Abstract
Understanding the processes controlling organic matter (OM) stocks in upland soils, and the ability to management them, is crucial for maintaining soil fertility and carbon (C) storage as well as projecting change with time. OM inputs are balanced by the mineralization (oxidation) rate, with the difference determining whether the system is aggrading, degrading or at equilibrium with reference to its C storage. In upland soils, it is well recognized that the rate and extent of OM mineralization is affected by climatic factors (particularly temperature and rainfall) in combination with OM chemistry, mineral–organic associations, and physical protection. Here we examine evidence for the existence of persistent anaerobic microsites in upland soils and their effect on microbially mediated OM mineralization rates. We corroborate long-standing assumptions that residence times of OM tend to be greater in soil domains with limited oxygen supply (aggregates or peds). Moreover, the particularly long residence times of reduced organic compounds (e.g., aliphatics) are consistent with thermodynamic constraints on their oxidation under anaerobic conditions. Incorporating (i) pore length and connectivity governing oxygen diffusion rates (and thus oxygen supply) with (ii) ‘hot spots’ of microbial OM decomposition (and thus oxygen consumption), and (iii) kinetic and thermodynamic constraints on OM metabolism under anaerobic conditions will thus improve conceptual and numerical models of C cycling in upland soils. We conclude that constraints on microbial metabolism induced by oxygen limitations act as a largely unrecognized and greatly underestimated control on overall rates of C oxidation in upland soils.
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Abbreviations
- fanaerobic :
-
‘Anaerobic fraction’, anaerobic proportion of the overall pore space
- roxygen :
-
Scaling factor that describes the effect of oxygen limitations on overall OM oxidation rates (ranges from 0 to 1)
- Ft :
-
Thermodynamic driving force for the oxidation of a carbon compound coupled to the reduction of a given terminal electron acceptor. It varies from 0 (reaction inhibited) to 1 (reaction occurs at maximum rates) and can be estimated based on NOSC
- NOSC:
-
Nominal oxidation state of carbon can be calculated for any given compound based on its stoichiometry (LaRowe and Van Cappellen 2011)
References
Amelung W, Kaiser K, Kammerer G, Sauer G (2002) Organic carbon at soil particle surfaces—evidence from X-ray photoelectron spectroscopy and surface abrasion. Soil Sci Soc Am J 66:1526–1530
Andersen BL, Bidoglio G, Leip A, Rembges D (1998) A new method to study simultaneous methane oxidation and methane production in soils. Glob Biogeochem Cycles 12:587–594. doi:10.1029/98GB01975
Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862. doi:10.1038/ismej.2011.141
Arah JRM, Smith KA (1989) Steady-state denitrification in aggregated soils: a mathematical model. J Soil Sci 40:139–149. doi:10.1111/j.1365-2389.1989.tb01262.x
Arah JRM, Vinten AJA (1995) Simplified models of anoxia and denitrification in aggregated and simple-structured soils. Eur J Soil Sci 46:507–517. doi:10.1111/j.1365-2389.1995.tb01347.x
Arndt S, Jørgensen BB, LaRowe DE et al (2013) Quantifying the degradation of organic matter in marine sediments: a review and synthesis. Earth Sci Rev 123:53–86. doi:10.1016/j.earscirev.2013.02.008
