Abstract
Nitrate dual stable isotopes (δ15N and δ18O of NO3 −) have proven to be a powerful technique to elucidate nitrogen (N) cycling pathways in aquatic systems. We applied this technique for the first time in the pelagic zone of a small temperate meso-eutrophic lake to identify the dominant N cycling pathways, and their spatial and temporal variability. We measured the lake NO3 − δ15N and δ18O signatures over an annual cycle and compared them to that of the watershed. Both δ15N and δ18O of NO3 − in the lake increased during summer relative to the inputs. Relationships between lake NO3 − isotopic composition and concentrations were different across thermal strata with an apparent isotope effect in the epilimnion of 15εepi = 4.6‰ and 18εepi = 10.9‰. We found a strong deviation of the lake NO3 − δ18O and δ15N from the expected 1:1 line for assimilation (slope = 1.73) suggesting that nitrification was co-occurring. We estimated that nitrification could support between 5 and 30% of nitrate-based production during the growing season, but was negligible in early spring and fall, and probably more dominant under ice. We showed that the technique is promising to study N processes at the ecosystem scale in shallow lakes, particularly during winter. Our results suggest that recycled NO3 − could support primary productivity and influence phytoplankton composition in the surface waters of small lakes.
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References
American Public Health Association (2005) Standard methods for the examination of water and wastewater. American Public Health Association, Washington, DC
Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726
Anisfeld SC, Barnes RT, Altabet MA, Wu T (2007) Isotopic apportionment of atmospheric and sewage nitrogen sources in two Connecticut rivers. Environ Sci Technol 41:6363–6369
Berg G, Balode M, Purina I, Bekere S, Béchemin C, Maestrini S (2003) Plankton community composition in relation to availability and uptake of oxidized and reduced nitrogen. Aquat Microb Ecol 30:263–274
Botrel M (2011) Caractérisation du cycle et des sources d’azote dans les lacs tempérés par l’utilisation d’isotopes stables. Dissertation, Université de Montréal https://papyrus.bib.umontreal.ca
Bourbonnais A, Lehmann MF, Waniek JJ, Schulz-Bull DE (2009) Nitrate isotope anomalies reflect N-2 fixation in the Azores Front region (subtropical NE Atlantic). J Geophys Res-Oceans 114:1–16. doi:10.1029/2007JC004617
Bowen GJ (2012) The online isotopes in precipitation calculator, version 2.2. http://www.waterisotopes.org
Buchwald C, Casciotti KL (2010) Oxygen isotopic fractionation and exchange during bacterial nitrite oxidation. Limnol Oceanogr 55:1064–1074
Buchwald C, Casciotti KL (2013) Isotopic ratios of nitrite as tracers of the sources and age of oceanic nitrite. Nat Geosci 6(4):308–313
Buchwald C, Santoro AE, McIlvin MR, Casciotti KL (2012) Oxygen isotopic composition of nitrate and nitrite produced by nitrifying cocultures and natural marine assemblages. Limnol Oceanogr 57(5):1361–1375
Burns DA, Boyer EW, Elliott EM, Kendall C (2009) Sources and transformations of nitrate from streams draining varying land uses: evidence from dual isotope analysis. J Environ Qual 38:1149–1159
Carpenter SR, Caraco NF, Correll DL, Howarth RW, Sharpley AN, Smith VH (1998) Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol Appl 8:559–568
Casciotti KL, Buchwald C (2012) Insights on the marine microbial nitrogen cycle from isotopic approaches to nitrification. Front Microbiol 3:1–14. doi:10.3389/fmicb.2012.00356
Casciotti KL, McIlvin MR (2007) Isotopic analyses of nitrate and nitrite from reference mixtures and application to Eastern Tropical North Pacific waters. Mar Chem 107:184–201
Casciotti KL, Sigman DM, Hasting MG, Bölke JK, Hilkert A (2002) Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method. Anal Chem 74:4905–4912
Casciotti KL, Sigman DM, Ward BB (2003) Linking diversity and stable isotope fractionation in ammonia-oxidizing bacteria. Geomicrobiol J 20:335–353
Casciotti KL, McIlvin M, Buchwald C (2010) Oxygen isotopic exchange and fractionation during bacterial ammonia oxidation. Limnol Oceanogr 55(2):753–762
Casciotti KL, Buchwald C, Santoro AE, Frame C (2011) Assessment of nitrogen and oxygen isotopic fractionation during nitrification and its expression in the marine environment. In: Klotz MG (ed) Methods in enzymology: research on nitrification and related processes, part A, vol 486. Academic Press, San Diego, pp 253–280
