Abstract
Mineral-associated organic matter (MAOM) is a key component of the global carbon (C) and nitrogen (N) cycles, but the processes controlling its formation from plant litter are not well understood. Recent evidence suggests that more MAOM will form from higher quality litters (e.g., those with lower C/N ratios and lower lignocellulose indices), than lower quality litters. Shoots and roots of the same non-woody plant can provide good examples of high and low quality litters, respectively, yet previous work tends to show a majority of soil organic matter is root-derived. We investigated the effect of litter quality on MAOM formation from shoots versus roots using a litter-soil slurry incubation of isotopically labeled (13C and 15N) shoots or roots of Big Bluestem (Andropogon gerardii) with isolated silt or clay soil fractions. The slurry method minimized the influence of soil structure and maximized contact between plant material and soil. We tracked the contribution of shoot- and root-derived C and N to newly formed MAOM over 60 days. We found that shoots contributed more C and N to MAOM than roots. The formation of shoot-derived MAOM was also more efficient, meaning that less CO2 was respired per unit MAOM formed. We suggest that these results are driven by initial differences in litter chemistry between the shoot and root material, while results of studies showing a majority of soil organic matter is root-derived may be driven by alternate mechanisms, such as proximity of roots to mineral surfaces, greater contribution of roots to aggregate formation, and root exudation. Across all treatments, newly formed MAOM had a low C/N ratio compared to the parent plant material, which supports the idea that microbial processing of litter is a key pathway of MAOM formation.
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References
Abiven S, Recous S, Reyes V, Oliver R (2005) Mineralisation of C and N from root, stem and leaf residues in soil and role of their biochemical quality. Biol Fertil Soils 42:119–128. https://doi.org/10.1007/s00374-005-0006-0
Adair EC, Parton WJ, Del Grosso SJ et al (2008) Simple three-pool model accurately describes patterns of long-term litter decomposition in diverse climates. Glob Chang Biol 14:2636–2660. https://doi.org/10.1111/j.1365-2486.2008.01674.x
Allison SD, Jastrow JD (2006) Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biol Biochem 38:3245–3256. https://doi.org/10.1016/j.soilbio.2006.04.011
Anderson DW, Paul EA (1984) Organo-mineral complexes and their study by radiocarbon dating. Soil Sci Soc Am J 48:298–301. https://doi.org/10.2136/sssaj1984.03615995004800020014x
Balesdent J, Balabane M (1996) Major contribution of roots to soil carbon storage inferred from maize cultivated soils. Soil Biol Biochem 28:1261–1263. https://doi.org/10.1016/0038-0717(96)00112-5
Balesdent J, Mariotti A, Guillet B (1987) Natural C-13 abundance as a tracer for studies of soil organic-matter dynamics. Soil Biol Biochem 19:25–30. https://doi.org/10.1016/0038-0717(87)90120-9
Balesdent J, Balesdent J, Mariotti A et al (1996) Measurement of soil organic matter turnover using 13C natural abundance. In: Boutton TW, Yamasaki S-I (eds) Mass spectrometry of soils. Marcel Dekker Inc, New York, pp 83–111
Batjes NH (2014) Total carbon and nitrogen in the soils of the world. Eur J Soil Sci 65:4–21. https://doi.org/10.1111/ejss.12114_2
Birch HF (1958) The effect of soil drying on humus decomposition and nitrogen availability. Plant Soil 10:9–31. https://doi.org/10.1007/BF01343734
Bird JA, Kleber M, Torn MS (2008) 13C and 15N stabilization dynamics in soil organic matter fractions during needle and fine root decomposition. Org Geochem 39:465–477. https://doi.org/10.1016/j.orggeochem.2007.12.003
Birge HE, Conant RT, Follett RF et al (2015) Soil respiration is not limited by reductions in microbial biomass during long-term soil incubations. Soil Biol Biochem 81:304–310. https://doi.org/10.1016/j.soilbio.2014.11.028
Bolinder MA, Angers DA, Giroux M, Laverdière MR (1999) Estimating C inputs retained as soil organic matter from corn (Zea mays L.). Plant Soil 215:85–91. https://doi.org/10.1023/A:1004765024519
