Cited by 333Soil Carbon and Nitrogen DynamicsSoil and Water Nutrient DynamicsPlant nutrient uptake and metabolism

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A mechanism of abiotic immobilization of nitrate in forest ecosystems: the ferrous wheel hypothesis

Davidson, Eric A., Chorover, Jon, Dail, D. Bryan·2003·Global Change Biology

DOI 10.1046/j.1365-2486.2003.00592.x

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Abstract

Forest soils, rather than woody biomass, are the dominant long‐term sink for N in forest fertilization studies and, by inference, for N from atmospheric deposition. Recent evidence of significant abiotic immobilization of inorganic‐N in forest humus layers challenges a previously widely held view that microbial processes are the dominant pathways for N immobilization in soil. Understanding the plant, microbial, and abiotic mechanisms of N immobilization in forest soils has important implications for understanding current and future carbon budgets. Abiotic immobilization of nitrate is particularly perplexing because the thermodynamics of nitrate reduction in soils are not generally favorable under oxic conditions. Here we present preliminary evidence for a testable hypothesis that explains abiotic immobilization of nitrate in forest soils. Because iron (and perhaps manganese) plays a key role as a catalyst, with Fe(II) reducing nitrate and reduced forms of carbon then regenerating Fe(II), we call this ‘the ferrous wheel hypothesis’. After nitrate is reduced to nitrite, we hypothesize that nitrite reacts with dissolved organic matter through nitration and nitrosation of aromatic ring structures, thus producing dissolved organic nitrogen (DON). In addition to ignorance about mechanisms of DON production, little is known about DON dynamics in soil and its fate within ecosystems. Evidence from leaching and watershed studies suggests that DON production and consumption may be largely uncoupled from seasonal biological processes, although biological processes ultimately produce the DOC and reducing power that affect DON formation and the entire N cycle. The ferrous wheel hypothesis includes both biological and abiological processes, but the reducing power of plant‐derived organic matter may build up over seasons and years while the abiotic reduction of nitrate and reaction of organic matter with nitrite may occur in a matter of seconds after nitrate enters the soil solution.