Bailey VL, Bilskis CL, Fansler SJ et al (2012) Measurements of microbial community activities in individual soil macroaggregates. Soil Biol Biochem 48:192–195. doi:10.1016/j.soilbio.2012.01.004
Baldock JA, Skjemstad JO (2000) Role of the soil matrix and minerals in protecting natural organic materials against biological attack. Org Geochem 31:697–710
Baldock JA, Oades JM, Waters AG et al (1992) Aspects of the chemical structure of soil organic materials as revealed by solid-state 13C NMR spectroscopy. Biogeochemistry 16:1–42. doi:10.1007/BF02402261
Bartlett RJ (1988) Manganese redox reactions and organic interactions in soils. In: Graham RD, Hannam RJ, Uren NC (eds) Manganese in soils and plants. Springer, Dordrecht, pp 59–73
Bidel LPR, Renault P, Pagès L, Rivière LM (2000) Mapping meristem respiration of Prunus persica (L.) Batsch seedlings: potential respiration of the meristems, O2 diffusional constraints and combined effects on root growth. J Exp Bot 51:755–768. doi:10.1093/jexbot/51.345.755
Bridge BJ, Rixon AJ (1976) Oxygen uptake and respiratory quotient of field soil cores in relation to their air-filled pore space. J Soil Sci 27:279–286
Bundt M, Jäggi M, Blaser P et al (2001a) Carbon and nitrogen dynamics in preferential flow paths and matrix of a forest soil. Soil Sci Soc Am J 65:1529–1538
Bundt M, Widmer F, Pesaro M et al (2001b) Preferential flow paths: biological “hot spots” in soils. Soil Biol Biochem 33:729–738. doi:10.1016/S0038-0717(00)00218-2
Castelle CJ, Hug LA, Wrighton KC et al (2013) Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment. Nat Commun. doi:10.1038/ncomms3120
Chacon N, Silver WL, Dubinsky EA, Cusack DF (2006) Iron reduction and soil phosphorus solubilization in humid tropical forests soils: the roles of labile carbon pools and an electron shuttle compound. Biogeochemistry 78:67–84. doi:10.1007/s10533-005-2343-3
Claypool GE, Kaplan IR (1974) The origin and distribution of methane in marine sediments. In: Kaplan IR (ed) Natural gases in marine sediments. Springer, New York, pp 99–139
Clemente JS, Simpson AJ, Simpson MJ (2011) Association of specific organic matter compounds in size fractions of soils under different environmental controls. Org Geochem 42:1169–1180. doi:10.1016/j.orggeochem.2011.08.010
Cotrufo MF, Wallenstein MD, Boot CM et al (2013) The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Change Biol 19:988–995. doi:10.1111/gcb.12113
Currie J (1961) Gaseous diffusion in the aeration of aggregated soils. Soil Sci 92:40–45
Currie JA (1984) Gas diffusion through soil crumbs: the effects of compaction and wetting. J Soil Sci 35:1–10. doi:10.1111/j.1365-2389.1984.tb00253.x
Davidson EA, Samanta S, Caramori SS, Savage K (2012) The dual Arrhenius and Michaelis–Menten kinetics model for decomposition of soil organic matter at hourly to seasonal time scales. Glob Change Biol 18:371–384. doi:10.1111/j.1365-2486.2011.02546.x
De Gryze S, Jassogne L, Six J et al (2006) Pore structure changes during decomposition of fresh residue: X-ray tomography analyses. Geoderma 134:82–96. doi:10.1016/j.geoderma.2005.09.002
De-Campos AB, Huang C, Johnston CT (2011) Biogeochemistry of terrestrial soils as influenced by short-term flooding. Biogeochemistry 111:239–252. doi:10.1007/s10533-011-9639-2
Devêvre OC, Horwáth WR (2000) Decomposition of rice straw and microbial carbon use efficiency under different soil temperatures and moistures. Soil Biol Biochem 32:1773–1785. doi:10.1016/S0038-0717(00)00096-1