Calderón FJ, Reeves JB III, Collins HP, Paul EA (2011) Chemical differences in soil organic matter fractions determined by diffuse-reflectance mid-infrared spectroscopy. Soil Sci Soc Am J 75:568–579. https://doi.org/10.2136/sssaj2009.0375
Cambardella CA, Elliott ET (1992) Particulate soil organic-matter changes across a grassland cultivation sequence. Soil Sci Soc Am J 56:777–783. https://doi.org/10.2136/sssaj1992.03615995005600030017x
Castellano MJ, Mueller KE, Olk DC et al (2015) Integrating plant litter quality, soil organic matter stabilization, and the carbon saturation concept. Glob Chang Biol 21:3200–3209. https://doi.org/10.1111/gcb.12982
Christensen BT (2001) Physical fractionation of soil and structural and functional complexity in organic matter turnover. Eur J Soil Sci 52:345–353. https://doi.org/10.1046/j.1365-2389.2001.00417.x
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 Chang Biol 19:988–995. https://doi.org/10.1111/gcb.12113
Cotrufo MF, Soong JL, Horton AJ et al (2015) Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nat Geosci 8:776–779. https://doi.org/10.1038/ngeo2520
Crow SE, Swanston CW, Lajtha K et al (2007) Density fractionation of forest soils: methodological questions and interpretation of incubation results and turnover time in an ecosystem context. Biogeochemistry 85:69–90. https://doi.org/10.1007/s10533-007-9100-8
Feng X, Simpson AJ, Simpson MJ (2005) Chemical and mineralogical controls on humic acid sorption to clay mineral surfaces. Org Geochem 36:1553–1566. https://doi.org/10.1016/j.orggeochem.2005.06.008
Fisher BA (2016) Geomorphic controls on mineral weathering, elemental transport, carbon cycling, and production of mineral surface area in a schist bedrock weathering profile, Piedmont Pennsylvania. Doctoral dissertation. University of Minnesota. Minneapolis
Goering HK, Van Soest PJ (1970) Forage fiber analyses (apparatus, reagents, prcedures, and some applications). In: USDA agriculture handbook no. 379. Washington, D.C
Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307. https://doi.org/10.1016/j.scitotenv.2007.11.013
Haddix ML, Plante AF, Conant RT et al (2011) The role of soil characteristics on temperature sensitivity of soil organic matter. Soil Sci Soc Am J 75:56–68. https://doi.org/10.2136/sssaj2010.0118
Haddix ML, Paul EA, Cotrufo MF (2016) Dual, differential isotope labeling shows the preferential movement of labile plant constituents into mineral-bonded soil organic matter. Glob Chang Biol 22:2301–2312. https://doi.org/10.1111/gcb.13237
Hassink J, Whitmore AP, Kubat J (1997) Size and density fractionation of soil organic matter and the physical capacity of soils to protect organic matter. Eur J Agron 7:189–199. https://doi.org/10.1016/S1161-0301(97)00045-2
Hatton P-J, Castanha C, Torn MS, Bird JA (2015) Litter type control on soil C and N stabilization dynamics in a temperate forest. Glob Chang Biol 21:1358–1367. https://doi.org/10.1111/gcb.12786
Jackson RB, Lajtha K, Crow SE et al (2017) The ecology of soil carbon: pools, vulnerabilities, and biotic and abiotic controls. Annu Rev Ecol Evol Syst. https://doi.org/10.1146/annurev-ecolsys-112414-054234
Jagadamma S, Steinweg JM, Mayes MA et al (2013) Decomposition of added and native organic carbon from physically separated fractions of diverse soils. Biol Fertil Soils 50:613–621. https://doi.org/10.1007/s00374-013-0879-2
Kallenbach CM, Frey SD, Grandy AS (2016) Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat Commun 7:13630. https://doi.org/10.1038/ncomms13630
Keiluweit M, Bougoure JJ, Nico PS et al (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Chang 5:588–595. https://doi.org/10.1038/nclimate2580
Khomo L, Trumbore S, Bern CR, Chadwick OA (2017) Timescales of C turnover in soils with mixed crystalline mineralogies, Kruger National Park, South Africa. SOIL 3:17–30. https://doi.org/10.5194/soil-3-17-2017
Kleber M, Mikutta R, Torn MS, Jahn R (2005) Poorly crystalline mineral phases protect organic matter in acid subsoil horizons. Eur J Soil Sci 56:717–725. https://doi.org/10.1111/j.1365-2389.2005.00706.x
