Abstract
Permeable or sandy sediments cover the majority of the seafloor on continental shelves worldwide, but little is known about their role in the coastal nitrogen cycle. We investigated the rates and controls of nitrogen loss at a sand flat (Janssand) in the central German Wadden Sea using multiple experimental approaches, including the nitrogen isotope pairing technique in intact core incubations, slurry incubations, a flow-through stirred retention reactor and microsensor measurements. Results indicate that permeable Janssand sediments are characterized by some of the highest potential denitrification rates (⩾0.19 mmol N m−2 h−1) in the marine environment. Moreover, several lines of evidence showed that denitrification occurred under oxic conditions. In intact cores, microsensor measurements showed that the zones of nitrate/nitrite and O2 consumption overlapped. In slurry incubations conducted with 15NO3− enrichment in gas-impermeable bags, denitrification assays revealed that N2 production occurred at initial O2 concentrations of up to ∼90 μM. Initial denitrification rates were not substantially affected by O2 in surficial (0–4 cm) sediments, whereas rates increased by twofold with O2 depletion in the at 4–6 cm depth interval. In a well mixed, flow-through stirred retention reactor (FTSRR), 29N2 and 30N2 were produced and O2 was consumed simultaneously, as measured online using membrane inlet mass spectrometry. We hypothesize that the observed high denitrification rates in the presence of O2 may result from the adaptation of denitrifying bacteria to recurrent tidally induced redox oscillations in permeable sediments at Janssand.
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References
Bateman EJ, Baggs EM . (2005). Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biol Fert Soils 41: 379–388.
Bergaust L, Shapleigh J, Frostegård Å, Bakken L . (2008). Transcription and activities of NOx reductases in Agrobacterium tumefaciens: the influence of nitrate, nitrite and oxygen availability. Environ Microbiol 10: 3070–3081.
Billerbeck M, Werner U, Bosselmann K, Walpersdorf E, Huettel M . (2006a). Nutrient release from an exposed intertidal sand flat. Mar Ecol-Prog Ser 316: 35–51.
Billerbeck M, Werner U, Polerecky L, Walpersdorf E, de Beer D, Huettel M . (2006b). Surficial and deep pore water circulation governs spatial and temporal scales of nutrient recycling in intertidal sand flat sediment. Mar Ecol-Prog Ser 326: 61–76.
Boer SI, Hedtkamp SIC, Beusekom JEE, Fuhrman JA, Boetius A, Ramette A . (2009). Time-, sediment depth-related variations in bacterial diversity, community structure in subtidal sands. ISME J 3: 780–791.
Braman RS, Hendrix SA . (1989). Nanogram nitrite and nitrate determination in environmental and biological-materials by vanadium(III) reduction with chemi-luminescence detection. Anal Chem 61: 2715–2718.
Brandes JA, Devol AH, Deutsch C . (2007). New developments in the marine nitrogen cycle. Chem Rev 107: 577–589.
Carter J, Hsaio Y, Spiro S, Richardson D . (1995). Soil and sediment bacteria capable of aerobic nitrate respiration. Appl Environ Microb 61: 2852–2858.
Chen F, Xia Q, Ju LK . (2003). Aerobic denitrification of pseudomonas aeruginosa monitored by online NAD(P)H fluorescence. Appl Environ Microb 69: 6715–6722.
Codispoti LA, Brandes JA, Christensen JP, Devol AH, Naqvi SWA, Paerl HW et al. (2001). The oceanic fixed nitrogen and nitrous oxide budgets: moving targets as we enter the anthropocene? Sci Mar 65: 85–105.
Cook PLM, Wenzhofer F, Rysgaard S, Galaktionov OS, Meysman FJR, Eyre BD et al. (2006). Quantification of denitrification in permeable sediments: insights from a two-dimensional simulation analysis and experimental data. Limnol Oceanogr-Meth 4: 294–307.
Dalsgaard T, Zwart Jd, Robertson LA, Kuenen JG, Revsbech NP . (1995). Nitrification, denitrification and growth in artificial Thiosphaera pantotropha biofilms as measured with a combined microsensor for oxygen and nitrous oxide. FEMS Microbiol Ecol 17: 137–148.
de Beer D, Wenzhofer F, Ferdelman TG, Boehme SE, Huettel M, van Beusekom JEE et al. (2005). Transport and mineralization rates in North Sea sandy intertidal sediments, Sylt-Rømø Basin, Wadden Sea. Limnolo Oceanogr 50: 113–127.