Ewing SA, Sanderman J, Baisden WT et al (2006) Role of large-scale soil structure in organic carbon turnover: evidence from California grassland soils. J Geophys Res Biogeosci. doi:10.1029/2006JG000174
Fan Z, Neff JC, Waldrop MP et al (2014) Transport of oxygen in soil pore–water systems: implications for modeling emissions of carbon dioxide and methane from peatlands. Biogeochemistry. doi:10.1007/s10533-014-0012-0
Fiedler S, Kalbitz K (2003) Concentrations and properties of dissolved organic matter in forest soils as affected by the redox regime. Soil Sci 168:793–801
Fiedler S, Vepraskas MJ, Richardson JL (2007) Soil redox potential: importance, field measurements, and observations. In: Sparks DL (ed) Advances in agronomy. Academic, San Diego, pp 1–54
Fimmen RL Jr, de Richter DB, Vasudevan D et al (2008) Rhizogenic Fe–C redox cycling: a hypothetical biogeochemical mechanism that drives crustal weathering in upland soils. Biogeochemistry 87:127–141. doi:10.1007/s10533-007-9172-5
Fischer WR, Flessa H, Schaller G (1989) pH values and redox potentials in microsites of the rhizosphere. Z Pflanzenernaehr Bodenk 152:191–195. doi:10.1002/jpln.19891520209
Frank D, Reichstein M, Bahn M et al (2015) Effects of climate extremes on the terrestrial carbon cycle: concepts, processes and potential future impacts. Glob Change Biol. doi:10.1111/gcb.12916
Freeman C, Ostle N, Kang H (2001) An enzymic “latch” on a global carbon store. Nature 409:149–149. doi:10.1038/35051650
Froelich PN, Klinkhammer GP, Bender ML et al (1979) Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis. Geochim Cosmochim Acta 43:1075–1090. doi:10.1016/0016-7037(79)90095-4
Frolking S, Roulet NT, Moore TR et al (2001) Modeling northern peatland decomposition and peat accumulation. Ecosystems 4:479–498. doi:10.1007/s10021-001-0105-1
Fuss CB, Driscoll CT, Johnson CE et al (2010) Dynamics of oxidized and reduced iron in a northern hardwood forest. Biogeochemistry 104:103–119. doi:10.1007/s10533-010-9490-x
Glissmann K, Conrad R (2002) Saccharolytic activity and its role as a limiting step in methane formation during the anaerobic degradation of rice straw in rice paddy soil. Biol Fertil Soils 35:62–67. doi:10.1007/s00374-002-0442-z
Greenwood DJ (1961) The effect of oxygen concentration on the decomposition of organic materials in soil. Plant Soil 14:360–376. doi:10.1007/BF01666294
Greve P, Orlowsky B, Mueller B et al (2014) Global assessment of trends in wetting and drying over land. Nat Geosci 7:716–721. doi:10.1038/ngeo2247
Hall SJ, McDowell WH, Silver WL (2013) When wet gets wetter: decoupling of moisture, redox biogeochemistry, and greenhouse gas fluxes in a humid tropical forest soil. Ecosystems 16:576–589. doi:10.1007/s10021-012-9631-2
Hall SJ, Treffkorn J, Silver WL (2014) Breaking the enzymatic latch: impacts of reducing conditions on hydrolytic enzyme activity in tropical forest soils. Ecology 95:2964–2973. doi:10.1890/13-2151.1
Hansel CM, Fendorf S, Jardine PM, Francis CA (2008) Changes in cacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl Environ Microbiol 74:1620–1633. doi:10.1128/AEM.01787-07
Hartnett HE, Keil RG, Hedges JI, Devol AH (1998) Influence of oxygen exposure time on organic carbon preservation in continental margin sediments. Nature 391:572–575. doi:10.1038/35351
Hedges JI, Keil RG (1995) Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar Chem 49:81–115. doi:10.1016/0304-4203(95)00008-F
Hojberg O, Sorensen J (1993) Microgradients of microbial oxygen consumption in a barley rhizosphere model system. Appl Environ Microbiol 59:431–437
