Abstract
Nitrite (NO2 −) is an intermediate in a variety of soil N cycling processes. However, NO2 − dynamics are often not included in studies that explore the N cycle in soil. Within the presented study, nitrite dynamics were investigated in a Nothofagus betuloides forest on an Andisol in southern Chile. We carried out a 15N tracing study with six 15N labeling treatments, including combinations of NO3 −, NH4 + and NO2 −. Gross N transformation rates were quantified with a 15N tracing model in combination with a Markov chain Monte Carlo optimization routine. Our results indicate the occurrence of functional links between (1) NH4 + oxidation, the main process for NO2 − production (nitritation), and NO2 − reduction, and (2) oxidation of soil organic N, the dominant NO3 − production process in this soil, and dissimilatory NO3 − reduction to NH4 + (DNRA). The production of NH4 + via DNRA was approximately ten times higher than direct mineralization from recalcitrant soil organic matter. Moreover, the rate of DNRA was several magnitudes higher than the rate of other NO3 − reducing processes, indicating that DNRA is able to outcompete denitrification, which is most likely not an important process in this ecosystem. These functional links are most likely adaptations of the microbial community to the prevailing pedo-climatic conditions of this Nothofagus ecosystem.
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Abbreviations
- Anammox:
-
Anaerobic ammonium oxidation
- DNRA:
-
Dissimilatory nitrate reduction to ammonium
- GWC:
-
Gravimetric water content
- MCMC:
-
Markov chain Monte Carlo
- MOM:
-
Macro organic matter
- PDF:
-
Parameter density function
- SOM:
-
Soil organic matter
- WFPS:
-
Water filled pore space
References
Azhar ES, Verhe R, Proot M, Sandra P, Verstraete E (1986) Binding of nitrite-N on polyphenols during nitrification. Plant Soil 94:369–382. doi:10.1007/BF02374331
Bengtsson G, Bergwall C (2000) Fate of 15N labelled nitrate and ammonium in a fertilized forest soil. Soil Biol Biochem 32:545–557. doi:10.1016/S0038-0717(99)00183-2
Berntson GM, Aber JD (2000) Fast nitrate immobilization in N saturated temperate forest soils. Soil Biol Biochem 32:151–156. doi:10.1016/S0038-0717(99)00132-7
Betlach MR, Tiedje JM (1981) Kinetic explanation for accumulation of nitrite, nitric oxide, and nitrous oxide during bacterial denitrification. Appl Environ Microbiol 42:1074–1084
Booth MS, Stark JM, Rastetter EB (2005) Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol Monogr 75:139–157. doi:10.1890/04-0988
Burger M, Jackson LE (2004) Plant and microbial use and turnover: rapid conversion of nitrate to ammonium in soil with roots. Plant Soil 266:289–301. doi:10.1007/s11104-005-1362-0
Burns LC, Stevens RJ, Laughlin RJ (1995) Determination of the simultaneous production and consumption of soil nitrite using 15N. Soil Biol Biochem 27:839–844. doi:10.1016/0038-0717(94)00219-Q
Burns LC, Stevens RJ, Laughlin RJ (1996) Production of nitrite in soil by simultaneous nitrification and denitrification. Soil Biol Biochem 28:609–616. doi:10.1016/0038-0717(95)00175-1
Burton J, Chen C, Xu Z, Ghadiri H (2007) Gross nitrogen transformations in adjacent native and plantation forests of subtropical Australia. Soil Biol Biochem 39:426–433. doi:10.1016/j.soilbio.2006.08.011
Chalk PM, Smith CJ (1983) Chemodenitrification. In: Freney JR, Simpson JR (eds) Gaseous loss of nitrogen from plant soil systems. Martinus Nijhoff and Dr. W. Junk, Dordrecht, pp 65–89
Cho CM, Mills JG (1979) Kinetic formulation of the denitrification process in soil. Can J Soil Sci 59:249–257
Davidson EA, Keller M, Erickson HE, Verchot LV, Veldkamp E (2000) Testing a conceptual model of soil emissions of nitrous and nitric oxides. Bioscience 50:667–680