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Liu, S.-R., Berns, A., Vereecken, H., Wu, D., & Brüggemann, N. (2017) · Scientific Reports · doi:10.1038/srep39590 · Cited by 30
The role of gross and net N transformation processes and NH4+ and NO3− immobilization in controlling the mineral N pool of a temperate mixed deciduous forest soil
Vervaet, H., Boeckx, P., Boko, A., van Cleemput, O., & Hofman, G. (2004) · Plant and Soil · doi:10.1023/b:plso.0000047766.16919.5e · Cited by 30
Does soil organic matter variation affect the retention of 15NH4+ and 15NO3− in forest ecosystems?
Zhu, W.-X., & Wang, W.-W. (2011) · doi:10.1016/j.foreco.2010.11.024 · Cited by 29
Mobility of Nitrogen‐15‐Labeled Nitrate and Sulfur‐34‐Labeled Sulfate during Snowmelt
Campbell, J., Mitchell, M., Mayer, B., Groffman, P., & Christenson, L. (2007) · Soil Science Society of America Journal · doi:10.2136/sssaj2006.0283 · Cited by 29
“While this process is poorly understood and its relative importance is unclear, evidence suggests that abiotic NO3 − retention has the potential to rapidly retain large quantities of N in soil (Davidson et al., 2003).”
BackgroundInfluential
Seeps regulate stream nitrate concentration in a forested Appalachian catchment.
O'Driscoll, M., & Dewalle, D. R. (2010) · Journal of Environmental Quality · doi:10.2134/jeq2009.0083 · Cited by 29
Hydrologic and Biogeochemical Drivers of Riparian Denitrification in an Agricultural Watershed
McPhillips, L., Groffman, P., Goodale, C., & Walter, M. (2015) · Water, Air and Soil Pollution · doi:10.1007/s11270-015-2434-2 · Cited by 28
“Several studies have documented rapid biotic and abiotic immobilization of NO3 − and NO2 − into soil organic matter (Berntson and Aber 2000; Davidson et al. 2003; Fitzhugh et al. 2003).”
BackgroundResultInfluential
Nitrogen budgets of urban lawns under three different management regimes in southern California
Wang, W.-W., Haver, D., & Pataki, D. (2014) · Biogeochemistry · doi:10.1007/s10533-013-9942-1 · Cited by 28
“This suggests ‘‘luxury uptake’’ and storage of N by the microbial community when N was supplied in large amount (Fog 1988), or rapid abiotic immobilization of N into mineral soil, which has been reported to occur within minutes to a few hours in many (15)N tracer studies (e.g., Aber et al. 1998; Dail et al. 2001; Davi…”
Background
A Quantitative Model of Soil Organic Matter Accumulation During Floodplain Primary Succession
Bechtold, J., & Naiman, R. (2009) · Ecosystems · doi:10.1007/s10021-009-9294-9 · Cited by 28
Effects of exogenous N and endogenous nutrients on alpine tundra litter decomposition in an area of high nitrogen deposition.
Zhang, Y.-J., Jin, Y.-H., Xu, J.-W., He, H.-S., Tao, Y., Yang, Z.-P., & Bai, Y. (2022) · Science of the Total Environment · doi:10.1016/j.scitotenv.2021.150388 · Cited by 27
Topographic differences in nitrogen cycling mediate nitrogen retention in a subtropical, N-saturated forest catchment
Zhu, J., Jansen-Willems, A., Müller, C., & Dörsch, P. (2021) · doi:10.1016/j.soilbio.2021.108303 · Cited by 27
Effects of Fe oxide on N transformations in subtropical acid soils
Jiang, X.-J., Xin, X., Li, S.-W., Zhou, J., Zhu, T., Müller, C., Cai, Z.-C., & Wright, A. (2015) · Scientific Reports · doi:10.1038/srep08615 · Cited by 27
Development of a Process‐Based N2O Emission Model for Natural Forest and Grassland Ecosystems
Ma, M., Song, C., Fang, H., Zhang, J., Wei, J., Liu, S.-R., Chen, X.-Z., Zhang, K.-R., Yuan, W.-P., & Lu, H. (2022) · Journal of Advances in Modeling Earth Systems · doi:10.1029/2021ms002460 · Cited by 26
Chemical Composition of High Organic Carbon Soil Amendments Affects Fertilizer-Derived N2O Emission and Nitrogen Immobilization in an Oxic Sandy Loam
Wei, J., Reichel, R., Islam, M., Wissel, H., Amelung, W., & Brüggemann, N. (2020) · Frontiers in Environmental Science · doi:10.3389/fenvs.2020.00015 · Cited by 26
Retention of Nitrate-N in Mineral Soil Organic Matter in Different Forest Age Classes
Fuss, C., Lovett, G., Goodale, C., Ollinger, S., Lang, A., & Ouimette, A. (2019) · Ecosystems · doi:10.1007/s10021-018-0328-z · Cited by 26
Simulated Atmospheric Nitrogen Deposition Alters Decomposition of Ephemeral Roots
Sun, T., Dong, L.-L., & Mao, Z. (2015) · Ecosystems · doi:10.1007/s10021-015-9895-4 · Cited by 26
Influence of Dissolved Organic Matter and Invertebrates on the Function of Microbial Films in Groundwater
Cooney, T. J., & Simon, K. (2009) · Microbial Ecology · doi:10.1007/s00248-009-9523-y · Cited by 26
“Abiotic uptake of NO3 − has been observed in soils ([11], but see [9]), but any abiotic uptake would have been equal across our treatments because microcosms were of the same construction, contained the same sediment, and were randomly assigned to treatments.”
Background
Long-term behaviour of 15N in an alpine grassland ecosystem
Gerzabek, M., Haberhauer, G., Stemmer, M., Klepsch, S., & Haunold, E. (2004) · doi:10.1023/b:biog.0000049336.84556.62 · Cited by 26