Emery KO . (1968). Relict sands on continental shelves of the world. Am Assoc Petrol Geo Bull 52: 445–464.
Gihring TM, Canion A, Riggs A, Huettel M, Kostka JE . (2010). Denitrification in shallow, sublittoral Gulf of Mexico permeable sediments. Limonolo Oceanogr 54: 43–54.
Gray NF . (1990). Activated Sludge: Theory and Practice. Oxford University Press: Oxford, United Kingdom.
Hall PJ, Aller RC . (1992). Rapid, small-volume, flow injection analysis for ΣCO2, and NH4+ in marine and freshwaters. Limnol Oceanogr 37: 1113–1119.
Hayatsu M, Tago K, Saito M . (2008). Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54: 33–45.
Huang HK, Tseng SK . (2001). Nitrate reduction by Citrobacter diversus under aerobic environment. Appl Microbiol Biot 55: 90–94.
Huettel M, Rusch A . (2000). Transport and degradation of phytoplankton in permeable sediment. Limnol Oceanogr 45: 534–549.
Huettel M, Gust G . (1992). Impact of bioroughness on interfacial solute exchange in permeable sediments. Mar Ecol-Prog Ser 89: 253–267.
Hulth S, Aller RC, Canfield DE, Dalsgaard T, Engstrom P, Gilbert F et al. (2005). Nitrogen removal in marine environments: recent findings and future research challenges. Mar Chem 94: 125–145.
Hunter EM, Mills HJ, Kostka JE . (2006). Microbial community diversity associated with carbon and nitrogen cycling in permeable shelf sediments. Appl Environ Microb 72: 5689–5701.
Jahnke RA, Nelson JR, Marinelli RL, Eckman JE . (2000). Benthic flux of biogenic elements on the Southeastern US continental shelf: influence of pore water advective transport and benthic microalgae. Cont Shelf Res 20: 109–127.
Jansen S, Walpersdorf E, Werner U, Billerbeck M, Böttcher M, de Beer D . (2009). Functioning of intertidal flats inferred from temporal and spatial dynamics of O2, H2S and pH in their surface sediment. Ocean Dynam 59: 317–332.
Johnson HD, Baldwin CT . (1986). Shallow siliciclastic seas. In: Reading HG (ed). Sedimentary Environments and Facies, 2nd edn. Blackwell Scientific Publications: Oxford. pp 229–282.
Larsen LH, Kjaer T, Revsbech NP . (1997). A microscale NO3− biosensor for environmental applications. Anal Chem 69: 3527–3531.
Laursen AE, Seitzinger SP . (2002). The role of denitrification in nitrogen removal and carbon mineralization in Mid-Atlantic Bight sediments. Cont Shelf Res 22: 1397–1416.
Lloyd D, Boddy L, Davies KJP . (1987). Persistence of bacterial denitrification capacity under aerobic conditions—the rule rather than the exception. FEMS Microbiol Ecol 45: 185–190.
Mills HJ, Hunter E, Humphrys M, Kerkhof L, McGuinness L, Huettel M et al. (2008). Characterization of nitrifying, denitrifying, and overall bacterial communities in permeable marine sediments of the northeastern Gulf of Mexico. Appl Environ Microb 74: 4440–4453.
Nielsen LP . (1992). Denitrification in sediment determined from nitrogen isotope pairing. FEMS Microbiol Ecol 86: 357–362.
Patureau D, Zumstein E, Delgenes JP, Moletta R . (2000). Aerobic denitrifiers isolated from diverse natural and managed ecosystems. Microbial Ecol 39: 145–152.
Ploug H . (2001). Small-scale oxygen fluxes and remineralization in sinking aggregates. Limnol Oceanogr 46: 1624–1631.
Polerecky L, Franke U, Werner U, Grunwald B, de Beer D . (2005). High spatial resolution measurement of oxygen consumption rates in permeable sediments. Limnol Oceanogr-Meth 3: 75–85.
Rao AMF, McCarthy MJ, Gardner WS, Jahnke RA . (2007). Respiration and denitrification in permeable continental shelf deposits on the South Atlantic Bight: rates of carbon and nitrogen cycling from sediment column experiments. Cont Shelf Res 27: 1801–1819.
