Abstract
In addition to increasing plant C inputs, strategies for enhancing soil C sequestration include reducing C turnover and increasing its residence time in soils. Two major mechanisms, (bio)chemical alteration and physicochemical protection, stabilize soil organic C (SOC) and thereby control its turnover. With (bio)chemical alteration, SOC is transformed by biotic and abiotic processes to chemical forms that are more resistant to decomposition and, in some cases, more easily retained by sorption to soil solids. With physicochemical protection, biochemical attack of SOC is inhibited by organomineral interactions at molecular to millimeter scales. Stabilization of otherwise decomposable SOC can occur via sorption to mineral and organic soil surfaces, occlusion within aggregates, and deposition in pores or other locations inaccessible to decomposers and extracellular enzymes. Soil structure is a master integrating variable that both controls and indicates the SOC stabilization status of a soil. One potential option for reducing SOC turnover and enhancing sequestration, is to modify the soil physicochemical environment to favor the activities of fungi. Specific practices that could accomplish this include manipulating the quality of plant C inputs, planting perennial species, minimizing tillage and other disturbances, maintaining a near-neutral soil pH and adequate amounts of exchangeable base cations (particularly calcium), ensuring adequate drainage, and minimizing erosion. In some soils, amendment with micro- and mesoporous sorbents that have a high specific surface – such as fly ash or charcoal – can be beneficial.
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Adu JK, Oades JM (1978) Utilization of organic materials in soil aggregates by bacteria and fungi. Soil Biol Biochem 10:117–122
Allen MF, Klironomos JN, Treseder KK, Oechel WC (2005) Responses of soil biota to elevated CO2 in a chaparral ecosystem. Ecol Appl 15:1701–1711
Allison FE (1968) Soil aggregation – some facts and fallacies as seen by a microbiologist. Soil Sci 106:136–143
Amonette JE, Capp JA, Lüttge A, Baer DR, Arvidson RS (2000) Geochemical mechanisms in terrestrial carbon sequestration. In: Annual report 1999, environmental dynamics and simulation, PNNL-13206/UC-400. Pacific Northwest National Laboratory, Richland, Washington, pp 3-23 to 3-27
Amonette JE, Kim J, Russell CK (2004) Enhancement of soil carbon sequestration: a catalytic approach. Preprint paper – Am Chem Soc, Div Fuel Chem 49:366–367
Amonette JE, Kim J, Russell CK, Palumbo AV, Daniels WL (2003a) Enhancement of soil carbon sequestration by amendment with fly ash. In: Proceedings 2003 International, Ash Utilization Symposium, Lexington, Kentucky, Paper #47
Amonette JE, Kim J, Russell CK, Palumbo AV, Daniels WL (2003b) Fly ash catalyzes carbon sequestration. In: Proceedings Second Annual Conference on Carbon Sequestration, Alexandria, Virginia, http://www.carbonsq.com/pdf/posters/TI3.pdf
Angers DA, Recous S, Aita C (1997) Fate of carbon and nitrogen in water-stable aggregates during decomposition of 13C15N-labeled wheat straw in situ. Eur J Soil Sci 48:295–300
Bailey VL, Smith JL, Bolton H Jr (2002) Fungal-to-bacterial ratios in soils investigated for enhanced carbon sequestration. Soil Biol Biochem 34:1385–1389
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
Beare MH, Coleman DC, Crossley DA Jr, Hendrix PF, Odum EP (1995) A hierarchical approach to evaluating the significance of soil biodiversity to biogeochemical cycling. Plant Soil 170:5–22
Beare MH, Parmelee RW, Hendrix PF, Cheng W, Coleman DC, Crossley DA Jr (1992) Microbial and faunal interactions and effects on litter nitrogen and decomposition in agroecosystems. Ecol Monogr 62:569–591
Besnard E, Chenu C, Balesdent J, Puget P, Arrouays D (1996) Fate of particulate organic matter in soil aggregates during cultivation. Eur J Soil Sci 47:495–503
Blanco-Canqui H, Lal R (2004) Mechanisms of carbon sequestration in soil aggregates. Crit Rev Plant Sci 23:481–504
Booth KJ, Patti AF, Scott JL, Wallis PJ (2004) Organic matter transformation catalyzed by clays: model reactions for carbon sequestration in soils. In: SuperSoil 2004, 3rd Australian New Zealand Soils Conference, University of Sydney, Australia. http://www.regional.org.au/au/asssi/supersoil2004/s10/oral/1538_wallisp.htm
Bossuyt H, Six J, Hendrix PF (2002) Aggregate-protected carbon in no-tillage and conventional tillage agroecosystems using carbon-14 labeled plant residue. Soil Sci Soc Am J 66:1965–1973
Boyd SA, Mortland MM (1990) Enzyme interactions with clays and clay-organic matter complexes. In: Bollag J-M, Stotzky G (eds) Soil biochemistry, vol. 6. Marcel Dekker, New York, pp 1–28
Carter MR (2004) Researching structural complexity in agricultural soils. Soil Tillage Res 79:1–6