Kleber M, Sollins P, Sutton R (2007) A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces. Biogeochemistry 85:9–24. https://doi.org/10.1007/s10533-007-9103-5
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. https://doi.org/10.1890/10-1307.1
Knicker H (2011) Soil organic N—an under-rated player for C sequestration in soils? Soil Biol Biochem 43:1118–1129. https://doi.org/10.1016/j.soilbio.2011.02.020
Kögel-Knabner I, Guggenberger G, Kleber M et al (2008) Organo-mineral associations in temperate soils: integrating biology, mineralogy, and organic matter chemistry. J Plant Nutr Soil Sci 171:61–82. https://doi.org/10.1002/jpln.200700048
Kramer MG, Sanderman J, Chadwick OA et al (2012) Long-term carbon storage through retention of dissolved aromatic acids by reactive particles in soil. Glob Chang Biol 18:2594–2605. https://doi.org/10.1111/j.1365-2486.2012.02681.x
Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68. https://doi.org/10.1038/nature16069
Leifeld J (2006) Soils as sources and sinks of greenhouse gases. Geol Soc Lond Spec Publ 266:23–44. https://doi.org/10.1144/GSL.SP.2006.266.01.03
Manzoni S, Taylor P, Richter A et al (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91. https://doi.org/10.1111/j.1469-8137.2012.04225.x
Martin RE, Asner GP, Ansley RJ, Mosier AR (2003) Effects of woody vegetation encroachment on soil nitrogen oxide emissions in a temperate savanna. Ecol Appl 13:897–910. https://doi.org/10.1890/1051-0761(2003)13[897:EOWVEO]2.0.CO;2
McKeague JA, Day DH (1966) Dithionite- and oxalate-extractable Fe and Al as aids in differentiating various classes of soils. Can J Soil Sci 46:13–22. https://doi.org/10.4141/cjss66-003
McKee GA, Soong JL, Calderón F et al (2016) An integrated spectroscopic and wet chemical approach to investigate grass litter decomposition chemistry. Biogeochemistry 128:107–123. https://doi.org/10.1007/s10533-016-0197-5
Mehra OP, Jackson ML (1960) Iron oxide removal from soils and clays by a dithionite–citrate system buffered with sodium bicarbonate. Clays Clay Miner 7:317–327. https://doi.org/10.1346/CCMN.1958.0070122
Mikutta R, Kleber M, Torn MS, Jahn R (2006) Stabilization of soil organic matter: association with minerals or chemical recalcitrance? Biogeochemistry 77:25–56. https://doi.org/10.1007/s10533-005-0712-6
Murage EW, Voroney P, Beyaert RP (2007) Turnover of carbon in the free light fraction with and without charcoal as determined using the 13C natural abundance method. Geoderma 138:133–143. https://doi.org/10.1016/j.geoderma.2006.11.002
Paul EA (2016) The nature and dynamics of soil organic matter: plant inputs, microbial transformations, and organic matter stabilization. Soil Biol Biochem 98:109–126. https://doi.org/10.1016/j.soilbio.2016.04.001
Plante AF, Conant RT, Stewart CE et al (2006) Impact of soil texture on the distribution of soil organic matter in physical and chemical fractions. Soil Sci Soc Am J 70:287–296. https://doi.org/10.2136/sssaj2004.0363
Preston CM, Trofymow JA (2015) The chemistry of some foliar litters and their sequential proximate analysis fractions. Biogeochemistry 126:197–209. https://doi.org/10.1007/s10533-015-0152-x
R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Rasse DP, Rumpel C, Dignac M-F (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356. https://doi.org/10.1007/s11104-004-0907-y
Sanderman J, Maddern T, Baldock J (2014) Similar composition but differential stability of mineral retained organic matter across four classes of clay minerals. Biogeochemistry 121:409–424. https://doi.org/10.1007/s10533-014-0009-8
Schmidt MWI, Torn MS, Abiven S et al (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56. https://doi.org/10.1038/nature10386
Singh M, Sarkar B, Biswas B et al (2017) Relationship between soil clay mineralogy and carbon protection capacity as influenced by temperature and moisture. Soil Biol Biochem 109:95–106. https://doi.org/10.1016/j.soilbio.2017.02.003
Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett 16:930–939. https://doi.org/10.1111/ele.12113
Six J, Elliott ET, Paustian K (1999) Aggregate and soil organic matter dynamics under conventional and no-tillage systems. Soil Sci Soc Am J 63:1350–1358. https://doi.org/10.2136/sssaj1999.6351350x