Machine Learning Models for Predicting the Ammonium Concentration in Alluvial Groundwaters
Perović, M., Šenk, I., Tarjan, L., Obradović, V., & Dimkić, M. A. (2020) · Environmental Modeling & Assessment · doi:10.1007/s10666-020-09731-9 · Cited by 32
Limnology of the Green Lakes Valley: phytoplankton ecology and dissolved organic matter biogeochemistry at a long-term ecological research site
Miller, M. P., & McKnight, D. (2015) · doi:10.1080/17550874.2012.738255 · Cited by 25
“The redox state of quinones has important implications for environmental processes such as metal transport (Davidson et al. 2003) and the formation of disinfection by-products during drinking water treatment (Beggs et al.”
Background
Estimation of Gross Nitrogen Transformations and Nitrogen Retention in Grassland Soils Using FLUAZ
Accoe, F., Boeckx, P., Videla, X., Pino, I., Hofman, G., & van Cleemput, O. (2005) · Soil Science Society of America Journal · doi:10.2136/sssaj2004.0282 · Cited by 25
Inhibition of Extracellular Enzyme Activities in a Forest Soil by Additions of Inorganic Nitrogen
Kang, H., & Lee, D. (2005) · doi:10.1080/00103620500194650 · Cited by 25
“Recently, Davidson et al. (2003) proposed a chemical mechanism for nitrate immobilization in forest ecosystems.”
Background
Do organic amendments improve the synchronism between soil N supply and wheat demand
Pan, F.-F., Yu, W.-T., Ma, Q., Zhou, H., Jiang, C.-M., & Xu, Y.-G. (2018) · Applied Soil Ecology · doi:10.1016/j.apsoil.2018.01.006 · Cited by 24
Reducing N losses through surface runoff from rice-wheat rotation by improving fertilizer management
Cao, Y.-S., Sun, H., Liu, Y.-Q., Fu, Z.-S., Chen, G.-F., Zou, G., & Zhou, S. (2017) · Environmental science and pollution research international · doi:10.1007/s11356-016-8191-y · Cited by 24
Effects of sterilization techniques on chemodenitrification and N2O production in tropical peat soil microcosms
Buessecker, S., Tylor, K. M., Nye, J., Holbert, K., Urquiza-Muñoz, J., Glass, J., Hartnett, H., & Cadillo-Quiroz, H. (2019) · Biogeosciences · doi:10.5194/bg-16-4601-2019 · Cited by 23
“(1) and (2) (Davidson et al., 2003; Kampschreur et al., 2011; Zhu et al., 2013; Zhu-Barker et al., Published by Copernicus Publications on behalf of the European Geosciences Union.”
Background
Nitrogen Fate and Transport in a Conventional Onsite Wastewater Treatment System Installed in a Clay Soil: Experimental Results
Bradshaw, J. K., & Radcliffe, D. (2013) · doi:10.2136/vzj2012.0149 · Cited by 23
“We suspect that redox cycling of iron in the draini eld may have occurred [e.g., “ferrous wheel” mechanism described by Davidson et al. (2003)]; however, we did not have data to support the irondependent pH changes.”
Background
Nutrient dynamics through fine litterfall in three plantations in Sabah, Malaysia, in relation to nutrient supply to surface soil
Inagaki, M., Kamo, K., Titin, J., Jamalung, L., Lapongan, J., & Miura, S. (2010) · Nutrient Cycling in Agroecosystems · doi:10.1007/s10705-010-9364-6 · Cited by 23
“Metallic elements such as Mn and Fe have a positive effect on the decomposition of litter or dissolved organic matter and act like catalysts (Berg et al. 2000; Davidson et al. 2003).”
Background
Litter N retention over winter for a low and a high phenolic species in the alpine tundra
Steltzer, H., & Bowman, W. (2005) · Plant and Soil · doi:10.1007/s11104-005-3100-z · Cited by 23
Rapid immobilisation and leaching of wet-deposited nitrate in upland organic soils.
Evans, C., Norris, D., Ostle, N., Grant, H., Rowe, E., Curtis, C., & Reynolds, B. (2008) · Environmental Pollution · doi:10.1016/j.envpol.2008.06.019 · Cited by 22
“A mechanism for this involving catalysis by iron has been proposed (Dail et al., 2001; Davidson et al., 2003), but has been recently challenged (Colman et al.”
Background
Contrasting patterns and drivers of soil micronutrient availability in paddy and maize fields of eastern China
Peng, Z.-H., Liu, Y., An, Y., Wang, Z., Li, X., Gao, H., Wei, G.-H., & Jiao, S. (2023) · Geoderma · doi:10.1016/j.geoderma.2023.116342 · Cited by 21
Feedbacks and synergism among biogeochemistry, basic ecology, and forest soil science ☆
van Miegroet, H., & Johnson, D. W. (2009) · Forest Ecology and Management · doi:10.1016/j.foreco.2009.02.007 · Cited by 21
Assessing denitrification and N leaching in a field with organic amendments
Radersma, S., & Smit, A. (2011) · NJAS - Wageningen Journal of Life Sciences · doi:10.1016/j.njas.2010.06.001 · Cited by 20
Soil Inorganic N Leaching in Edges of Different Forest Types Subject to High N Deposition Loads
Wuyts, K., Schrijver, A. D., Staelens, J., van Nevel, L., Adriaenssens, S., & Verheyen, K. (2011) · Ecosystems · doi:10.1007/s10021-011-9448-4 · Cited by 20
Dissolved Organic Carbon and Nitrogen in Andisol for Six Crop Rotations with Different Soil Management Intensity
PabloUndurraga, D., Zagal, E., GloriaSepúlveda, W., & NataliaValderrama, V. (2009) · doi:10.4067/s0718-58392009000300018 · Cited by 20