Davidson EA, Chorover J, Dail DB (2003) A mechanism of abiotic immobilization of nitrate in forest ecosystems: the ferrous wheel hypothesis. Glob Chang Biol 9:228–236. doi:10.1046/j.1365-2486.2003.00592.x
Davidson EA, Dail DB, Chorover J (2008) Iron interference in the quantification of nitrate in soil extracts and its effect on hypothesized abiotic immobilization of nitrate. Biogeochemistry 90:65–73. doi:10.1007/s10533-10008-19231-10536
Doff Sotta E, Corre MD, Veldkamp E (2008) Differing N status and N retention processes of soils under old-growth lowland forest in Eastern Amazonia, Caxiuanã, Brazil. Soil Biol Biochem 40:740–750. doi:10.1016/j.soilbio.2007.10.009
Doxtader KG, Alexander M (1966) Nitrification by heterotrophic soil microorganisms. Soil Sci Soc Am Proc 30:351–355
Elliott ET, Paustian K, Frey SD (1996) Modeling the measurable or measuring the modelable: a hierarchical approach to isolating meaningful soil organic matter fractionations. In: Powlson DS, Smith P, Smith JU (eds) Evaluation of soil organic matter models using existing long-term datasets. Springer, Berlin, pp 161–179
Eylar OR, Schmidt EL (1959) A survey of heterotrophic micro-organisms from soil for ability to from nitrite and nitrate. J Gen Microbiol 20:473–481
Fahrmeir l Künstler R, Pigeot I, Tutz G (2004) Statistik—Der Weg zur Datenanalyse. Springer, Berlin
Fitzhugh RD, Christenson LM, Lovett GM (2003a) The fate of 15NO2 − tracer in soils under different tree species of the Catskill mountains, New York. Soil Sci Soc Am J 67:1257–1265
Fitzhugh RD, Lovett GM, Venterea RT (2003b) Biotic and abiotic immobilization of ammonium, nitrite, and nitrate in soils developed under different tree species in the Catskill Mountains, New York, USA. Glob Chang Biol 9:1591–1601. doi:10.1046/j.1365-2486.2003.00694.x
Godoy R, Oyarzún CE, Gerding V (2001) Precipitation chemistry in deciduous and evergreen Nothofagus forests of southern Chile under a low-deposition climate. Basic Appl Ecol 2:65–72. doi:10.1078/1439-1791-00037
Grenon F, Bradley RL, Titus BD (2004) Temperature sensitivity of mineral N transformation rates, and heterotrophic nitrification: possible factors controlling the post-disturbance mineral N flush in forest floors. Soil Biol Biochem 36:1465–1474. doi:10.1016/j.soilbio.2004.04.021
Hackl E, Bachmann G, Zechmeister-Boltenstern S (2004) Microbial nitrogen turnover in soils under different types of natural forest. For Ecol Manage 188:101–112. doi:10.1016/j.foreco.2003.07.014
Hart SC, Binkley D, Perry DA (1997) Influence of red alder on soil nitrogen transformations in two conifer forests of contrasting productivity. Soil Biol Biochem 29:1111–1123. doi:10.1016/S0038-0717(97)00004-7
Hassink J (1995) Density fractions of soil macroorganic matter and microbial biomass as predictors of C and N mineralization. Soil Biol Biochem 27:1099–1108. doi:10.1016/0038-0717(95)00027-C
Hauck RD (1982) Nitrogen isotope ratio analysis. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Soil Science Society of America, American Society of Agronomy, Madison, WI, pp 735–779
Holland EA, Dentener FJ, Braswell BH, Sulzman JM (1999) Contemporary and pre-industrial global reactive nitrogen budgets. Biogeochemistry 46:7–43
Huygens D, Boeckx P, Van Cleemput O, Oyarzún CE, Godoy R (2005) Aggregate and soil organic carbon dynamics in South Chilean Andisols. Biogeosciences 2:159–174
Huygens D, Rütting T, Boeckx P, Van Cleemput O, Godoy R, Müller C (2007) Soil nitrogen conservation mechanisms in a pristine south Chilean Nothofagus ecosystem. Soil Biol Biochem 39:2448–2458. doi:10.1016/j.soilbio.2007.04.013
