Advertisement

Biogeochemistry

, Volume 135, Issue 1–2, pp 103–119 | Cite as

Seasonal benthic nitrogen cycling in a temperate shelf sea: the Celtic Sea

  • V. KitidisEmail author
  • K. Tait
  • J. Nunes
  • I. Brown
  • E. M. S. Woodward
  • C. Harris
  • A. J. M. Sabadel
  • D. B. Sivyer
  • B. Silburn
  • S. Kröger
Article

Abstract

We undertook a seasonal study of benthic N-cycling on the Celtic Sea continental shelf in 2015, augmented by an earlier cruise in 2014. Two cruises in 2015 were centred before and after the Spring phytoplankton bloom and a further cruise was carried out in late summer. Five sites covering the mud to sand continuum were visited on all cruises, where we determined ammonium-oxidation, anammox and denitrification rates, expression of anammox and denitrification genes, N-nutrient fluxes and sediment porewater profiles of N-nutrients. Highest process rates were found during the post-bloom and late summer periods. The Celtic Sea was overwhelmingly a source of inorganic-N to the overlying water column. The efflux of nitrate was controlled by the magnitude of ammonium-oxidation. The latter accounted for 10–16% of total Oxygen consumption in cohesive sediments and 35–56% in sandy sediments. Ammonium oxidation rates in the range of 0.001–2.288 mmol m−2 days−1 were inversely correlated with sediment porosity and positively correlated with organic matter content (OM) which together explained 66% of the variance in rates. N-removal was dominated by anammox (0.003–0.636 mmol m−2 days−1), rather than denitrification (0.000–0.034 mmol m−2 days−1). This finding was supported by the corresponding gene expression data. The expression of hydrazine oxidoreductase (anammox) was significantly correlated with anammox and total N-removal rates. Anammox was positively correlated with porosity and OM, whilst denitrification was correlated with OM. The N-requirement of these processes was largely met through nitrification (ammonium-oxidation) rather than influx from the overlying water column. We estimated that N-removal via denitrification and anammox removed 6–9% of the organic-N deposited at the sea-floor from the overlying water column. The Celtic Sea system was thereby losing N which must be replenished on an annual basis in order to sustain productivity.

Keywords

Shelf-seas N-cycle Sediment Nitrification Denitrification Anammox 

Notes

Acknowledgements

We would like to thank two anonymous reviewers for the constructive reviews of this manuscript. This work was conducted under Work-packages 1 and 2 of the Shelf Sea Biogeochemistry programme (SSB WP2, [NE/K00204X/1 and NE/K002058/1], 2011-2017), jointly funded by the Natural Environment Research Council (NERC) and the Department for Environment, Food and Rural Affairs (Defra). The views expressed are those of the author(s) and do not necessarily represent those of NERC or Defra.