“The highest DON contents in the ecosystems can be related to the indications by Perakis and Hedin (2001) and Davidson et al. (2003) who set out abiotic mechanisms for DON production through a loss of nitrate by reduction and later conversion to DON.”
Background
Evaporation as a nutrient retention mechanism at Sycamore Creek, Arizona
McLaughlin, C. (2008) · Hydrobiologia · doi:10.1007/s10750-007-9275-y · Cited by 20
“, 2003), although the specific mechanism is not completely understood (Berntson & Aber, 2000; Dail et al., 2001; Davidson et al., 2003; Hungtington, 2005).”
Background
Synthesizing redox biogeochemistry at aquatic interfaces
Lau, M. P., Niederdorfer, R., Sepulveda‐Jauregui, A., & Hupfer, M. (2017) · Limnologica · doi:10.1016/j.limno.2017.08.001 · Cited by 20
“In general, Fe(II) Fe(III) redox reactions are reported to run on many different abiotic and microbial mediated pathways (see the comprehensive review by Melton et al., 2014) and led to the hypothesis of a “ferrous wheel”, initially brought forward by Davidson et al. (2003).”
Background
Abiotic nitrate loss and nitrogenous trace gas emission from Chinese acidic forest soils
Wang, Y.-J., Cao, W.-C., Zhang, X.-M., & Guo, J.-H. (2017) · Environmental science and pollution research international · doi:10.1007/s11356-017-9797-4 · Cited by 19
Retention of surface nitrate additions in a temperate old field: implications for atmospheric nitrogen deposition over winter and plant nitrogen availability
Joseph, G., & Henry, H. A. L. (2009) · Plant and Soil · doi:10.1007/s11104-008-9862-3 · Cited by 19
“Although abiotic nitrate retention can also reduce nitrate mobility during spring melt (Davidson et al. 2003; Campbell et al. 2007), this mechanism did not appear to contribute substantially to nitrate retention in our system, given that little of the 15N label was recovered in the soil extracts.”
Background
Abiotic immobilization of nitrate in two soils of relic Abies pinsapo-fir forests under Mediterranean climate
Torres-Cañabate, P., Davidson, E., Bulygina, E., García-Ruiz, R., & Carreira, J. (2008) · doi:10.1007/s10533-008-9255-y · Cited by 19
Self-citation
Long-term N and S addition and changed litter chemistry do not affect trembling aspen leaf litter decomposition, elemental composition and enzyme activity in a boreal forest
Wang, Q., Kwak, J., Choi, W., & Chang, S. X. (2019) · Environmental Pollution · doi:10.1016/j.envpol.2019.04.007 · Cited by 18
Variability in Soil Nitrogen Retention Across Forest, Urban, and Agricultural Land Uses
Weitzman, J., & Kaye, J. (2016) · Ecosystems · doi:10.1007/s10021-016-0007-x · Cited by 18
Manure increase the leaching risk of soil extractable organic nitrogen in intensively irrigated greenhouse vegetable cropping systems
Quan, Z., Lu, C.-Y., Shi, Y., Chen, X., Huang, B., Wang, Y.-Z., Zhao, Y.-J., & Ma, J. (2015) · doi:10.1080/09064710.2014.990501 · Cited by 18
“N into N-rich dissolved organic matter (Berntson & Aber 2000; Davidson et al. 2003; Fang et al. 2009).”
Background
The fate of 15NH4+ labeled deposition in a Scots pine forest in the Netherlands under high and lowered NH4+ deposition, 8 years after application
Wessel, W., Tietema, A., & Boxman, A. W. (2013) · Biogeochemistry · doi:10.1007/s10533-012-9775-3 · Cited by 18
“…N deposition include soil microbial uptake (Zak et al. 2004), uptake by mosses (Friedrich et al. 2011), abiotic fixation of NO3 - (Aber et al. 1998; Davidson et al. 2003, 2008; but see Colman et al. 2007), and immobilization into carbon (C) compounds from mycorrhiza (Aber et al. 1998; Frey et al.…”
Background
Abiotic reaction of nitrite with dissolved organic carbon? Testing the Ferrous Wheel Hypothesis
Schmidt, B. H. M., & Matzner, E. (2009) · doi:10.1007/s10533-009-9290-3 · Cited by 18
“Davidson et al. (2003) showed that NO2 - as highly”
BackgroundInfluential
Nitrogen and calcium additions increase forest growth in northeastern USA spruce–fir forests
Kulmatiski, A., Vogt, K. A., Vogt, D., Wargo, P. M., Tilley, J., Siccama, T., Sigurdardottir, R., & Ludwig, D. (2007) · doi:10.1139/x07-040 · Cited by 18
“Interestingly, greater soil C storage is expected to slow the effects of N saturation because it may abiotically immobilize N (Davidson et al. 2003).”
Background
Gaseous Nitrogen Losses from Coastal Acid Sulfate Soils: A Short-Term Study
Macdonald, B., Denmead, O., White, I., & Byrant, G. (2011) · Pedosphere · doi:10.1016/s1002-0160(11)60118-5 · Cited by 17
Nitrogen Cycling and Mass Balance for a Forested Catchment in the Italian Alps. Assessment of Nitrogen Status
Balestrini, R., Martino, N. A. E. D., & van Miegroet, H. (2006) · doi:10.1007/s10533-005-3429-7 · Cited by 17
“There is also increasing evidence of abiotic N-NO3 immobilisation process in forest soils (Johnson et al 2000; Davidson et al. 2003 ), or abiotic transformation of N-NO3 into dissolved organic N in organic horizons of Harvard Forest, USA (Dail et al. 2001) and of temperate forests in Chile (Perakis and Hedin”
Background

