Winter nitrification in ice-covered lakes


Autoři: Emily Cavaliere aff001;  Helen M. Baulch aff001
Působiště autorů: University of Saskatchewan, School of Environment and Sustainability, Global Institute for Water Security, Saskatoon, Saskatchewan, Canada aff001
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224864

Souhrn

With changes in ice cover duration, nutrient loading, and anoxia risk, it is important to understand the mechanisms that control nitrogen cycling and oxygen depletion in lakes through winter. Current understanding is largely limited to description of changes in chemistry, with few measurements of the processes driving winter changes, how they differ across lakes, and how they are impacted by under-ice conditions. Nitrification is a process which consumes oxygen and ammonium (NH4+), and supplies nitrate (NO3). To date, nitrification has been measured under ice cover in only two lakes globally. Here, we used 15NH4+ enrichment to measure rates of pelagic nitrification in thirteen water bodies in two ecozones. Our work demonstrates ecologically important rates of nitrification can occur despite low water temperatures, impacting NH4+, NO3 and, most importantly, oxygen concentrations. However, high rates are not the norm. When, where and why is nitrification important in winter? We found that nitrification rates were highest in a eutrophic lake chain downstream of a wastewater treatment effluent (mean: 226.5 μg N L-1 d-1), and in a semi-saline prairie lake (110.0 μg N L-1 d-1). In the boreal shield, a eutrophic lake had nitrification rates exceeding those of an oligotrophic lake by 6-fold. Supplementing our results with literature data we found NH4+ concentrations were the strongest predictor of nitrification rates across lentic ecosystems in winter. Higher nitrification rates were associated with higher concentrations of NH4+, NO3 and nitrous oxide (N2O). While more work is required to understand the switch between high and low nitrification rates and strengthen our understanding of winter nitrogen cycling, this work demonstrates that high nitrification rates can occur in winter.

Klíčová slova:

Bacterial disk diffusion – Lakes – Nitrates – Oxygen – Ponds – Surface water – Nitrification


Zdroje

1. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science. 2008;320: 889–892. doi: 10.1126/science.1136674 18487183

2. Carpenter SR, Caraco NF, Correll DL, Howarth RW, Sharpley AN, Smith VH, et al. Nonpoint Pollution of surface waters with phosphorus and nitrogen. Ecol Appl. 1998;8: 559–568. doi: 10.1890/1051-0761(1998)008[0559:NPOSWW]2.0.CO;2

3. Leavitt PR, Brock CS, Ebel C, Patoine A. Landscape-scale effects of urban nitrogen on a chain of freshwater lakes in central North America. Limnol Oceanogr. 2006;51: 2262–2277. doi: 10.4319/lo.2006.51.5.2262

4. Ribot M, Martí E, von Schiller D, Sabater F, Daims H, Battin TJ. Nitrogen processing and the role of epilithic biofilms downstream of a wastewater treatment plant. Freshw Sci. 2012;31: 1057–1069. doi: 10.1899/11-161.1

5. Ward BB, Olson RJ, Perry MJ. Microbial nitrification rates in the primary nitrite maximum off southern California. Deep Sea Res Part A Oceanogr Res Pap. 1982;29: 247–255. doi: 10.1016/0198-0149(82)90112-1

6. Powers SM, Baulch HM, Hampton SE, Labou SG, Lottig NR, Stanley EH. Nitrification contributes to winter oxygen depletion in seasonally frozen forested lakes. Biogeochemistry. Springer International Publishing; 2017;136: 1–11. doi: 10.1007/s10533-017-0382-1

7. Magnuson JJ, Beckel AL, Mills K, Brandt SB. Surviving winter hypoxia—behavioral adaptations of fishes in a northern Wisconsin winterkill lake. Environ Biol Fishes. 1985;14: 241–250. doi: 10.1007/bf00002627

8. Kemp MJ, Dodds WK. The influence of ammonium, nitrate, and dissolved oxygen concentrations on uptake, nitrification, and denitrification rates associated with prairie stream substrata. Limnol Oceanogr. 2002;47: 1380–1393. doi: 10.4319/lo.2002.47.5.1380

9. Glibert PM, Wilkerson FP, Dugdale RC, Raven JA, Dupont CL, Leavitt PR, et al. Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions. Limnol Oceanogr. 2016;61: 165–197. doi: 10.1002/lno.10203

10. Allison FE, editor. Nitrification. Developments in soil science. Elsevier; 1973. pp. 230–253. https://doi.org/10.1016/S0166-2481(08)70570-1.

