016/j.marchem.2009.01.002
Joye SB, Anderson IC (2008) Nitrogen cycling in coastal sediments. Nitrogen in the marine environment, In: Bronk DA, Capone D, Carpenter, E (Eds), 2nd Edition, Academic Press, pp. 868–915.
Joye SB, Hollibaugh JT (1995) Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments. Science 270:623–625. https://doi.org/10.1126/science.270.5236.623
Joye SB, Smith SV, Hollibaugh JT, Paerl HW (1996) Estimating denitrification rates in estuarine sediments: a comparison of stoichiometric and acetylene based. Biogeochemistry 33:197–215
Justić D, Wang L (2014) Assessing temporal and spatial variability of hypoxia over the inner Louisiana–upper Texas shelf: Application of an unstructured-grid three-dimensional coupled hydrodynamic-water quality model. Cont Shelf Res 72:163–179
Justić D, Rabalais NN, Turner RE (1996) Effects of climate change on hypoxia in coastal waters: a doubled CO 2 scenario for the northern Gulf of Mexico. Limnol Oceanogr 41:992–1003. https://doi.org/10.4319/lo.1996.41.5.0992
Kalvelage T, Lavik G, Lam P et al (2013) Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone. Nat Geosci 6:228–234
Kana TM, Darkangelo C, Hunt MD, Oldham JB, Bennett GE, Cornwell JC (1994) Membrane Inlet Mass Spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Anal Chem 66:4166–4170. https://doi.org/10.1021/ac00095a009
Karl DM, Beversdorf L, Björkman KM, Church MJ, Martinez A, Delong EF (2008) Aerobic production of methane in the sea. Nat Geosci 1(7):473–478. https://doi.org/10.1038/ngeo234
Kelley C (2003) Methane oxidation potential in the water column of two diverse coastal marine sites. Biogeochemistry 65:105–120. https://doi.org/10.1023/A:1026014008478
Kits KD, Klotz MG, Stein LY (2015) Methane oxidation coupled to nitrate reduction under hypoxia by the Gammaproteobacterium Methylomonas denitrificans, sp. nov. type strain FJG1. Environ Microbiol 17:3219–3232. https://doi.org/10.1111/1462-2920.12772
Kitzinger K, Marchant HK, Bristow LA, Herbold CW, Padilla CC, Kidane AT, Littmann S, Daims H, Pjevac P, Stewart FJ, Wagner M, Kuypers MMM (2020) Single cell analyses reveal contrasting life strategies of the two main nitrifiers in the ocean. Nat Commun 11:767. https://doi.org/10.1038/s41467-020-14542-3
Klawonn I, Bonaglia S, Brüchert V, Ploug H (2015) Aerobic and anaerobic nitrogen transformation processes in N2-fixing cyanobacterial aggregates. ISME J 9:1456–1466. https://doi.org/10.1038/ismej.2014.232
Knowles R (1982) Denitrification. Microbiol Rev 46:43–70. https://doi.org/10.1128/CMR.5.4.356.Updated
Kojima H, Tokizawa R, Kogure K et al (2014) Community structure of planktonic methane-oxidizing bacteria in a subtropical reservoir characterized by dominance of phylotype closely related to nitrite reducer. Sci Rep 4:1–7. https://doi.org/10.1038/srep05728
Kolpin DW (2000) Importance of the Mississippi River Basin for investigating agricultural–chemical contamination of the hydrologic cycle. Science Tot Environ 248:71–72
Kowalczuk P, Zablocka M, Sagan S, Kulinski K (2010) Fluorescence measured in situ as a proxy of CDOM absorption and DOC concentration in the Baltic Sea. Oceanologia 52:431–471. https://doi.org/10.5697/oc.52-3.431
Kozlowski JA, Stieglmeier M, Schleper C, Klotz MG, Stein LY (2016) Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota. ISME J 10:1836–1845. https://doi.org/10.1038/ismej.2016.2
Lammers S, Suess E (1994) An improved head-space analysis method for CH4 in seawater. Mar Chem 47:115–125. https://doi.org/10.1016/0304-4203(94)90103-1
Lelieveld J, Crutzen PJ, Brühl C (1993) Climate effects of atmospheric methane. Chemosphere 26:739–768. https://doi.org/10.1016/0045-6535(93)90458-H
Levin LA (2018) Manifestation, drivers, and emergence of open ocean deoxygenation. Ann Rev Mar Sci 10:229–260
Loginova AN, Thomsen S, Engel A (2016) Chromophoric and fluorescent dissolved organic matter in and above the oxygen minimum zone off Peru. J Geophys Res Oceans 121:7973–7990. https://doi.org/10.1002/2016JC011906