References

  1. An SM, 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(3):1171–1178CrossRefGoogle Scholar
  2. Anderson LA, Sarmiento JL (1994) Redfield ratios of remineralization determined by nutrient data-analysis. Glob Biogeochem Cycle 8(1):65–80CrossRefGoogle Scholar
  3. Balzer W, Helder W, Epping E, Lohse L, Otto S (1998) Benthic denitrification and nitrogen cycling at the slope and rise of the NW European Continental Margin (Goban Spur). Prog Oceanogr 42(1–4):111–126CrossRefGoogle Scholar
  4. Beman JM, Chow C-E, King AL, Feng Y, Fuhrman JA, Andersson A, Bates NR, Popp BN, Hutchins DA (2011) Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc Natl Acad Sci USA 108(1):208–213CrossRefGoogle Scholar
  5. Boucher G, Clavier J, Garrigue C (1994) Oxygen and carbon-dioxide fluxes at the water-sediment interface of a tropical lagoon. Mar Ecol Prog Ser 107(1–2):185–193CrossRefGoogle Scholar
  6. Bouskill NJ, Eveillard D, Chien D, Jayakumar A, Ward BB (2012) Environmental factors determining ammonia-oxidizing organism distribution and diversity in marine environments. Environ Microbiol 14(3):714–729CrossRefGoogle Scholar
  7. Brewer PG, Riley JP (1965) The automatic determination of nitrate in sea water. Deep-Sea Res 12:765–772Google Scholar
  8. Cai WJ, Dai M, Wang Y (2006) Air-sea exchange of carbon dioxide in ocean margins: a province based synthesis. Geophys Res Lett 33:L12603Google Scholar
  9. Chen Z, Liu JB, Wu MN, Xie XL, Wu JS, Wei WX (2012) Differentiated Response of Denitrifying Communities to Fertilization Regime in Paddy Soil. Microb Ecol 63(2):446–459CrossRefGoogle Scholar
  10. Crowe SA, Canfield DE, Mucci A, Sundby B, Maranger R (2012) Anammox, denitrification and fixed-nitrogen removal in sediments from the Lower St. Lawrence Estuary. Biogeosciences 9(11):4309–4321CrossRefGoogle Scholar
  11. Decleyre H, Heylen K, Van Colen C, Willems A (2015) Dissimilatory nitrogen reduction in intertidal sediments of a temperate estuary: small scale heterogeneity and novel nitrate-to-ammonium reducers. Front Microbiol 6:1124CrossRefGoogle Scholar
  12. Delwiche CC (1959) Production and utilization of nitrous oxide by Pseudomonas denitrificans. J Bacteriol 77:55–59Google Scholar
  13. Devol AH (2008) Denitrification including Anammox. In: Capone DG, Bronk DA, Mulholland MR, Carpenter EJ (eds) Nitrogen in the marine environment, 2nd edn. Academic Press, Amsterdam, pp 263–301CrossRefGoogle Scholar
  14. Forja JM, Ortega T, DelValls TA, Gomez-Parra A (2004) Benthic fluxes of inorganic carbon in shallow coastal ecosystems of the Iberian Peninsula. Mar Chem 85(3–4):141–156CrossRefGoogle Scholar
  15. Garcia HE, Gordon LI (1992) Oxygen solubility in seawater - better fitting equations. Limnol Oceanogr 37(6):1307–1312CrossRefGoogle Scholar
  16. Gihring TM, Humphrys M, Mills HJ, Huettel M, Kostka JE (2009) Identification of phytodetritus-degrading microbial communities in sublittoral Gulf of Mexico sands. Limnol Oceanogr 54(4):1073–1083CrossRefGoogle Scholar
  17. Glud RN (2008) Oxygen dynamics of marine sediments. Mar Biol Res 4(4):243–289CrossRefGoogle Scholar
  18. 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):526–532Google Scholar
  19. Grasshoff K (1983) Determination of nitrite. In: Grasshoff K, Ehrhardt M, Kremling K (eds) Methods of seawater analysis. Verlag Chemie, Weinheim, pp 139–142Google Scholar