11. Klingensmith KM, Alexander V. Sediment nitrification, denitrification, and nitrous oxide production in a deep arctic lake. Appl Environ Microbiol. 1983;46: 1084–1092. 16346416

12. Wrage N, Velthof GL, Van Beusichem ML, Oenema O. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem. 2001;33: 1723–1732. doi: 10.1016/S0038-0717(01)00096-7

13. Frame CH, Casciotti KL. Biogeochemical controls and isotopic signatures of nitrous oxide production by a marine ammonia-oxidizing bacterium. Biogeosciences. 2010;7: 2695–2709. doi: 10.5194/bg-7-2695-2010

14. Firestone MK, Davidson EA. Microbiological basis of NO and N2O production and consumption in soil. Exchange of trace gases between terrestrial ecosystems and the atmosphere. 1989. pp. 7–21. doi: 10.1017/CBO9781107415324.004

15. Burgin AJ, Hamilton SK. Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ. 2007;5: 89–96. doi: 10.1890/1540-9295(2007)5[89:HWOTRO]2.0.CO;2

16. Ravishankara AR, Daniel JS, Portmann RW. Nitrous Oxide (N2O): The Dominant Ozone-Depleting Substance Emitted in the 21st Century. Science. 2009;326: 123–125. doi: 10.1126/science.1176985 19713491

17. Cavaliere E, Baulch HM. Denitrification under lake ice. Biogeochem Lett. 2018;137: 285–295. doi: 10.1007/s10533-018-0419-0

18. Soued C, del Giorgio PA, Maranger R. Nitrous oxide sinks and emissions in boreal aquatic networks in Québec. Nat Geosci. Springer Nature; 2015;9: 116–120. doi: 10.1038/NGEO2611

19. Powers SM, Labou SG, Baulch HM, Hunt RJ, Lottig NR, Hampton SE, et al. Ice duration drives winter nitrate accumulation in north temperate lakes. Limnol Oceanogr Lett. 2017; 177–186. doi: 10.1002/lol2.10048

20. Hosseini N, Chun KP, Wheater H, Lindenschmidt KE. Parameter Sensitivity of a Surface Water Quality Model of the Lower South Saskatchewan River—Comparison Between Ice-On and Ice-Off Periods. Environ Model Assess. Environmental Modeling & Assessment; 2017;22: 291–307. doi: 10.1007/s10666-016-9541-3

21. Knowles R, Lean DRS. Nitrification: a significant cause of oxygen depletion under winter ice. Can J Fish Aquat Sci. 1987;44: 743–749.

22. Souza AC, Gardner WS, Dunton KH. Rates of nitrification and ammonium dynamics in northeastern Chukchi Sea shelf waters. Deep Res II. Elsevier; 2014;102: 68–76. doi: 10.1016/j.dsr2.2013.12.017

23. Hampton SE, Galloway AWE, Powers SM, Ozersky T, Woo KH, Batt RD, et al. Ecology under lake ice. Ecol Lett. 2017;20: 98–111. doi: 10.1111/ele.12699 27889953

24. Barica J, Mathias JA. Oxygen depletion and winterkill risk in small prairie lakes under extended ice cover. J Fish Res Board Canada. 1979;36: 980–986.

25. Bertilsson S, Burgin A, Carey CC, Fey SB, Grossart H-P, Grubisic LM, et al. The under-ice microbiome of seasonally frozen lakes. Limnol Oceanogr. 2013;58: 1998–2012. doi: 10.4319/lo.2013.58.6.1998

26. Catalan J. Evolution of dissolved and particulate matter during the ice-covered period in a deep, high-mountain lake. Can J Fish Aquat Sci. 1992;49: 945–955. doi: 10.1139/f92-105

27. Merbt SN, Stahl DA, Casamayor EO, Marti E, Nicol GW, Prosser JI. Differential photoinhibition of bacterial and archaeal ammonia oxidation. FEMS Microbiol Lett. 2012;327: 41–46. doi: 10.1111/j.1574-6968.2011.02457.x 22093004

28. Guerrero MA, Jones RD. Photoinhibition of marine nitrifying bacteria. I. Wavelength-dependent response. Mar Ecol Prog Ser. 1996;141: 183–192. doi: 10.3354/meps141183

29. Mathias JA, Barica J. Factors Controlling Oxygen Depletion in Ice-Covered Lakes. Can J Fish Aquat Sci. 1980;37: 185–194. Available: http://www.nrcresearchpress.com/doi/abs/10.1139/f80-024.