Six J, Conant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–176. https://doi.org/10.1023/A:1016125726789
Smith P, Cotrufo MF, Rumpel C et al (2015) Biogeochemical cycles and biodiversity as key drivers of ecosystem services provided by soils. SOIL 2:665–685. https://doi.org/10.5194/soild-2-537-2015
Sollins P, Swanston C, Kleber M et al (2006) Organic C and N stabilization in a forest soil: evidence from sequential density fractionation. Soil Biol Biochem 38:3313–3324. https://doi.org/10.1016/j.soilbio.2006.04.014
Soong JL, Reuss D, Pinney C et al (2014) Design and operation of a continuous 13C and 15N labeling chamber for uniform or differential, metabolic and structural, plant isotope labeling. J Vis Exp 83:e51117. https://doi.org/10.3791/51117
Soong JL, Parton WJ, Calderón F et al (2015) A new conceptual model on the fate and controls of fresh and pyrolized plant litter decomposition. Biogeochemistry 124:27–44. https://doi.org/10.1007/s10533-015-0079-2
Steffens C, Helfrich M, Joergensen RG et al (2015) Translocation of 13C-labeled leaf or root litter carbon of beech (Fagus sylvatica L.) and ash (Fraxinus excelsior L.) during decomposition—a laboratory incubation experiment. Soil Biol Biochem 83:125–137. https://doi.org/10.1016/j.soilbio.2015.01.015
Stewart CE, Paustian K, Conant RT et al (2007) Soil carbon saturation: concept, evidence and evaluation. Biogeochemistry 86:19–31. https://doi.org/10.1007/s10533-007-9140-0
Stewart CE, Plante AF, Paustian K et al (2008) Soil carbon saturation: linking concept and measurable carbon pools. Soil Sci Soc Am J 72:379–392. https://doi.org/10.2136/sssaj2007.0104
Stewart CE, Zheng J, Botte J, Cotrufo MF (2013) Co-generated fast pyrolysis biochar mitigates green-house gas emissions and increases carbon sequestration in temperate soils. GCB Bioenergy 5:153–164. https://doi.org/10.1111/gcbb.12001
Swift MJ, Heal OW, Anderson JM (1997) Decomposition in terrestrial ecosystems. University of California Press, Berkeley
Tip** E, Somerville CJ, Luster J (2016) The C:N:P: S stoichiometry of soil organic matter. Biogeochemistry 130:117–131. https://doi.org/10.1007/s10533-016-0247-z
Tisdall J, Oades J (1982) Organic matter and water-stable aggregates in soils. J Soil Sci 33:141–163. https://doi.org/10.1111/j.1365-2389.1982.tb01755.x
Torn MS, Trumbore SE, Chadwick OA et al (1997) Mineral control of soil organic carbon storage and turnover. Nature 389:170–173. https://doi.org/10.1038/38260
Voroney RP, Paul EA, Anderson DW (1989) Decomposition of wheat straw and stabilization of microbial products. Can J Soil Sci 69:63–77. https://doi.org/10.4141/cjss89-007
Wallenstein MD, Haddix ML, Lee DD et al (2012) A litter-slurry technique elucidates the key role of enzyme production and microbial dynamics in temperature sensitivity of organic matter decomposition. Soil Biol Biochem 47:18–26. https://doi.org/10.1016/j.soilbio.2011.12.009
Wattel-Koekkoek E, Van GP, Buurman P, van Lagen B (2001) Amount and composition of clay-associated soil organic matter in a range of kaolinitic and smectitic soils. Geoderma 99:27–49. https://doi.org/10.1016/S0016-7061(00)00062-8
Acknowledgements
We thank Michelle Haddix and Dan Reuss for their assistance in the laboratory, and Gene Kelly and Thomas Borch for their comments on the early manuscript. This work was funded by the National Science Foundation awards to RTC (Grant Number DEB-0842315) and to RTC and JML (Doctoral Dissertation Improvement Grant Number DEB-1310821). Funding for the growth of isotopically labeled plant litter was provided by the Cotrufo-Hoppess Fund for Soil Ecology Research.
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Lavallee, J.M., Conant, R.T., Paul, E.A. et al. Incorporation of shoot versus root-derived 13C and 15N into mineral-associated organic matter fractions: results of a soil slurry incubation with dual-labelled plant material. Biogeochemistry 137, 379–393 (2018). https://doi.org/10.1007/s10533-018-0428-z
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DOI: https://doi.org/10.1007/s10533-018-0428-z