Collos Y, Linley E, Frikha M, Ravail B (1988) Phytoplankton death and nitrification at low temperatures. Estuar Coast Shelf S 27:341–347
Dehairs F et al (2015) Nitrogen cycling in the Southern Ocean Kerguelen Plateau area: evidence for significant surface nitrification from nitrate isotopic compositions. Biogeosciences 12:1459–1482
Deutsch B, Voss M, Fischer H (2009) Nitrogen transformation processes in the Elbe River: distinguishing between assimilation and denitrification by means of stable isotope ratios in nitrate. Aquat Sci 71:228–237
DiFiore PJ, Sigman DM, Dunbar RB (2009) Upper ocean nitrogen fluxes in the Polar Antarctic Zone: Constraints from the nitrogen and oxygen isotopes of nitrate. Geochem Geophys Geosyst. 10:1–22. doi:10.1029/2009gc002468
Dijkstra P, LaViolette CM, Coyle JS, Doucett RR, Schwartz E, Hart SC, Hungate BA (2008) 15N enrichment as an integrator of the effects of C and N on microbial metabolism and ecosystem function. Ecol Lett 11:389–397
Downing JA, Prairie YT, Cole JJ, Duarte CM, Tranvik LJ, Striegl RG, McDowell WH, Kortelainen P, Caraco NF, Melack JM, Middelburg JJ (2006) The global abundance and size distribution of lakes, ponds, and impoundments. Limnol Oceanogr 51:2388–2397
Finlay JC, Sterner RW, Kumar S (2007) Isotopic evidence for in-lake production of accumulating nitrate in Lake Superior. Ecol Appl 17:2323–2332
Finlay K, Patoine A, Donald DB, Bogard MJ, Leavitt PR (2010) Experimental evidence that pollution with urea can degrade water quality in phosphorus-rich lakes of the Northern Great Plains. Limnol Oceanogr 55:1213–1230
Flores E, Herrero A (2005) Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem Soc Trans 33:164–167
Fogel ML, Cifuentes LA (1993) Isotope fractionation during primary production. In: Engel MH, Macko SA (eds) Organic geochemistry. Plenum Press, New York, pp 73–98
Granger J, Sigman DM, Needoba JA, Harrison PJ (2004) Coupled nitrogen and oxygen isotope fractionation of nitrate during assimilation by cultures of marine phytoplankton. Limnol Oceanogr 49:1763–1773
Granger J, Sigman DM, Lehmann MF, Tortell PD (2008) Nitrogen and oxygen isotope fractionation during dissimilatory nitrate reduction by denitrifying bacteria. Limnol Oceanogr 53:2533–2545
Hadas O, Altabet MA, Agnihotri R (2009) Seasonally varying nitrogen isotope biogeochemistry of particulate organic matter in Lake Kinneret, Israel. Limnol Oceanogr 54:75–85
Hampton SE et al (2017) Ecology under lake ice. Ecol Lett 20:98–111
Harrelson CC, Rawlins CL, Potyondy JP (1994) Stream channel reference sites: an illustrated guide to field technique. United State Department of Agriculture, General Technical Report RM-245. www.stream.fs.fed.us/publications/PDFs/RM245E.PDF. Accessed 12 Jan 2010
Harrison JA et al (2009) The regional and global significance of nitrogen removal in lakes and reservoirs. Biogeochemistry 93:143–157
Kalff J (2002) Limnology. Prentice-Hall, Upper Saddle River
Kendall C, Elliot EM, Wankel SD (2007) Tracing anthropogenic inputs of nitrogen to ecosystems. In: Michener R, Lajtha K (eds) Stable isotope in ecology and environmental science. Blackwell, Oxford, pp 375–449
Knowles R (1982) Denitrification. Microbiol Rev 46:43–70
Knowles R, Lean DRS (1987) Nitrification—a significant cause of oxygen depletion under winter ice. Can J Fish Aquat Sci 44:743–749
Lehmann MF, Bernasconi SM, Barbieri A, McKenzie JA (2002) Preservation of organic matter and alteration of its carbon and nitrogen isotope composition during simulated and in situ early sedimentary diagenesis. Geochim Cosmochim Acta 66:3573–3584
Massé S (2014) Dynamique saisonnière des communautés nitrifiantes dans un petit lac oligotrophe. Dissertation, Université de Montréal. https://papyrus.bib.umontreal.ca
McIlvin MR, Altabet MA (2005) Chemical conversion of nitrate and nitrite to nitrous oxide for nitrogen and oxygen isotopic analysis in freshwater and seawater. Anal Chem 77:5589–5595
McMeekin K (2009) Le bilan de phosphore du lac Bromont : vers l’identification des activités humaines causant les blooms de cyanobactéries. Dissertation, Université du Québec à Montréal http://www.lacbromont.ca/recherches-et-eacutetudes.html
Monchamp M-E (2013) Rôle de l’azote dans la structure et la fonction des communautés de cyanobactéries toxiques. Dissertation, Université de Montréal https://papyrus.bib.umontreal.ca
Monchamp M-E, Pick FR, Beisner BE, Maranger R (2014) Nitrogen forms influence microcystin concentration and composition via changes in cyanobacterial community structure. PLoS ONE. doi:10.1371/e85573