Hong H, Gu Y, Yin K et al (2010) Red soils with white net-like veins and their climate significance in south China. Geoderma 160:197–207. doi:10.1016/j.geoderma.2010.09.019
Jacobs PM, West LT, Shaw JN (2002) Redoximorphic features as indicators of seasonal saturation, Lowndes County, Georgia. Soil Sci Soc Am J 66:315–323
Jarvis NJ (2007) A review of non-equilibrium water flow and solute transport in soil macropores: principles, controlling factors and consequences for water quality. Eur J Soil Sci 58:523–546. doi:10.1111/j.1365-2389.2007.00915.x
Jin Q, Bethke CM (2003) A new rate law describing microbial respiration. Appl Environ Microbiol 69:2340–2348. doi:10.1128/AEM.69.4.2340-2348.2003
Kane ES, Chivers MR, Turetsky MR et al (2013) Response of anaerobic carbon cycling to water table manipulation in an Alaskan rich fen. Soil Biol Biochem 58:50–60. doi:10.1016/j.soilbio.2012.10.032
Keiluweit M, Bougoure JJ, Nico PS et al (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Change 5:588–595. doi:10.1038/nclimate2580
Kelleher BP, Simpson MJ, Simpson AJ (2006) Assessing the fate and transformation of plant residues in the terrestrial environment using HR-MAS NMR spectroscopy. Geochim Cosmochim Acta 70:4080–4094. doi:10.1016/j.gca.2006.06.012
Killham K, Amato M, Ladd JN (1993) Effect of substrate location in soil and soil pore–water regime on carbon turnover. Soil Biol Biochem 25:57–62
Klotzbücher T, Kaiser K, Guggenberger G et al (2011) A new conceptual model for the fate of lignin in decomposing plant litter. Ecology 92:1052–1062. doi:10.1890/10-1307.1
Köchy M, Hiederer R, Freibauer A (2015) Global distribution of soil organic carbon—Part 1: masses and frequency distributions of SOC stocks for the tropics, permafrost regions, wetlands, and the world. SOIL 1:351–365. doi:10.5194/soil-1-351-2015
Koven CD, Riley WJ, Subin ZM et al (2013) The effect of vertically resolved soil biogeochemistry and alternate soil C and N models on C dynamics of CLM4. Biogeosciences 10:7109–7131. doi:10.5194/bg-10-7109-2013
LaRowe DE, Van Cappellen P (2011) Degradation of natural organic matter: a thermodynamic analysis. Geochim Cosmochim Acta 75:2030–2042. doi:10.1016/j.gca.2011.01.020
Lee CG, Watanabe T, Murase J et al (2012) Growth of methanogens in an oxic soil microcosm: elucidation by a DNA-SIP experiment using 13C-labeled dried rice callus. Appl Soil Ecol 58:37–44. doi:10.1016/j.apsoil.2012.03.002
Leschine SB (1995) Anaerobic cellulose degradation. Annu Rev Microbiol 49:399–426
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. doi:10.2136/sssaj1984.03615995004800060013x
Liptzin D, Silver WL, Detto M (2010) Temporal dynamics in soil oxygen and greenhouse gases in two humid tropical forests. Ecosystems 14:171–182. doi:10.1007/s10021-010-9402-x
Lorenz K, Lal R, Preston CM, Nierop KGJ (2007) Strengthening the soil organic carbon pool by increasing contributions from recalcitrant aliphatic bio(macro)molecules. Geoderma 142:1–10. doi:10.1016/j.geoderma.2007.07.013
Malik AA, Dannert H, Griffiths RI et al (2015) Rhizosphere bacterial carbon turnover is higher in nucleic acids than membrane lipids: implications for understanding soil carbon cycling. Front Microbiol. doi:10.3389/fmicb.2015.00268
Mangalassery S, Sjögersten S, Sparkes DL et al (2013) The effect of soil aggregate size on pore structure and its consequence on emission of greenhouse gases. Soil Tillage Res 132:39–46. doi:10.1016/j.still.2013.05.003