Huygens D, Boeckx P, Templer PH, Paulino L, Van Cleemput O, Oyarzún CE, Müller C, Godoy R (2008) Mechanisms for retention of bioavailable nitrogen in volcanic rainforest soil. Nat Geosci 1:543–548. doi:10.1038/ngeo252
Islam A, Chen D, White RE, Weatherley AJ (2008) Chemical decomposition and fixation of nitrite in acidic pasture soils and implications for measurement of nitrification. Soil Biol Biochem 40:262–265. doi:10.1016/j.soilbio.2007.07.008
IUSS Working Group WRB (2006) World reference base for soil resources. World soil resources report no. 103. FAO, Rome
Kirkham D, Bartholomew WV (1954) Equations for following nutrient transformations in soil, utilizing tracer data. Soil Sci Soc Am Proc 18:33–34
Knowles R (1982) Denitrification. Microbiol Rev 46:43–70
Landi L, Badalucco L, Pomarè F, Nannipieri P (1993) Effectiveness of antibiotics to distinguish the contributions of fungi and bacteria net nitrogen mineralization, nitrification and respiration. Soil Biol Biochem 25:1771–1778. doi:10.1016/0038-0717(93)90182-B
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809. doi:10.1038/nature04983
Linn DM, Doran JW (1984) Effect of water-filled pore space on carbon dioxide and nitrous oxide production in tilled and nontilled soils. Soil Sci Soc Am J 48:1267–1272
Luxhøi J, Nielsen NE, Jensen LS (2003) Influence of 15NH4 +-application on gross N turnover rates in soil. Soil Biol Biochem 35:603–606. doi:10.1016/S0038-0717(03)00002-6
Mary B, Recous S, Robin D (1998) A model for calculating nitrogen fluxes in soil using 15N tracing. Soil Biol Biochem 30:1963–1979. doi:10.1016/S0038-0717(98)00068-6
Marzluf GA (1997) Genetic regulation of nitrogen metabolism in the fungi. Microbiol Mol Biol Rev 61:17–32
Meijboom FW, Hassink J, von Noordwijk M (1995) Density fractionation of soil macroorganic matter using silica suspensions. Soil Biol Biochem 27:1109–1111. doi:10.1016/0038-0717(95)00028-D
Mulder A, Van de Graaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol 16:177–184. doi:10.1111/j.1574-6941.1995.tb00281.x
Müller C, Stevens RJ, Laughlin RJ (2004) A 15N tracing model to analyse N transformations in old grassland soil. Soil Biol Biochem 36:619–632. doi:10.1016/j.soilbio.2003.12.006
Müller C, Stevens RJ, Laughlin RJ (2006) Sources of nitrite in a permanent grassland soil. Eur J Soil Sci 57:337–343. doi:10.1111/j.1365-2389.2005.00769.x (Erratum. Eur J Soil Sci 357:279)
Müller C, Rütting T, Kattge J, Laughlin RJ, Stevens RJ (2007) Estimation of parameters in complex 15N tracing models via Monte Carlo sampling. Soil Biol Biochem 39:715–726. doi:10.1016/j.soilbio.2006.09.021
Mulvaney RL (1996) Nitrogen-inorganic forms. In: Sparks DL (ed) Methods of soil analysis. Soil Science Society of America, American Society of Agronomy, Madison, WI, pp 1123–1184
Nanzyo M, Dahlgren RA, Shoji S (1993) Chemical characteristics of volcanic ash soils. In: Shoji S, Nanzyo M, Dahlgren RA (eds) Volcanic ash soils: genesis, properties and utilization. Elsevier, Amsterdam, The Netherlands, pp 147–187
Nelson DW, Bremner JM (1969) Factors affecting chemical transformations of nitrite in soils. Soil Biol Biochem 1:229–239. doi:10.1016/0038-0717(69)90023-6
Nijburg JW, Laanbroek HJ (1997) The influence of Glyceria maxima and nitrate input on the composition and nitrate metabolism of the dissimilatory nitrate-reducing bacterial community. FEMS Microbiol Ecol 22:57–63. doi:10.1111/j.1574-6941.1997.tb00356.x
Oyarzún CE, Godoy R, de Schrijver A, Staelens J, Lust N (2004) Water chemistry and nutrient budgets in an undisturbed evergreen rainforest of southern Chile. Biogeochemistry 71:107–123. doi:10.1007/s10533-004-4107-x
Parfitt RL, Scott NA, Ross DJ, Salt GJ, Tate KR (2002) Land-use change effects on soil C and N transformations in soils of high N status: comparisons under indigenous forest, pasture and pine plantation. Biogeochemistry 66:203–221. doi:10.1023/B:BIOG.0000005324.37711.63