  20. Grundmanis V, Murray JW (1982) Aerobic respiration in pelagic marine-sediments. Geochim Cosmochim Acta 46(6):1101–1120CrossRefGoogle Scholar
  21. Hamersley MR, Lavik G, Woebken D, Rattray JE, Lam P, Hopmans EC, Sinninghe Damste JS, Krueger S, Graco M, Gutierrez D, Kuypers MMM (2007) Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol Oceanogr 52(3):923–933CrossRefGoogle Scholar
  22. Hamme RC, Emerson SR (2004) The solubility of neon, nitrogen and argon in distilled water and seawater. Deep Sea Res Part I 51(11):1517–1528CrossRefGoogle Scholar
  23. Henriksen K, Hansen JI, Blackburn TH (1981) Rates of nitrification, distribution of nitrifying bacteria, and nitrate fluxes in different types of sediment from Danish waters. Mar Biol 61(4):299–304CrossRefGoogle Scholar
  24. Hopkinson CS, Giblin AE, Tucker J (2001) Benthic metabolism and nutrient regeneration on the continental shelf of Eastern Massachusetts, USA. Mar Ecol Prog Ser 224:1–19CrossRefGoogle Scholar
  25. Howes E, Joos F, Eakin M, Gattuso J-P (2015) An updated synthesis of the observed and projected impacts of climate change on the chemical, physical and biological processes in the oceans. Front Mar Sci 2:36CrossRefGoogle Scholar
  26. Hydes DJ, Aoyama M, Aminot A, Bakker K, Becker S, Coverly S, Daniel A, Dickson G, Grosso O, Kerouel R, van-Ooijen J, Sato K, Tanhua T, Woodward EMS, Zhang JZ (2010) Determination of dissolved nutrients (N,P,Si) in seawater with high precision and inter-comparability using gas-segmented continuous flow analysers. In: Hood EM, Sabine CL & Sloyan BM (eds) The GO-SHIP Repeat Hyrography Manual: a collection of expert reports and guidelines. p IOCCP Report Number 14, ICPO Publication Series Number 134. http://www.go-ship.org/HydroMan.html
  27. Jahnke RA (2010) Global synthesis. Carbon and nutrient fluxes in continental margins. Springer, Berlin, pp 597–615CrossRefGoogle Scholar
  28. Jenkins MC, Kemp WM (1984) The coupling of nitrification and denitrification in 2 estuarine sediments. Limnol Oceanogr 29(3):609–619CrossRefGoogle Scholar
  29. Jensen MM, Kuypers MMM, Lavik G, Thamdrup B (2008) Rates and regulation of anaerobic ammonium oxidation and denitrification in the Black Sea. Limnol Oceanogr 53(1):23–36CrossRefGoogle Scholar
  30. Jickells TD (1998) Nutrient biogeochemistry of the coastal zone. Science 281:217–222CrossRefGoogle Scholar
  31. Joye SB, Anderson IC (2008) Nitrogen cycling in coastal sediments. In: Capone DG, Bronk DA, Mulholland MR, Carpenter EJ (eds) Nitrogen in the marine environment, 2nd edn. Academic Press, Amsterdam, pp 868–915Google Scholar
  32. Kana TM, Darkangelo C, Hunt MD, Oldham JB, Bennett GE, Cornwell JC (1994) Membrane Inlet Mass-Spectrometer for rapid high-precision determination of N-2, O-2 and Ar in environmental water samples. Anal Chem 66(23):4166–4170CrossRefGoogle Scholar
  33. Kartal B, Maalcke WJ, de Almeida NM, Cirpus I, Gloerich J, Geerts W, den Camp HJMO, Harhangi HR, Janssen-Megens EM, Francoijs K-J, Stunnenberg HG, Keltjens JT, Jetten MSM, Strous M (2011) Molecular mechanism of anaerobic ammonium oxidation. Nature 479(7371):127-U159CrossRefGoogle Scholar
  34. Kitidis V, Laverock B, McNeill LC, Beesley A, Cummings D, Tait K, Osborn MA, Widdicombe S (2011) Impact of ocean acidification on benthic and water column ammonia oxidation. Geophys Res Lett. doi: 10.1029/2011GL049095 Google Scholar