Manzoni S, Schimel JP, Porporato A (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93:930–938
Mateos MP, Carcedo SG (1985) Effect of fractionation on location of enzyme activities in soil structural units. Biol Fertil Soils 1:153–159. doi:10.1007/BF00301783
Megonigal JP, Hines ME, Visscher PT (2003) Anaerobic metabolism: linkages to trace gases and aerobic processes. In: Holland HD, Turekian KK (eds) Treatise on geochemistry. Pergamon, Oxford, pp 317–424
Mikutta R, Kleber M, Torn MS, Jahn R (2006) Stabilization of soil organic matter: association with minerals or chemical recalcitrance? Biogeochemistry 77:25–56. doi:10.1007/s10533-005-0712-6
Miller AJ, Schuur EAG, Chadwick OA (2001) Redox control of phosphorus pools in Hawaiian montane forest soils. Geoderma 102:219–237. doi:10.1016/S0016-7061(01)00016-7
Moyano FE, Manzoni S, Chenu C (2013) Responses of soil heterotrophic respiration to moisture availability: an exploration of processes and models. Soil Biol Biochem 59:72–85. doi:10.1016/j.soilbio.2013.01.002
Myrold DD, Tiedje JM (1985) Diffusional constraints on denitrification in soil. Soil Sci Soc Am J 49:651–657
Navarro-García F, Casermeiro MÁ, Schimel JP (2012) When structure means conservation: effect of aggregate structure in controlling microbial responses to rewetting events. Soil Biol Biochem 44:1–8. doi:10.1016/j.soilbio.2011.09.019
Nielson KK, Rogers VC, Gee GW (1984) Diffusion of radon through soils: a pore distribution model1. Soil Sci Soc Am J 48:482. doi:10.2136/sssaj1984.03615995004800030002x
Oades JM (1988) The retention of organic matter in soils. Biogeochemistry 5:35–70. doi:10.1007/BF02180317
Parr JF, Reuszer HW (1962) Organic matter decomposition as influenced by oxygen level and flow rate of gases in the constant aeration method1. Soil Sci Soc Am J 26:552. doi:10.2136/sssaj1962.03615995002600060012x
Peters V, Conrad R (1995) Methanogenic and other strictly anaerobic bacteria in desert soil and other oxic soils. Appl Environ Microbiol 61:1673–1676
Pisani O, Hills KM, Courtier-Murias D et al (2014) Accumulation of aliphatic compounds in soil with increasing mean annual temperature. Org Geochem 76:118–127. doi:10.1016/j.orggeochem.2014.07.009
Poplawski AB, Mårtensson L, Wartiainen I, Rasmussen U (2007) Archaeal diversity and community structure in a Swedish barley field: specificity of the EK510R/(EURY498) 16S rDNA primer. J Microbiol Methods 69:161–173. doi:10.1016/j.mimet.2006.12.018
Postma D, Jakobsen R (1996) Redox zonation: equilibrium constraints on the Fe(III)/SO4–reduction interface. Geochim Cosmochim Acta 60:3169–3175. doi:10.1016/0016-7037(96)00156-1
Reddy KR, Patrick WH Jr (1975) Effect of alternate aerobic and anaerobic conditions on redox potential, organic matter decomposition and nitrogen loss in a flooded soil. Soil Biol Biochem 7:87–94. doi:10.1016/0038-0717(75)90004-8
Reddy KR, D’Angelo EM, Harris WG (2000) Biogeochemistry of wetlands. In: Sumner ME (ed) Handbook of soil science. CRC Press, Boca Raton, pp G89–G119
Reineke W (2001) Aerobic and anaerobic biodegradation potentials of microorganisms. In: Beek B (ed) Biodegradation and persistance. Springer, Berlin, pp 1–161
Richter DD, Oh N-H, Fimmen R, Jackson J (2007) The rhizosphere and soil formation. The rhizosphere: an ecological perspective. Academic, Amsterdam, pp 179–200
Riederer M, Matzke K, Ziegler F, Kögel-Knabner I (1993) Occurrence, distribution and fate of the lipid plant biopolymers cutin and suberin in temperate forest soils. Org Geochem 20:1063–1076. doi:10.1016/0146-6380(93)90114-Q