Lohrenz SE, Fahnenstiel GL, Redalje DG, Lang GA, Dagg MJ, Whitledge TE, Dortch Q (1999) Nutrients, irradiance, and mixing as factors regulating primary production in coastal waters impacted by the Mississippi River plume. Cont Shelf Res 19:1113–1141. https://doi.org/10.1016/S0278-4343(99)00012-6
Löscher CR, Kock A, Könneke M, LaRoche J, Bange HW, Schmitz RA (2012) Production of oceanic nitrous oxide by ammonia oxidizing archaea. Biogeosci 9(7):2419–2429. https://doi.org/10.5194/bg-9-2419-2012
Magen C, Lapham LL, Pohlman JW, Marshall K, Bosman S, Casso M, Chanton JP (2014) A simple headspace equilibration method for measuring dissolved methane. Limnol Oceanogr Meth 12:637–650. https://doi.org/10.4319/lom.2014.12.637
Marty D, Bonin P, Michotey V, Bianchi M (2001) Bacterial biogas production in coastal systems affected by freshwater inputs. Cont Shelf Res 21:2105–2115
Mau S, Blees J, Helmke E, Niemann H, Damm E (2013) Vertical distribution of methane oxidation and methanotrophic response to elevated methane concentrations in stratified waters of the Arctic fjord Storfjorden (Svalbard, Norway). Biogeosci 10:6267–6268. https://doi.org/10.5194/bg-10-6267-2013
Mayer LM, Schick LL, Allison MA (2008) Input of nutritionally rich organic matter from the mississippi river to the Louisiana Coastal Zone. Estuaries Coast 13:1052–1062. https://doi.org/10.1007/s12237-008-9080-5
McCarthy MJ, Newell SE, Carini SA, Gardner WS (2015) Denitrification dominates sediment nitrogen removal and is enhanced by bottom-water hypoxia in the northern Gulf of Mexico. Estuaries Coasts 38:2279–2294
Meade RH (1995) Contaminants in the Mississippi River, 1987–1992. U.S. Geological Survey Circular 1133, U.S. Department of the Interior, U.S. Geological Survey, Denver, Colorado.
Milliman JD, Meade RH (1983) World-wide delivery of river sediment to the oceans. J Geol 91:1–21
Munoz SE, Dee SG (2017) El Niño increases the risk of lower Mississippi River flooding. Sci Rep 7:1772. https://doi.org/10.1038/s41598-017-01919-6
Naqvi SWA, Lam P, Narvenkar G et al (2018) Methane stimulates massive nitrogen loss from freshwater reservoirs in India. Nat Commun 9:1265. https://doi.org/10.1038/s41467-018-03607-z
National Water Information System (NWIS). Department of the Interior; U.S. Geological Survey; National Streamflow Information Program and National Water-Quality Assessment Project. Baton Rouge, LA. https://waterdata.usgs.gov/usa/nwis/uv?site_no=07374000. Accessed 21 September 2017
Nixon SW (1995) Coastal marine eutrophication: A definition, social causes, and future concerns. Ophelia 41(1):199–219. https://doi.org/10.1080/00785236.1995.10422044
Osudar R, Matoušů A, Alawi M, Wagner D, Bussmann I (2015) Environmental factors affecting methane distribution and bacterial methane oxidation in the German Bight (North Sea). Estuar Coast Shelf Sci 160:10–21. https://doi.org/10.1016/j.ecss.2015.03.028
Padilla CC, Bristow LA, Sarode N et al (2016) NC10 bacteria in marine oxygen minimum zones. ISME J 10:2067–2071. https://doi.org/10.1038/ismej.2015.262
Padilla CC, Bertagnolli AD, Bristow LA, Sarode N, Glass JB, Thamdrup B, Stewart FJ (2017) Metagenomic binning recovers a transcriptionally active Gammaproteobacterium linking methanotrophy to partial denitrification in an anoxic oxygen minimum zone. Front Mar Sci 4:1–15. https://doi.org/10.3389/fmars.2017.00023
Pakulski JD, Benner R, Whitledge T et al (2000) Microbial metabolism and nutrient cycling in the Mississippi and Atchafalaya River plumes. Estuar Coast Shelf Sci 50:173–184. https://doi.org/10.1006/ecss.1999.0561
Patureau D, Zumstein E, Delgenes JP, Moletta R (2000) Aerobic denitrifiers isolated from diverse natural and managed ecosystems. Microb Ecol 39:145–152. https://doi.org/10.1007/s002480000009