30. Rysgaard S, Risgaard-Petersen N, Sloth NP, Jensen K, Nielsen LP, Nielsen P. Oxygen regulation of nitrification and denitrification in sediments. Source Limnol Oceanogr Limnol Ocean. 1994;39: 1643–1652. doi: 10.4319/lo.1994.39.7.1643

31. Stark JM. Modeling the temperature response of nitrification. Biogeochemistry. 1996; 433–445. doi: 10.1007/BF02183035

32. Zeng J, Zhao D, Yu Z, Huang R, Wu QL. Temperature responses of ammonia-oxidizing prokaryotes in freshwater sediment microcosms. PLoS One. 2014;9: 1–9. doi: 10.1371/journal.pone.0100653 24959960

33. Thamdrup B, Fleischer S. Temperature dependence of oxygen respiration, nitrogen mineralization, and nitrification in Arctic sediments. Aquat Microb Ecol. 1998;15: 191–199. doi: 10.3354/ame015191

34. Canelhas MR, Denfeld BA, Weyhenmeyer GA, Bastviken D, Bertilsson S. Methane oxidation at the water-ice interface of an ice-covered lake. Limnol Oceanogr. 2016;61: S78–S90. doi: 10.1002/lno.10288

35. Denfeld BA, Baulch HM, Giorgio PA, Hampton SE, Karlsson J. A synthesis of carbon dioxide and methane dynamics during the ice-covered period of northern lakes. Limnol Oceanogr Lett. 2018; 1–15. doi: 10.1002/lol2.10079

36. Bédard C, Knowles R, Bedard C, Knowles R, Bédard C, Knowles R. Physiology, biochemistry, and specific inhibitors of CH4, NH4+, and CO oxidation by methanotrophs and nitrifiers. Microbiol Rev. 1989;53: 68–84. doi: 0146-0749/89/010068-17 2496288

37. Carini SA, Orcutt BN, Joye SB. Interactions between methane oxidation and nitrification in coastal sediments. Geomicrobiol J. 2003;20: 355–374. doi: 10.1080/01490450390241044

38. Massé S, Botrel M, Walsh DA, Maranger R. Annual nitrification dynamics in a seasonally ice-covered lake. PLoS One. 2019;14: 1–21. doi: 10.1371/journal.pone.0213748 30893339

39. Gu B. Stable isotopes as indicators for seasonally dominant nitrogen cycling processes in a subarctic lake. Int Rev Hydrobiol. 2012;97: 233–243. doi: 10.1002/iroh.201111466

40. Small GE, Bullerjahn GS, Sterner RW, Beall BFN, Brovold S, Finlay JC, et al. Rates and controls of nitrification in a large oligotrophic lake. Limnol Oceanogr. 2013;58: 276–286. https://doi.org/10.4319/lo.2013.58.1.0276.

41. Verpoorter C, Kutser T, Seekell DA, Tranvik LJ. A global inventory of lakes based on high-resolution satellite imagery. Geophys Res Lett. 2014;41: 6396–6402. doi: 10.1002/2014GL060641

42. Ecological Stratification Working Group. A national ecological framework for Canada. Hull, Quebec; 1995. Cat. No. A42-65/1996E; ISBN 0-662-24107-X.

43. Montoya JP, Voss M, Kahler P, Capone DG. A simple, high-precision, high-sensitivity tracer assay for N2 fixation. Appl Environ Microbiol. 1996;62: 986–993. 16535283

44. Peng X, Fuchsman CA, Jayakumar A, Warner MJ, Devol AH, Ward BB. Revisiting nitrification in the Eastern Tropical South Pacific: A focus on controls. J Geophys Res Ocean. 2016;121: 1667–1684. doi: 10.1002/2015JC011455.Received

45. Allan RJ, Roy M. Lake Water Nutrient Chemistry and Chlorophyll a in Pasqua, Echo, Mission, Katepwa, Crooked and Round Lakes on the Qu’Appelle River, Saskatchewan. Regina, (SK): National Water Research Institute, Inland Waters Directorate. 1980. Scientific Series No. 112. Sponsored by Environment Canada.

46. Pomeroy J. W., De Boer D. and Martz L. W. Saskatoon (SK): Hydrology and water resources of Saskatchewan Centre for Hydrology, University of Saskatchewan. 2005. Centre for Hydrology Report 1. Available: http://www.usask.ca/hydrology/reports/CHRpt01_Hydrology-Water-Resources-Sask_Feb05.pdf.