  35. Kitidis V, Hardman-Mountford NJ, Litt E, Brown I, Cummings D, Hartman S, Hydes D, Fishwick JR, Harris C, Martinez-Vicente V, Woodward EMS, Smyth TJ (2012) Seasonal dynamics of the carbonate system in the Western English Channel. Cont Shelf Res 42:30–40CrossRefGoogle Scholar
  36. Kitidis V, Brown I, Hardman-Mountford N, Lefevre N (2016) Surface ocean carbon dioxide during the Atlantic Meridional Transect (1995-2013); evidence of ocean acidification. Prog Oceanogr. doi: 10.1016/j.pocean.2016.1008.1005 Google Scholar
  37. Laverock B, Kitidis V, Tait K, Gilbert JA, Osborn AM, Widdicombe S (2013) Bioturbation determines the response of benthic ammonia-oxidizing microorganisms to ocean acidification. Philos Trans R Soc Lond B Biol Sci 368(1627):20120441CrossRefGoogle Scholar
  38. Le Quéré C, Moriarty R, Andrew RM, Canadell JG, Sitch S, Korsbakken JI, Friedlingstein P, Peters GP, Andres RJ, Boden TA, Houghton RA, House JI, Keeling RF, Tans P, Arneth A, Bakker DCE, Barbero L, Bopp L, Chang J, Chevallier F, Chini LP, Ciais P, Fader M, Feely RA, Gkritzalis T, Harris I, Hauck J, Ilyina T, Jain AK, Kato E, Kitidis V, Klein Goldewijk K, Koven C, Landschützer P, Lauvset SK, Lefèvre N, Lenton A, Lima ID, Metzl N, Millero F, Munro DR, Murata A, Nabel JEMS, Nakaoka S, Nojiri Y, O’Brien K, Olsen A, Ono T, Pérez FF, Pfeil B, Pierrot D, Poulter B, Rehder G, Rödenbeck C, Saito S, Schuster U, Schwinger J, Séférian R, Steinhoff T, Stocker BD, Sutton AJ, Takahashi T, Tilbrook B, van der Laan-Luijkx IT, van der Werf GR, van Heuven S, Vandemark D, Viovy N, Wiltshire A, Zaehle S, Zeng N (2015) Global carbon budget 2015. Earth Syst Sci Data 7(2):349–396CrossRefGoogle Scholar
  39. Li M, Hong YG, Klotz MG, Gu JD (2010) A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments. Appl Microbiol Biotechnol 86(2):781–790CrossRefGoogle Scholar
  40. Mantoura RFC, Woodward EMS (1983) Optimization of the indophenol blue method for the automated determination of ammonia in estuarine waters. Estuar Coast Shelf Sci 17:219–224CrossRefGoogle Scholar
  41. Marchant HK, Holtappels M, Lavik G, Ahmerkamp S, Winter C, Kuypers MMM (2016) Coupled nitrification-denitrification leads to extensive N loss in subtidal permeable sediments. Limnol Oceanogr 61(3):1033–1048CrossRefGoogle Scholar
  42. Naqvi SWA, Jayakumar DA, Narvekar PV, Naik H, Sarma V, D’Souza W, Joseph S, George MD (2000) Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf. Nature 408(6810):346–349CrossRefGoogle Scholar
  43. Neubacher EC, Parker RE, Trimmer M (2011) Short-term hypoxia alters the balance of the nitrogen cycle in coastal sediments. Limnol Oceanogr 56(2):651–665CrossRefGoogle Scholar
  44. Patsch J, Kuhn W (2008) Nitrogen and carbon cycling in the North Sea and exchange with the North Atlantic—a model study. Part I. Nitrogen budget and fluxes. Cont Shelf Res 28(6):767–787CrossRefGoogle Scholar
  45. Pina-Ochoa E, Alvarez-Cobelas M (2006) Denitrification in aquatic environments: a cross-system analysis. Biogeochemistry 81(1):111–130CrossRefGoogle Scholar
  46. Rabouille C, Denis L, Dedieu K, Stora G, Lansard B, Grenz C (2003) Oxygen demand in coastal marine sediments: comparing in situ microelectrodes and laboratory core incubations. J Exp Mar Biol Ecol 285:49–69CrossRefGoogle Scholar
  47. Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326(5949):123–125CrossRefGoogle Scholar