Porubsky WP, Velasquez LE, Joye SB (2008) Nutrient-replete benthic microalgae as a source of dissolved organic carbon to coastal waters. Estuaries Coasts 31:860–876
Quigg A, Sylvan JB, Gustafson AB, Fisher TR, Oliver RL, Tozzi S, Ammerman JW (2011) Going west: Nutrient limitation of primary production in the northern Gulf of Mexico and the importance of the Atchafalaya River. Aquat Geochem 17:519–544. https://doi.org/10.1007/s10498-011-9134-3
Rabalais NN, Turner RE (2013) Bottom Water Dissolved Oxygen – 2013 Size of bottom-water hypoxia in mid-summer. https://gulfhypoxia.net/research/shelfwide-cruise/?y=2013&p=press_release Accessed 13 August 2018
Rabalais N, Turner RE (2015) Bottom Water Dissolved Oxygen – 2015 Size of bottom-water hypoxia in mid-summer. https://gulfhypoxia.net/research/shelfwide-cruise/?y=2016&p=hypoxia_fc Accessed 13 August 2018
Rabalais NN, Wiseman WJ, Turner RE (1994) Comparison of continuous records of near-bottom dissolved oxygen from the hypoxia zone along the Louisiana coast. Estuaries 17:850–861. https://doi.org/10.2307/1352753
Rabalais NN, Turner RE, Justić D, Dortch Q, Wiseman WJ, Sen Gupta BK (1996) Nutrient changes in the Mississippi River and system responses on the adjacent continental shelf. Estuaries 19:386–407. https://doi.org/10.2307/1352458
Rabalais NN, Turner RE, Wiseman WJ (2001) Hypoxia in the Gulf of Mexico. J Environ Qual 30:320–329. https://doi.org/10.2134/jeq2001.302320x
Rabalais NN, Turner RE, Wiseman WJ (2002) Gulf of Mexico Hypoxia, A.K.A. “The Dead Zone.” Annu Rev Ecol Syst 33:235–263. https://doi.org/10.1146/annurev.ecolsys.33.010802.150513
Rabalais NN, Turner RE, Gupta BS, Boesch DF, Chapman P, Murrell MC (2007) Hypoxia in the northern Gulf of Mexico: Does the science support the plan to reduce, mitigate, and control hypoxia? Estuaries Coasts 30:753–772
Rabalais NN, Turner RE (2016) Predicted Bottom Water Dissolved Oxygen- 2016. Louisiana Universities Marine Consortium. Retrieved from https://gulfhypoxia.net/research/shelfwide-cruise/?y=2016&p=hypoxia_fc Accessed 13 August 2018
Raghoebarsing AA, Pol A, van de Pas-Schoonen KT et al (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440:918–921. https://doi.org/10.1038/nature04617
Reeburgh WS (2007) Oceanic methane biogeochemistry. Chem Rev 107:486–513. https://doi.org/10.1021/cr050362v
Rhee TS, Kettle AJ, Andreae MO (2009) Methane and nitrous oxide emissions from the ocean: A reassessment using basin-wide observations in the Atlantic. J Geophys Res Atmospheres 114:D12304. https://doi.org/10.1029/2008JD011662
Rogener MK, Bracco A, Hunter KS, Saxton MA, Joye SB (2018) Long-term impact of the deepwater Horizon oil well blowout on methane oxidation dynamics in the northern Gulf of Mexico. Elem Sci Anth 6:73. https://doi.org/10.1525/elementa.332
Rönner U, Sörensson F (1985) Denitrification rates in the low-oxygen waters of the stratified Baltic proper. Appl Environ Microbiol 50:801–806
Scavia D, Rabalais NN, Turner RE, Justić D, Wiseman WJ (2003) Predicting the response of Gulf of Mexico hypoxia to variations in Mississippi River nitrogen load. Limnol Oceanogr 48:951–956. https://doi.org/10.4319/lo.2003.48.3.0951
Schmitt M, Faber E, Botz R, Stoffers P (1991) Extraction of methane from seawater using ultrasonic vacuum degassing. Anal Chem 63:529–532. https://doi.org/10.1021/ac00005a029
Schutte CA, Joye SB, Wilson AM, Evans T, Moore WS, Casciotti K (2015) Intense nitrogen cycling in permeable intertidal sediment revealed by a nitrous oxide hot spot. Global Biogeochem Cycles 29:1584–1598. https://doi.org/10.1002/2014GB005052
Seitzinger SP (1988) Denitrification in freshwater and coastal marine ecosystems: Ecological and geochemical significance. Limnol Oceanogr 33:702–724. https://doi.org/10.4319/lo.1988.33.4part2.0702
Seitzinger SP, Nixon SW (1985) Eutrophication and the rate of denitrification and N2O production in coastal marine sediments. Limnol Oceanogr 30:1332–1339