47. Van Der Kamp G, Keir D, Evans MSS. Long-term water level changes in closed-basin lakes of the Canadian prairies. Can Water Resour J. 2008;33: 23–38. doi: 10.4296/cwrj3301023

48. Hosseini N, Johnston J, Lindenschmidt K-E. Impacts of climate change on the water quality of a regulated prairie river. Water. 2017;9: 199. doi: 10.3390/w9030199

49. Kehoe MJ, Chun KP, Baulch HM. Who smells? Forecasting taste and odor in a drinking water reservoir. Environ Sci Technol. American Chemical Society (ACS); 2015;49: 10984–10992. doi: 10.1021/acs.est.5b00979 26266956

50. Elser JJ, Frost P, Kyle M, Urabe J, Andersen T. Effects of light and nutrients on plankton stoichiometry and biomass in a P-limited lake. Hydrobiologia. 2002;481: 101–112. doi: 10.1023/A:1021217221004

51. Schindler DW, Hecky RE, Findlay DL, Stainton MP, Parker BR, Paterson MJ, et al. Eutrophication of lakes cannot be controlled by reducing nitrogen input: Results of a 37-year whole-ecosystem experiment. Proc Natl Acad Sci U S A. 2008;105: 11254–11258. doi: 10.1073/pnas.0805108105 18667696

52. Cole JJ, Caraco NF, Kling GW, Kratz TK. Carbon dioxide supersaturation in the surface waters of lakes. Science. 1994;265: 1568–1570. doi: 10.1126/science.265.5178.1568 17801536

53. Weiss RF, Price BA. Nitrous oxide solubility in water and seawater. Mar Chem. 1980;8: 347–359. Available: http://www.sciencedirect.com/science/article/pii/0304420380900249.

54. Pawlowicz R. Calculating the conductivity of natural waters. Limnol Oceanogr Methods. 2008;6: 489–501. doi: 10.4319/lom.2008.6.489

55. Wilhelm E, Battino R, Wilcock RJ. Low-pressure solubility of gases in liquid water. Chem Rev. 1977;77: 219–262. doi: 10.1021/cr60306a003

56. Carini SA, Joye SB. Nitrification in Mono Lake, California: Activity and community composition during contrasting hydrological regimes. Limnol Oceanogr. 2008;53: 2546–2557. Available: http://www.avto.aslo.info/lo/toc/vol_53/issue_6/2546.pdf.

57. Ward BB. Nitrogen transformations in the Southern California Bight. Deep Sea Res Part A Oceanogr Res Pap. 1987;34: 785–805. doi: 10.1016/0198-0149(87)90037-9

58. Sigman DMM, Altabet M a., Michener R, McCorkle DCC, Fry B, Holmes RMM. Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: an adaptation of the ammonia diffusion method. Mar Chem. 1997;57: 227–242. doi: 10.1016/S0304-4203(97)00009-1

59. Dodds WK, Evans-White MA, Gerlanc NM, Gray L, Gudder DA, Kemp MJ, et al. Quantification of the nitrogen cycle in a prairie stream. Ecosystems. 2000;3: 574–589. doi: 10.1007/s100210000050

60. O’Brien JM, Dodds WK, Wilson KC, Murdock JN, Eichmiller J. The saturation of N cycling in Central Plains streams: 15N experiments across a broad gradient of nitrate concentrations. Biogeochemistry. 2007;84: 31–49. doi: 10.1007/s10533-007-9073-7

61. Andersson M, Brion N, Middelburg J. Comparison of nitrifier activity versus growth in the Scheldt estuary—a turbid, tidal estuary in northern Europe. Aquat Microb Ecol. 2006;42: 149–158.

62. Gribsholt B, Boschker HTS, Struyf E, Andersson M, Tramper A, De Brabandere L, et al. Nitrogen processing in a tidal freshwater marsh: A whole ecosystem 15N labeling study. Limnol Oceanogr. 2005;50: 1945–1959. doi: 10.4319/lo.2005.50.6.1945

63. Carini SA., McCarthy MJ, Gardner WS. An isotope dilution method to measure nitrification rates in the northern Gulf of Mexico and other eutrophic waters. Cont Shelf Res. Elsevier; 2010;30: 1795–1801. doi: 10.1016/j.csr.2010.08.001

64. Sigman DM, Casciotti KL, Andreani M, Barford C, Galanter M, Bohlke JK. A Bacterial Method for the Nitrogen Isotopic Analysis of Nitrate in Seawater and Freshwater. Anal Chem. 2001;73: 4145–4153. doi: 10.1021/ac010088e 11569803

65. R Core Team. R: a language and environment for statistical computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2018. Available: https://www.r-project.org/.

66. Wheeler B, Torchiano M. lmPerm: Permutation tests for linear models [Internet]. Boston, MA: Free Software Foundation, Inc.; 2016. Available: https://cran.r-project.org/package=lmPerm.