Rao AMF, Mccarthy MJ, Gardner WS, Jahnke RA . (2008). Respiration and denitrification in permeable continental shelf deposits on the South Atlantic Bight: N2:Ar and isotope pairing measurements in sediment column experiments. Cont Shelf Res 28: 602–613.
Revsbech NP . (1989). An oxygen microsensor with a guard cathode. Limnol Oceanogr 34: 474–478.
Robertson LA, Dalsgaard T, Revsbech NP, Kuenen JG . (1995). Confirmation of ‘aerobic denitrification’ in batch cultures, using gas chromatography and 15N mass spectrometry. FEMS Microbiol Ecol 18: 113–119.
Robertson LA, Kuenen JG . (1984). Aerobic denitrification—a controversy revived. Arch Microbiol 139: 351–354.
Robertson LA, Kuenen JG . (1988). Heterotrophic nitrification in thiosphaera-pantotropha—oxygen-uptake and enzyme studies. J Gen Microbiol 134: 857–863.
Ronner U, Sorensson F . (1985). Denitrification rates in the low-oxygen waters of the stratified baltic proper. Appl Environ Microbiol 50: 801–806.
Røy H, Lee JS, Jansen S, de Beer D . (2008). Tide-driven deep pore-water flow in intertidal sand flats. Limnol Oceanogr 53: 1521–1530.
Schmidt I, Sliekers O, Schmid M, Bock E, Fuerst J, Kuenen JG et al. (2003). New concepts of microbial treatment processes for the nitrogen removal in wastewater. FEMS Microbiol Rev 27: 481–492.
Schramm A, Santegoeds CM, Nielsen HK, Ploug H, Wagner M, Pribyl M et al. (1999). On the occurrence of anoxic microniches, denitrification, and sulfate reduction in aerated activated sludge. Appl Environ Microb 65: 4189–4196.
Seeberg-Elverfeldt J, Schlüter M, Feseker T, Kölling M . (2005). Rhizon sampling of pore waters near the sediment-water interface of aquatic systems. Limnol Oceanogr-Meth 3: 361–371.
Shapleigh J . (2006). The Denitrifying Prokaryotes. In: M Dworkin (ed). The Prokaryotes: A 740 Handbook on the Biology of Bacteria: Volume 2: Ecophysiology and Biochemistry. Springer-Verlag: New York, NY, pp 769–792.
Thamdrup B, Dalsgaard T . (2002). Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68: 1312–1318.
Tiedje JM . (1988). Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed). Environmental Microbiology of Anaerobes. John Wiley and Sons: New York. pp 179–244.
Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA . (1982). Denitrification: ecological niches, competition and survival. Antonie Van Leeuwenhoek 48: 569–583.
Trevors JT, Starodub ME . (1987). Effect of oxygen concentration on denitrification in freshwater sediment. J Basic Microb 27: 387–391.
Vance-Harris C, Ingall E . (2005). Denitrification pathways and rates in the sandy sediments of the Georgia continental shelf. Geochim Cosmochim Ac 69: A578.
Werner U, Billerbeck M, Polerecky L, Franke U, Huettel M . (2006). Spatial and temporal patterns of mineralization rates and oxygen distribution in a permeable intertidal sand flat (Sylt, Germany). Limnol Oceanogr 51: 2549–2563.
Zehr JP, Ward BB . (2002). Nitrogen cycling in the ocean: new perspectives on processes and paradigms. Appl Environ Microb 68: 1015–1024.
Zumft W . (1997). Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61: 533–616.
Acknowledgements
We thank the Captains Ronald Monas, Ole Pfeiler and colleagues Hans Roy, Stefan Jansen and Ingrid Dohrmann for their cheerful support on the ship and shipping time; Phyllis Lam for her constructive comments; Gabriele Klockgether and Daniela Franzke for technical supports. This research was supported by German Academic Exchange Center (Deutscher Akademischer Austausch Dienst, DAAD), Max-Planck-Society (MPG) and German Research Foundation (DFG). JEK was partially supported by the Hanse-Wissenschaftskolleg and by grants from the US National Science Foundation (OCE-0424967 and OCE-0726754).
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Gao, H., Schreiber, F., Collins, G. et al. Aerobic denitrification in permeable Wadden Sea sediments. ISME J 4, 417–426 (2010). https://doi.org/10.1038/ismej.2009.127
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DOI: https://doi.org/10.1038/ismej.2009.127
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