Seitzinger S, Nixon SW, Pilson MEQ, Burke S (1980) Denitrification and N2O production in near-shore marine sediments. Geochim Cosmochim Acta 44:1853–1860. https://doi.org/10.1016/0016-7037(80)90234-3
Shen Y, Fichot CG, Benner R (2012) Floodplain influence on dissolved organic matter composition and export from the Mississippi-Atchafalaya river system to the Gulf of Mexico. Limnol Oceanogr 57:1149–1160. https://doi.org/10.4319/lo.2012.57.4.1149
Solórzano L (1969) Determination of ammonia in natural waters by the phenol hypochlorite method. Limnol Oceanogr 14:799–801
Solorzano L, Sharp JH (1980) Determination of total dissolved phosphorus particulate phosphorus in natural water. Limnol Oceanogr 25:754–758
Steinle L, Graves CA, Treude T et al (2015) Water column methanotrophy controlled by a rapid oceanographic switch. Nat Geosci 8:1–6. https://doi.org/10.1038/ngeo2420
Steinle L, Maltby J, Treude T et al (2017) Effects of low oxygen concentrations on aerobic CH4 oxidation in seasonally hypoxic coastal waters. Biogeosci 14:1631–1645. https://doi.org/10.5194/bg-14-1631-2017
Stewart FJ, Ulloa O, Delong EF (2012) Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ Microbiol 14:23–40. https://doi.org/10.1111/j.1462-2920.2010.02400.x
Takaya N, Catalan-sakairi MAB, Sakaguchi Y, Kato I, Zhou Z, Shoun H (2003) Aerobic denitrifying bacteria that produce low levels of nitrous oxide. Appl Environ Microbiol 69:3152–3157. https://doi.org/10.1128/AEM.69.6.3152
Thamdrup B et al (2019) Anaerobic methane oxidation is an important sink for methane in the ocean’s largest oxygen minimum zone. Limnol Oceanogr: https://doi.org/10.1002/lno.11235
Thrash JC et al (2017) Metabolic roles of uncultivated bacterioplankton lineages in the Northern Gulf of Mexico “dead zone.” mBio 8:e01017-e1117
Tiedje JM (1982) Denitrification. In: Page AL (ed) Methods of soil analysis, Part 2: Chemical and microbiological properties. American Society of Agronomy, Madison, WI, pp 1011–1026. https://doi.org/https://doi.org/10.2134/agronmonogr9.2.2ed.c47
Turner RE, Rabalais NN (2003) Linking landscape and water quality in the Mississippi River Basin for 200 years. BioScience 53: 563–572. https://academic.oup.com/bioscience/article/53/6/563/224739
Turner RE, Rabalais NN (2013) N and P phytoplankton growth limitation, northern Gulf of Mexico. Aquat Microb Ecol 68:159–169. https://doi.org/10.3354/ame01607
Turner RE, Rabalais NN, Justić D (2006) Predicting summer hypoxia in the northern Gulf of Mexico: Riverine N, P, and Si loading. Mar Pollut Bull 52:139–148. https://doi.org/10.1016/j.marpolbul.2005.08.012
Turner RE, Rabalais NN, Justic D (2008) Gulf of Mexico hypoxia: alternate states and a legacy. Environ Sci Technol 42:2323–2327
Turner RE, Rabalais NN, Justić D (2012) Predicting summer hypoxia in the northern Gulf of Mexico Redux. Mar Pollut Bull 64:319–324. https://doi.org/10.1021/es0716103
Ulloa O, Canfield DE, DeLong EF, Letelier RM, Stewart FJ (2012) Microbial oceanography of anoxic oxygen minimum zones. Proc Nat Acad Sci USA 109:15996–16003. https://doi.org/10.1073/pnas.1205009109
Valentine DL, Blanton D, Reeburgh W, Kastner M (2001) Water column methane oxidation adjacent to an area of active hydrate dissociation, Eel River Basin. Geochim Cosmochim Acta 65:63–86. https://doi.org/10.1016/j.cognition.2008.05.007
Vitousek PM, Aber JD, Howarth RW et al (1997) Human alteration of the global nitrogen cycle: Sources and human alteration of the global nitrogen cycle: Sources and consequences. Ecol Appl 7:737–750
Walker JT, Stow CA, Geron C (2010) Nitrous oxide emissions from the Gulf of Mexico hypoxic zone. Environ Sci Techno 44:1617–1623. https://doi.org/10.1021/es902058t
Wanninkhof R (2014) Relationship between wind speed and gas exchange over the ocean revisited. Limnol Oceanogr Methods 12:351–362. https://doi.org/10.4319/lom.2014.12.351