67. Young B, Delatolla R, Kennedy K, Laflamme E, Stintzi A. Low temperature MBBR nitrification: Microbiome analysis. Water Res. 2017;111: 224–233. doi: 10.1016/j.watres.2016.12.050 28088719

68. Zhou H, Li X, Xu G, Yu H. Overview of strategies for enhanced treatment of municipal/domestic wastewater at low temperature. Sci Total Environ. Elsevier B.V.; 2018;643: 225–237. doi: 10.1016/j.scitotenv.2018.06.100 29936164

69. Saskatchewan Water Security Agency, Agency SWS. Saskatchewan Water Security Agency Regulations [Internet]. 2015. Available: http://www.publications.gov.sk.ca/freelaw/documents/English/Regulations/Regulations/W8-1R1.pdf

70. Arbabi M, Elzinga J, ReVelle C. The oxygen sag equation: New properties and a linear equation for the critical deficit. Water Resour Res. 1974;10: 921–929. doi: 10.1029/WR010i005p00921

71. Fair GM. The dissolved oxygen sag: An analysis. Sewage Work J. 1939;11: 445–461.

72. Lewis WM, Wurtsbaugh WA, Paerl HW. Rationale for control of anthropogenic nitrogen and phosphorus to reduce eutrophication of inland waters. Environ Sci Technol. 2011;45: 10300–10305. doi: 10.1021/es202401p 22070635

73. Schindler DW. Recent advances in the understanding and management of eutrophication. Limnol Oceanogr. 2006;51: 356–363. doi: 10.4319/lo.2006.51.1_part_2.0356

74. Müller B, Bryant LD, Matzinger A, Wüest A. Hypolimnetic oxygen depletion in eutrophic lakes. Environ Sci Technol. 2012;46: 9964–9971. doi: 10.1021/es301422r 22871037

75. Barica J. Nitrogen regime of shallow eutrophic lakes on the Canadian Prairies. Prog Wat Tech. 1977;8: 313–321.

76. Pernica P, North RL, Baulch HM. In the cold light of day: the potential importance of under-ice convective mixed layers to primary producers. Inl Waters. 2017;7: 138–150.

77. Carlucci AF, McNally PM. Nitrification By Marine Bacteria in Low Concentrations of Substrate and Oxygen. Limnol Oceanogr. 1969;14: 736–739. doi: 10.4319/lo.1969.14.5.0736

78. Goreau TJ, Kaplan WA, Wofsy SC. Production of NO2- and N2O by nitrifying bacteria at reduced concentrations of oxygen. Appl Environ Microbiol. 1980;40: 526–532. Available: http://www.ncbi.nlm.nih.gov/pubmed/16345632%5Cnhttp://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC291617 16345632

79. Cébron A, Garnier J, Billen G. Nitrous oxide production and nitrification kinetics by natural bacterial communities of the lower Seine river (France). Aquat Microb Ecol. 2005;41: 25–38. doi: 10.3354/ame041025

80. McClain ME, Boyer EW, Dent CL, Gergel SE, Grimm NB, Groffman PM, et al. Biogeochemical Hot Spots and Hot Moments at the Interface of Terrestrial and Aquatic Ecosystems. Ecosystems. 2003;6: 301–312. doi: 10.1007/s10021-003-0161-9

81. Lomas MW, Glibert PM. Temperature regulation of nitrate uptake: A novel hypothesis about nitrate uptake and reduction in cool-water diatoms. Limnol Oceanogr. 1999;44: 556–572. doi: 10.4319/lo.1999.44.3.0556

82. Glibert PM, Conley DJ, Fisher TR, Harding LW, Malone TC. Dynamics of the 1990 winter/spring bloom in Chesapeake Bay. Mar Ecol Prog Ser. 1995;122: 27–43. doi: 10.3354/meps122027

83. Seitzinger S, Harrison J a, Böhlke JK, Bouwman AF, Lowrance R, Peterson B, et al. Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl. 2006;16: 2064–2090. doi: 10.1890/1051-0761(2006)016[2064:dalawa]2.0.co;2 17205890

84. Jørgensen KS, Jensen HB, Sørensen J. Nitrous oxide production from nitrification and denitrification in marine sediment at low oxygen concentrations. Can J Microbiol. 1984;30: 1073–1078.

85. Baulch HM, Dillon PJ, Maranger R, Venkiteswaran JJ, Wilson HF, Schiff SL. Night and day: short-term variation in nitrogen chemistry and nitrous oxide emissions from streams. Freshw Biol. 2012;57: 509–525. doi: 10.1111/j.1365-2427.2011.02720.x


Článek vyšel v časopise

PLOS One


2019 Číslo 11