Rijtema PE, Kroes JG (1991) Some results of nitrogen simulations with the model ANIMO. Fertil Res 27:189–198. doi:10.1007/BF01051127
Riley WJ, Subin ZM, Lawrence DM et al (2011) Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM. Biogeosciences 8:1925–1953. doi:10.5194/bg-8-1925-2011
Riley WJ, Maggi FM, Kleber M et al (2014) Long residence times of rapidly decomposable soil organic matter: application of a multi-phase, multi-component, and vertically-resolved model (TOUGHREACTv1) to soil carbon dynamics. Geosci Model Dev Discuss 7:815–870. doi:10.5194/gmdd-7-815-2014
Roden EE, Sobolev D, Glazer B, Luther GW (2004) Potential for microscale bacterial fe redox cycling at the aerobic–anaerobic interface. Geomicrobiol J 21:379–391. doi:10.1080/01490450490485872
Rumpel C (2004) Location and chemical composition of stabilized organic carbon in topsoil and subsoil horizons of two acid forest soils. Soil Biol Biochem 36:177–190. doi:10.1016/j.soilbio.2003.09.005
Rumpel C, Kögel-Knabner I (2011) Deep soil organic matter—a key but poorly understood component of terrestrial C cycle. Plant Soil 338:143–158. doi:10.1007/s11104-010-0391-5
Rumpel C, Seraphin A, Goebel M-O et al (2004) Alkyl C and hydrophobicity in B and C horizons of an acid forest soil. J Plant Nutr Soil Sci 167:685–692. doi:10.1002/jpln.200421484
Schmidt MWI, Torn MS, Abiven S et al (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56. doi:10.1038/nature10386
Schuur EA, Matson PA (2001) Net primary productivity and nutrient cycling across a mesic to wet precipitation gradient in Hawaiian montane forest. Oecologia 128:431–442. doi:10.1007/s004420100671
Segers R (1998) Methane production and methane consumption: a review of processes underlying wetland methane fluxes. Biogeochemistry 41:23–51. doi:10.1023/A:1005929032764
Sexstone AJ, Revsbech NP, Parkin TB, Tiedje JM (1985) Direct measurement of oxygen profiles and denitrification rates in soil aggregates1. Soil Sci Soc Am J 49:645. doi:10.2136/sssaj1985.03615995004900030024x
Silver WL, Lugo AE, Keller M (1999) Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils. Biogeochemistry 44:301–328. doi:10.1007/BF00996995
Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404. doi:10.1016/j.soilbio.2009.10.014
Skopp J, Jawson MD, Doran JW (1990) Steady-state aerobic microbial activity as a function of soil water content. Soil Sci Soc Am J 54:1619. doi:10.2136/sssaj1990.03615995005400060018x
Smith KA (1977) Soil aeration. Soil Sci 123:284–291
Smith KA (1980) A model of the extent of anaerobic zones in aggregated soils, and its potential application to estimates of denitrification1. J Soil Sci 31:263–277. doi:10.1111/j.1365-2389.1980.tb02080.x
Smith AP, Marín-Spiotta E, de Graaff MA, Balser TC (2014) Microbial community structure varies across soil organic matter aggregate pools during tropical land cover change. Soil Biol Biochem 77:292–303. doi:10.1016/j.soilbio.2014.05.030
Stumm W, Morgan JJ (1996) Aquatic chemistry: chemical equilibria and rates in natural waters. Wiley, New York
Sunda WG, Kieber DJ (1994) Oxidation of humic substances by manganese oxides yields low-molecular-weight organic substrates. Nature 367:62–64. doi:10.1038/367062a0
Tang J, Riley WJ (2014) Weaker soil carbon-climate feedbacks resulting from microbial and abiotic interactions. Nat Clim Change. doi:10.1038/nclimate2438