Paul EA (2007) Soil microbiology, ecology, and biochemistry. Academic Press, Amsterdam
Paul EA, Clark FE (1996) Soil microbiology and biochemistry. Academic Press, San Diego
Pedersen H, Dunkin KA, Firestone MK (1999) The relative importance of autotrophic and heterotrophic nitrification in a conifer forest soil as measured by 15N tracer and pool dilution techniques. Biogeochemistry 44:135–150
Pepper DA, Eliasson PE, McMurtrie RE, Corbeels M, Ågren GI, Strömgren M, Linder S (2007) Simulated mechanisms of soil N feedback on the forest CO2 response. Glob Chang Biol 13:1265–1281. doi:10.1111/j.1365-2486.2007.01342.x
Perakis SS, Hedin LO (2001) Fluxes and fates of nitrogen in soil of an unpolluted old-growth temperate forest, southern Chile. Ecology 82:2245–2260
Pérez CA, Hedin LO, Armesto JJ (1998) Nitrogen mineralization in two unpolluted old-growth forests of contrasting biodiversity and dynamics. Ecosystems 1:361–374. doi:10.1007/s100219900030
Pett-Ridge J, Silver WL, Firestone MK (2006) Redox fluctuations frame microbial community impacts on N-cycling rates in humid tropical forest soil. Biogeochemistry 81:95–110. doi:10.1007/s10533-006-9032-8
Piňeiro G, Oesterheld M, Batista WB (2006) Opposite changes of whole-soil vs. pools C:N ratios: a case of Simpson’s paradox with implications on nitrogen cycling. Glob Chang Biol 12:804–809. doi:10.1111/j.1365-2486.2006.01139.x
Price SJ, Sherlock RR, Kelliher FM, McSeveny TM, Tate KR, Condron LM (2004) Pristine New Zealand forest soil is a strong methane sink. Glob Chang Biol 10:16–26. doi:10.1046/j.1529-8817.2003.00710x
Radcliffe DJ, Gillman GP (1985) Surface charge characteristics of volcanic ash soils from the southern highlands of Papua New Guinea. In: Cadas EF, Yaalon DH (eds) Volcanic soil. Catena, Braunschweig, pp 35–46
Rice EL, Pancholy SK (1972) Inhibition of nitrification by climax ecosystems. Am J Bot 59:1033–1040. doi:10.2307/2441488
Russow R, Sich I, Neue H-U (2000) The formation of the trace gases NO and N2O in soils by the coupled processes of nitrification and denitrification: results of kinetic 15N tracer investigations. Chemosphere Glob Chang Sci 2:359–366. doi:10.1016/S1465-9972(00)00012-X
Rütting T, Müller C (2007) 15N tracing models with a Monte Carlo optimization procedure provide new insights on gross N transformations in soil. Soil Biol Biochem 39:2351–2361. doi:10.1016/j.soilbio.2007.04.006
Rütting T, Müller C (2008) Process-specific analysis of nitrite dynamics in a permanent grassland soil by using a Monte Carlo sampling technique. Eur J Soil Sci 59:208–215. doi:10.1111/j.1365-2389.2007.00976.x
Saghir NS, Mulvaney RL, Azam F (1993) Determination of nitrogen by microdiffusion in mason jars. 1. Inorganic nitrogen in soil extracts. Commun Soil Sci Plant Anal 24:1745–1762
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602. doi:10.1890/03-8002
Schimel JP, Firestone MK, Killham KS (1984) Identification of heterotrophic nitrification in a Sierran forest soil. Appl Environ Microbiol 48:802–806
Shaviv A (1988) Control of nitrification rate by increasing ammonium concentration. Fert Res 17:177–188. doi:10.1007/BF01050278
Silver WL, Herman DJ, Firestone MK (2001) Dissimilatory nitrate reduction to ammonium in upland tropical forest soils. Ecology 82:2410–2416
Silver WL, Thompson AW, Bradbury D, Chapin FS III, Ewel JJ, Firestone MK (2003) Global patterns in dissimilatory nitrate reduction: a latitudinal gradient in nitrogen retention and loss. American Geophysical Union, Fall Meeting abstract B32B-0389
Silver WL, Thompson AW, Reich A, Ewel JJ, Firestone MK (2005) Nitrogen cycling in tropical plantation forests: potential controls on nitrogen retention. Ecol Appl 15:1604–1614. doi:10.1890/04-1322