Wanninkhof R, Asher WE, Ho DT, Sweeney C, McGillis WR (2009) Advances in quantifying air-sea gas exchange and environmental forcing. Ann Rev Mar Sci 1:213–244. https://doi.org/10.1146/annurev.marine.010908.163742
Ward BB, Devol AH, Rich JJ, Chang BX, Bulow SE, Naik H, Pratihary A (2009) Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461:78–81. https://doi.org/10.1038/nature08276
Wiseman WJ, Rabalais NN, Turner RE, Dinnel SP, MacNaughton A (1997) Seasonal and interannual variability within the Louisiana coastal current: Stratification and hypoxia. J Mar Syst 12:237–248. https://doi.org/10.1016/S0924-7963(96)00100-5
Wrage N, Velthof GL, van Beusichem ML, Oenema O (2001) Role of nitrifier dentification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732. https://doi.org/10.1016/S0038-0717(01)00096-7
Wright JJ, Konwar KM, Hallam SJ (2012) Microbial ecology of expanding oxygen minimum zones. Nat Rev Microbiol 10:381–394. https://doi.org/10.1038/nrmicro2778
Yamamoto S, Alcauskas JB, Crozier TE (1976) Solubility of CH4 in distilled water and seawater. J Chem Eng Data 21:78–80. https://doi.org/10.1021/je60068a029
Ye W, Zhang G, Zhu Z, Huang D, Han Y, Wang L, Sun M (2016) Methane distribution and sea-to-air flux in the East China Sea during the summer of 2013: impact of hypoxia. Deep Sea Res Part II Top Stud Oceanogr 124:74–83. https://doi.org/10.1016/j.dsr2.2015.01.008
Zhang G, Zhang J, Liu S, Ren J, Xu J, Zhang F (2008) Methane in the Changjiang (Yangtze River) Estuary and its adjacent marine area: riverine input, sediment release and atmospheric fluxes. Biogeochemistry 91:71–84. https://doi.org/10.1007/s10533-008-9259-7
Zhu W, Wang C, Hill J, He Y, Tao B, Mao Z, Wu W (2018) A missing link in the estuarine nitrogen cycle?: coupled nitrifcation-denitrifcation mediated by suspended particulate matter. Sci Rep 8:2282. https://doi.org/10.1038/s41598-018-20688-4
Zhuang GC, Montgomery A, Sibert RJ, Rogener MK, Samarkin VA, Joye SB (2018) Effects of pressure, methane concentration and temperature on the production of methane in marine sediments. Limnol Oceanogr 63:2080–2092. https://doi.org/10.1002/lno.10925
Zhu-Barker X, Cavazos AR, Ostrom NE, Horwath WR, Glass JB (2015) The importance of abiotic reactions for nitrous oxide production. Biogeochemistry 126:251–267. https://doi.org/10.1007/s10533-015-0166-4
Acknowledgements
We thank the captain and crew of the R/V Pelican for help in sample collection, and Lauren Gillies, Ariella Chelsky, and Matthew Rich for help with sample collection and onshore support. Guangchao Zhuang and Ryan Sibert provided help and guidance with the methane oxidation rate assays. This work was made possible by the generous support from Ecosystem Impacts of Oil and Gas in the Gulf (ECOGIG) to SBJ under The Gulf of Mexico Research Initiative, the National Science Foundation (awards OCE-1558916 and OCE-1151698 to FJS), and NOAA’s National Centers for Coastal Ocean Research (award NA09NOS4780204, NGOMEX #251) to NNR and RE Turner. Supporting data for the 2013 and 2015 hypoxia cruises are archived in NOAA’s National Center for Environmental Information. Data are publicly available through the Gulf of Mexico Research Initiative Information and Data Cooperative (GRIIDC) at https://data.gulfresearchinitiative.org (https://doi.org/10.7266/SQNEJDPR). This paper is ECOGIG contribution number 533.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Robert W. Howarth.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This paper is an invited contribution to the 35th Anniversary Special Issue, edited by Sujay Kaushal, Robert Howarth, and Kate Lajtha.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rogener, M.K., Hunter, K.S., Rabalais, N.N. et al. Pelagic denitrification and methane oxidation in oxygen-depleted waters of the Louisiana shelf. Biogeochemistry 154, 231–254 (2021). https://doi.org/10.1007/s10533-021-00778-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-021-00778-8