Teh YA, Silver WL, Conrad ME (2005) Oxygen effects on methane production and oxidation in humid tropical forest soils. Glob Change Biol 11:1283–1297. doi:10.1111/j.1365-2486.2005.00983.x
Thompson IA, Huber DM, Guest CA, Schulze DG (2005) Fungal manganese oxidation in a reduced soil. Environ Microbiol 7:1480–1487. doi:10.1111/j.1462-2920.2005.00842.x
Thompson A, Rancourt DG, Chadwick OA, Chorover J (2011) Iron solid-phase differentiation along a redox gradient in basaltic soils. Geochim Cosmochim Acta 75:119–133. doi:10.1016/j.gca.2010.10.005
Torn MS, Trumbore SE, Chadwick OA et al (1997) Mineral control of soil organic carbon storage and turnover. Nature 389:170–173. doi:10.1038/38260
Torn MS, Vitousek PM, Trumbore SE (2005) The influence of nutrient availability on soil organic matter turnover estimated by incubations and radiocarbon modeling. Ecosystems 8:352–372. doi:10.1007/s10021-004-0259-8
van der Lee GEM, de Winder B, Bouten W, Tietema A (1999) Anoxic microsites in Douglas fir litter. Soil Biol Biochem 31:1295–1301. doi:10.1016/S0038-0717(99)00048-6
Vavilin VA, Fernandez B, Palatsi J, Flotats X (2008) Hydrolysis kinetics in anaerobic degradation of particulate organic material: an overview. Waste Manag 28:939–951. doi:10.1016/j.wasman.2007.03.028
Veen JAV, Kuikman PJ (1990) Soil structural aspects of decomposition of organic matter by micro-organisms. Biogeochemistry 11:213–233. doi:10.1007/BF00004497
Vermes J-F, Myrold DD (1992) Denitrification in forest soils of Oregon. Can J For Res 22:504–512. doi:10.1139/x92-066
von Fischer JC, Hedin LO (2002) Separating methane production and consumption with a field-based isotope pool dilution technique: methane isotope pool dilution. Glob Biogeochem Cycles 16:8-1–8-13. doi:10.1029/2001GB001448
Wania R, Ross I, Prentice IC (2009) Integrating peatlands and permafrost into a dynamic global vegetation model: 2. Evaluation and sensitivity of vegetation and carbon cycle processes. Glob Biogeochem Cycles 23:GB3015. doi:10.1029/2008GB003413
Wasko C, Sharma A (2015) Steeper temporal distribution of rain intensity at higher temperatures within Australian storms. Nat Geosci. doi:10.1038/ngeo2456
West AE, Schmidt SK (2002) Endogenous methanogenesis stimulates oxidation of atmospheric CH4 in alpine tundra soil. Microb Ecol 43:408–415. doi:10.1007/s00248-001-1049-x
Wu X-L, Chin K-J, Stubner S, Conrad R (2001) Functional patterns and temperature response of cellulose-fermenting microbial cultures containing different methanogenic communities. Appl Microbiol Biotechnol 56:212–219. doi:10.1007/s002530100622
Zausig J, Stepniewski W, Horn R (1993) Oxygen concentration and redox potential gradients in unsaturated model soil aggregates. Soil Sci Soc Am J 57:908. doi:10.2136/sssaj1993.03615995005700040005x
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This work was supported by the US Department of Energy, Office of Biological and Environmental Research, Terrestrial Ecosystem Program (Award Number DE-FG02-13ER65542). We would also like to thank Patrick Megonigal and an anonymous reviewer for their help in improving this manuscript.
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Keiluweit, M., Nico, P.S., Kleber, M. et al. Are oxygen limitations under recognized regulators of organic carbon turnover in upland soils?. Biogeochemistry 127, 157–171 (2016). https://doi.org/10.1007/s10533-015-0180-6
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DOI: https://doi.org/10.1007/s10533-015-0180-6