  48. Rees AP, Gilbert JA, Kelly-Gerreyn BA (2009) Nitrogen fixation in the western English Channel (NE Atlantic Ocean). Mar Ecol Prog Ser 374:7–12CrossRefGoogle Scholar
  49. Ribas-Ribas M, Rérolle VMC, Bakker DCE, Kitidis V, Lee GA, Brown I, Achterberg EP, Hardman-Mountford NJ, Tyrrell T (2014) Intercomparison of carbonate chemistry measurements on a cruise in northwestern European shelf seas. Biogeosciences 11:4339–4355CrossRefGoogle Scholar
  50. Rich JJ, Dale OR, Song B, Ward BB (2008) Anaerobic ammonium oxidation (Anammox) in Chesapeake Bay sediments. Microb Ecol 55:311–320CrossRefGoogle Scholar
  51. Romero-Kutzner V, Packard TT, Berdalet E, Roy SO, Gagne JP, Gomez M (2015) Respiration quotient variability: bacterial evidence. Mar Ecol Prog Ser 519:47–59CrossRefGoogle Scholar
  52. Rysgaard S, Fossing H, Jensen MM (2001) Organic matter degradation through oxygen respiration, denitrification, and manganese, iron, and sulfate reduction in marine sediments (the Kattegat and the Skagerrak). Ophelia 55(2):77–91CrossRefGoogle Scholar
  53. Santoro AE, Casciotti KL (2011) Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation. ISME J 5(11):1796–1808CrossRefGoogle Scholar
  54. Santos IR, Eyre BD, Glud RN (2012) Influence of porewater advection on denitrification in carbonate sands: evidence from repacked sediment column experiments. Geochim Cosmochim Acta 96:247–258CrossRefGoogle Scholar
  55. Schmid MC, Hooper AB, Klotz MG, Woebken D, Lam P, Kuypers MMM, Pommerening-Roeser A, Op den Camp HJM, Jetten MSM (2008) Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ Microbiol 10(11):3140–3149CrossRefGoogle Scholar
  56. Sciberras M, Parker R, Powell C, Robertson C, Kroeger S, Bolam S, Hiddink JG (2016) Impacts of bottom fishing on the sediment infaunal community and biogeochemistry of cohesive and non-cohesive sediments. Limnol Oceanogr 61(6):2076–2089CrossRefGoogle Scholar
  57. Seitzinger S, Harrison JA, Bohlke JK, Bouwman AF, Lowrance R, Peterson B, Tobias C, Van Drecht G (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16(6):2064–2090CrossRefGoogle Scholar
  58. Smith CJ, Nedwell DB, Dong LF, Osborn AM (2006) Evaluation of quantitative polymerase chain reaction-based approaches for determining gene copy and gene transcript numbers in environmental samples. Environ Microbiol 8(5):804–815CrossRefGoogle Scholar
  59. Smyth TJ, Fishwick JR, Al-Moosawi L, Cummings DG, Harris C, Kitidis V, Rees A, Martinez-Vicente V, Woodward EMS (2010) A broad spatio-temporal view of the Western English Channel observatory. J Plankton Res 32(5):585–601CrossRefGoogle Scholar
  60. Spokes LJ, Jickells TD (2005) Is the atmosphere really an important source of reactive nitrogen to coastal waters? Cont Shelf Res 25(16):2022–2035CrossRefGoogle Scholar
  61. Stief P (2013) Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications. Biogeosciences 10(12):7829–7846CrossRefGoogle Scholar
  62. Strauss EA, Lamberti GA (2000) Regulation of nitrification in aquatic sediments by organic carbon. Limnol Oceanogr 45(8):1854–1859CrossRefGoogle Scholar
  63. Tait K, Kitidis V, Ward BB, Cummings DG, Jones MR, Somerfield PJ, Widdicombe S (2014) Spatio-temporal variability in ammonia oxidation and ammonia oxidising bacteria and archaea in coastal sediments of the Western English Channel. Mar Ecol Prog Ser 511:41–58CrossRefGoogle Scholar