Pannard A, Beisner BE, Bird DF, Braun J, Planas D, Bormans M (2011) Recurrent internal waves in a small lake: potential ecological consequences for metalimnetic phytoplankton populations. Limnol Oceanogr 1:91–109
Pedneault E, Galand PE, Potvin M, Tremblay J-É, Lovejoy C (2014) Archaeal amoA and ureC genes and their transcriptional activity in the Arctic. Ocean Sci Rep. doi:10.1038/srep04661
Planas D, Vanier C (2014a) Le programme de recherche sur les cyanobactéries au lac Bromont: cahier 9, synthèse, conclusions et recommandations. Université du Québec à Montréal. http://www.lacbromont.ca/recherches-et-eacutetudes.html. Accessed 24 May 2015
Planas D, Vanier C (2014b) Le programme de recherche sur les cyanobactéries au lac Bromont: cahier 7, étude pendant la période libre de glace de 2010. Université du Québec à Montréal. http://www.lacbromont.ca/recherches-et-eacutetudes.html. Accessed 24 May 2015
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 13 Sept 2016
Ryabenko E, Altabet MA, Wallace DWR (2009) Effect of chloride on the chemical conversion of nitrate to nitrous oxide for δ15N analysis. Limnol Oceanogr Meth 7:545–552
Seitzinger S et al (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16:2064–2090
Sigman DM, Granger J, DiFiore PJ, Lehmann MM, Ho R, Cane G, van Geen A (2005) Coupled nitrogen and oxygen isotope measurements of nitrate along the eastern North Pacific margin. Glob Biogeochem Cycle. doi:10.1029/2005gb002458
Sigman DM, Karsh KL, Casciotti KL (2009) Ocean progress tracers: nitrogen isotopes in the ocean. In: Steele JH, Turekian KK, Thorpe SA (eds) Encyclopedia of ocean science, 2nd edn. Elsevier, Amsterdam, pp 4138–4153
Small GE et al (2013) Rates and controls of nitrification in a large oligotrophic lake. Limnol Oceanogr 58:276–286
Soued C, del Giorgio PA, Maranger R (2016) Nitrous oxide sinks and emissions in boreal aquatic networks in Quebec. Nat Geosci 9:116–120
Taranu ZE et al (2015) Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the Anthropocene. Ecol Lett 18:375–384
Thibodeau B, Hélie J-F, Lehmann MF (2013) Variations of the nitrate isotopic composition in the St. Lawrence River caused by seasonal changes in atmospheric nitrogen inputs. Biogeochemistry 115:287–298
Vissers EW, Anselmetti FS, Bodelier PLE, Muyzer G, Schleper C, Tourna M, Laanbroek HJ (2013) Temporal and spatial coexistence of archaeal and bacterial amoA genes and gene transcripts in Lake Lucerne. Archaea. doi:10.1155/2013/289478
Wankel SD, Kendall C, Pennington JT, Chavez FP, Paytan A (2007) Nitrification in the euphotic zone as evidenced by nitrate dual isotopic composition: observations from Monterey Bay. Global Biogeochem Cycles, California. doi:10.1029/2006gb002723
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, San Diego, pp 199–261
Ward BB (2011) Measurement and distribution of nitrification rates in the oceans. In: Martin GK (ed) Methods in enzymology. Academic Press, London, pp 307–323
Wenk CB, Zopfi J, Gardner WS, McCarthy MJ, Niemann H, Veronesi M, Lehmann MF (2014) Partitioning between benthic and pelagic nitrate reduction in the Lake Lugano south basin. Limnol Oceanogr 59:1421–1433
Yool A, Martin AP, Fernandez C, Clark DR (2007) The significance of nitrification for oceanic new production. Nature 447:999–1002
Zhang L, Altabet MA, Wu TX, Hadas O (2007) Sensitive measurement of NH4 + 15N/14N (δ15NH4 +) at natural abundance levels in fresh and saltwaters. Anal Chem 79:5297–5303
Acknowledgements
We thank Marie-Ève Monchamp, Stéphanie Massé, Supriya Tandan, Dan Nguyen and Katherine Velghe for field assistance, Jen Larkum and Jean-François Hélie for stable isotopes measurements. We also thank two anonymous reviewers and Emily H. Stanley for insightful comments. This project was supported by the Fonds de recherche du Québec—Nature et technologies (FRQNT) Team grant to RM, an FQRNT travel award and GRIL support to MB, a National Sciences and Engineering Research Council of Canada (NSERC) grants to RM and IGE.
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Botrel, M., Bristow, L.A., Altabet, M.A. et al. Assimilation and nitrification in pelagic waters: insights using dual nitrate stable isotopes (δ15N, δ18O) in a shallow lake. Biogeochemistry 135, 221–237 (2017). https://doi.org/10.1007/s10533-017-0369-y
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DOI: https://doi.org/10.1007/s10533-017-0369-y