Authors: Davidson, E. A., Chorover, J., & Dail, D. B.
Affiliations: Woodwell Climate Research Center (US)
University of Arizona (US)
University of Maine (US)
Corresponding author: Davidson, Eric A.
ORCID: Davidson, Eric A.
Chorover, Jon
Venue: Global Change Biology
Publisher: Wiley
Published: 2003-02
Volume: 9
Issue: 2
Pages: 228-236
ISSN: 1354-1013 (ISSN-L)
1365-2486
DOI: 10.1046/j.1365-2486.2003.00592.x
OpenAlex: W2145062256
Cited by: 333
References: 65
Citations by year: 2026: 6 · 2025: 8 · 2024: 6 · 2023: 12 · 2022: 8 · 2021: 15 · 2020: 12 · 2019: 16 · 2018: 14 · 2017: 17 · 2016: 20 · 2015: 18 · 2014: 13 · 2013: 11 · 2012: 14
FWCI: 29.82
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 4 d)
Locations: Global Change Biology (publishedVersion)
Funders: National Science Foundation
Pennsylvania State University
Topics: Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
Physical Sciences › Environmental Science › Environmental Chemistry › Soil and Water Nutrient Dynamics
Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
Keywords: forest soils, dissolved organic nitrogen, dissolved organic matter, nitrogen cycling, forest humus, atmospheric nitrogen deposition

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A mechanism of abiotic immobilization of nitrate in forest ecosystems: the ferrous wheel hypothesis

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