  64. Tait K, Airs RL, Widdicombe CE, Tarran GA, Jones MR, Widdicombe S (2015) Dynamic responses of the benthic bacterial community at the Western English Channel observatory site L4 are driven by deposition of fresh phytodetritus. Prog Oceanogr 137:546–558CrossRefGoogle Scholar
  65. Thamdrup B, Dalsgaard T (2002) Production of N-2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68(3):1312–1318CrossRefGoogle Scholar
  66. Thouzeau G, Grall J, Clavier J, Chauvaud L, Jean F, Leynaert A, ni Longphuirt S, Amice E, Amouroux D (2007) Spatial and temporal variability of benthic biogeochemical fluxes associated with macrophytic and macrofaunal distributions in the Thau lagoon (France). Estuar Coast Shelf Sci 72(3):432–446CrossRefGoogle Scholar
  67. Tortell PD (2005) Dissolved gas measurements in oceanic waters made by membrane inlet mass spectrometry. Limnol Oceanogr Methods 3:24–37CrossRefGoogle Scholar
  68. Trimmer M, Nicholls JC (2009) Production of nitrogen gas via anammox and denitrification in intact sediment cores along a continental shelf to slope transect in the North Atlantic. Limnol Oceanogr 54(2):577–589CrossRefGoogle Scholar
  69. Trimmer M, Engstrom P, Thamdrup B (2013) Stark contrast in denitrification and anammox across the deep Norwegian trench in the Skagerrak. Appl Environ Microbiol 79(23):7381–7389CrossRefGoogle Scholar
  70. Ward BB (2008) Nitrification in marine systems. In: Capone DG, Bronk DA, Mulholland MR, Carpenter EJ (eds) Nitrogen in the marine environment, 2nd edn. Academic Press, Amsterdam, pp 199–261CrossRefGoogle Scholar
  71. Ward BB (2011) Measurement and distribution of nitrification rates in the oceans. In: Klotz MG (ed) Methods in enzymology: research on nitrification and related processes, part A. Methods in enzymology, vol 486., pp 307–323CrossRefGoogle Scholar
  72. Welshmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and phaeopigments. Limnol Oceanogr 39(8):1985–1992CrossRefGoogle Scholar
  73. Hicks N, Ubbara G, Silburn B, Smith H, Kröger S, Parker R, Sivyer D, Kitidis V, Stahl H, Mayor DJ, Hatton A (this issue) Oxygen dynamics in shelf seas sediments incorporating seasonal variability. BiogeochemistryGoogle Scholar
  74. Klar JK, Homoky WB, Statham PJ, Harris EL, Birchill A, Woodward EMS, Silburn B, Cooper M, James RH, Connelly DP, Chever F, Lichtschlag A, Graves C (this issue) Stability of dissolved and soluble Fe(II) in shelf sediment pore waters and release to an oxic water column. BiogeochemistryGoogle Scholar
  75. Thompson CEL, Amoudry LO, Godbold JA, Hale R, Hicks N, Hiddink JG, Homoky W, Hull T, Klar JK, Kowalik J, Kröger S, Laguionie Marchais C, Morris K, Parker E.R., Reynolds S, Ruhl H, Silburn B, Sivyer D, Solan M, Smith H, Kitidis V, Tate K, Widdicombe S, Williams ME, Woodward EMS (this issue) An approach for the identification of exemplar sites for scaling up targeted field observations of benthic biogeochemistry to regional predictions in heterogeneous environments. Biogeochemistry (submitted)Google Scholar
  76. Zhang Q, Warwick RM, McNeill CL, Widdicombe CE, Sheehan A, Widdicombe S (2015) An unusually large phytoplankton spring bloom drives rapid changes in benthic diversity and ecosystem function. Prog Oceanogr 137:533–545CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Plymouth Marine LaboratoryPlymouthUK
  2. 2.Department of ChemistryUniversity of OtagoDunedinNew Zealand
  3. 3.Centre for Environment, Fisheries and Aquaculture Science (CEFAS)LowestoftUK

Personalised recommendations