Skjemstad JO, Spouncer LR, Cowie B, Swift RS (2004) Calibration of the Rothamsted organic carbon turnover model (RothC ver. 26.3), using measurable soil organic carbon pools. Aust J Soil Res 42:79–88. doi:10.1071/SR03013
Smith CJ, Chalk PM (1979) Mineralization of nitrite fixed by soil organic matter. Soil Biol Biochem 11:515–519. doi:10.1016/0038-0717(79)90011-7
Smith RV, Doyle RM, Burns LC, Stevens RJ (1997) A model for nitrite accumulation in soils. Soil Biol Biochem 29:1241–1247. doi:10.1016/S0038-0717(97)00028-X
Smith JU, Smith P, Monaghan R, Macdonald AJ (2002) When is a measured soil organic matter fraction equivalent to a model pool? Eur J Soil Sci 53:405–416. doi:10.1046/j.1365-2389.2002.00458.x
Speir TW, Townsend JA, More RD, Hill LF (1999) Short-lived isotopic method to measure nitrous oxide emissions from a soil under four low-fertility management systems. Soil Biol Biochem 31:1413–1421. doi:10.1016/S0038-0717(99)00061-9
Sprent JI (1987) The ecology of the nitrogen cycle. Cambridge University Press, Cambridge
Stark JM (2000) Nutrient transformations. In: Sala OE, Jackson RB, Mooney HA, Howarth RW (eds) Methods in ecosystem science. Springer, New York, pp 215–234
Stevens RJ, Laughlin RJ (1994) Determining nitrogen-15 nitrite or nitrate by producing nitrous oxide. Soil Sci Soc Am J 58:1108–1116
Stroo HF, Klein TM, Alexander M (1986) Heterotrophic nitrification in an acid forest soil and by an acid-tolerant fungus. Appl Environ Microbiol 52:1107–1111
Tamm CO (1991) Nitrogen in terrestrial ecosystems (Ecological Studies 81). Springer, Berlin
Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA (1982) Denitrification: ecological niches, competition and survival. Antonie van Leeuwenhoek 48:569–583. doi:10.1007/BF00399542
Van Cleemput O, Baert L (1976) Theoretical considerations on nitrite self-decomposition reactions in soils. Soil Sci Soc Am J 40:322–324
Van Cleemput O, Baert L (1984) Nitrite: a key compound in N loss processes under acid conditions? Plant Soil 76:233–241. doi:10.1007/BF02205583
Van Cleemput O, Samater AH (1996) Nitrite in soils: accumulation and role in the formation of gaseous N compounds. Fert Res 45:81–89. doi:10.1007/BF00749884
Venterea RT (2007) Nitrite-driven nitrous oxide production under aerobic soil conditions: kinetics and biochemical controls. Glob Chang Biol 13:1798–1809. doi:10.1111/j.1365-2486.2007.01389.x
Venterea RT, Rolston DE (2000) Mechanisms and kinetics of nitric oxide and nitrous oxide production during nitrification in agricultural soils. Glob Chang Biol 6:303–316. doi:10.1046/j.1365-2486.2000.00309.x
Vitousek PM, Gosz JR, Grier CC, Melillo JM, Reiners WA, Todd RL (1979) Nitrate losses from disturbed ecosystems. Science 204:469–474. doi:10.1126/science.204.4392.469
Wrage N, Velthof GL, Van Beusichem ML, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732. doi:10.1016/S0038-0717(01)00096-7
Zeller B, Recous S, Kunze M, Moukoumi J, Colin-Belgrand M, Bienaimé S, Ranger J, Dambrine E (2007) Imfluence of tree species on gross and net N transformations in forest soil. Ann For Sci 64:151–158. doi:10.1051/forest:2006099
Zimmermann M, Leifeld J, Schmidt MWI, Smith P, Fuhrer J (2006) Measured soil organic matter fractions can be related to pools in the RothC model. Eur J Soil Sci 58:658–667. doi:10.1111/j.1365-2389.2006.00855.x
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Rütting, T., Huygens, D., Müller, C. et al. Functional role of DNRA and nitrite reduction in a pristine south Chilean Nothofagus forest. Biogeochemistry 90, 243–258 (2008). https://doi.org/10.1007/s10533-008-9250-3
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DOI: https://doi.org/10.1007/s10533-008-9250-3