Chefetz B, Tarchitzky J, Desmukh AP, Hatcher PG, Chen Y (2002) Structural characterization of soil organic matter and humic acids in particle-size fractions of an agricultural soil. Soil Sci Soc Am J 66:129–141
Christensen BT (2001) Physical fractionation of soil and structural and functional complexity in organic matter turnover. Eur J Soil Sci 52:345–353
Claus H, Gleixner G, Filip Z (1999) Formation of humic-like substances in mixed and pure cultures of aquatic microorganisms. Acta Hydrochim Hydrobiol 27:200–207
Clein JS, Schimel JP (1994) Reduction in microbial activity in birch litter due to drying and rewetting events. Soil Biol Biochem 26:403–406
Conesa A, Punt PJ, van den Hondel C (2002) Fungal peroxidases: molecular aspects and applications. J Biotechnol 93:143–158
Dai X, Boutton TW, Glaser B, Ansley RJ, Zech W (2005) Black carbon in a temperate mixed-grass savanna. Soil Biol Biochem 37:1879–1881
Dalal RC, Bridge BJ (1996) Aggregation and organic matter storage in sub-humid and semi-arid soils. In: Carter MR, Stewart BA (eds) Structure and organic matter storage in agricultural soils. CRC, Boca Raton, Florida, pp 263–307
Denef K, Six J, Bossuyt H, Frey SD, Elliott ET, Merckx R, Paustian K (2001) Influence of dry–wet cycles on the interrelationship between aggregate, particulate organic matter, and microbial community dynamics. Soil Biol Biochem 33:1599–1611
Dexter AR (1988) Advances in characterization of soil structure. Soil Tillage Res 11:199–238
Dick WA, Tabatabai MA (1992) Significance and potential uses of soil enzymes. In: Metting FB Jr (ed) Soil microbial ecology: applications in agricultural and environmental management. Marcel Dekker, New York, pp 95–127
Ekschmitt K, Liu M, Vetter S, Fox O, Wolters V (2005) Strategies used by soil biota to overcome soil organic matter stability – why is dead organic matter left over in soil? Geoderma 128:167–176
Elliott ET, Coleman DC (1988) Let the soil work for us. Ecol Bull 39:23–32
Elliott ET, Anderson RV, Coleman DC, Cole CV (1980) Habitable pore space and microbial trophic interactions. Oikos 35:327–335
Feller C, Beare MH (1997) Physical control of soil organic matter dynamics in the tropics. Geoderma 79:69–116
Fierer N, Schimel JP (2002) Effects of drying–rewetting frequency on soil carbon and nitrogen transformations. Soil Biol Biochem 34:777–787
Flaig W (1975) An introductory review on humic substances: aspects of research on their genesis, their physical and chemical properties, and their effect on organisms. In: Povoledo D, Golterman HL (eds) Humic substances: their structure and function in the biosphere. Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, pp 19–42
Franzluebbers AJ, Wright SF, Stuedemann JA (2000) Soil aggregation and glomalin under pastures in the Southern Piedmont USA. Soil Sci Soc Am J 64:1018–1026
Freeman C, Ostle N, Kang H (2001) An enzymic “latch” on a global carbon store – a shortage of oxygen locks up carbon in peatlands by restraining a single enzyme. Nature 409:149
Frey SD, Gupta VVSR, Elliott ET, Paustian K (2001) Protozoan grazing affects estimates of carbon utilization efficiency of the soil microbial community. Soil Biol Biochem 33:1759–1768
Gale WJ, Cambardella CA, Bailey TB (2000) Root-derived carbon and the formation and stabilization of aggregates. Soil Sci Soc Am J 64:201–207
Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390
George TS, Richardson AE, Simpson RJ (2005) Behaviour of plant-derived extracellular phytase upon addition to soil. Soil Biol Biochem 37:977–988
Glaser B, Lehmann J, Zech W (2002) Ameliorating physical and chemical properties of highly weathered soils in the tropics with charcoal – a review. Biol Fertil Soils 35:219–230
Golchin A, Oades JM, Skjemstad JO, Clark P (1994) Soil structure and carbon cycling. Aust J Soil Res 32:1043–1068
Gregorich EG, Kachanoski RG, Voroney RP (1989) Carbon mineralization in soil size fractions after various amounts of aggregate disruption. J Soil Sci 40:649–659
Guggenberger G, Frey SD, Six J, Paustian K, Elliot ET (1999) Bacterial and fungal cell-wall residues in conventional and no-tillage agroecosystems. Soil Sci Soc Am J 63:1188–1198
Haider K, Martin JP (1981) Decomposition in soil of specifically 14C-labeled model and cornstalk lignins and coniferyl alcohol over two years as influenced by drying, rewetting, and additions of an available C substrate. Soil Biol Biochem 13:447–450
Haider K, Martin JP, Filip Z, Fustec-Mathon E (1975) Contribution of soil microbes to the formation of humic compounds. In: Povoledo D, Golterman HL (eds) Humic substances: their structure and function in the biosphere. Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, pp 71–85
Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218
Hayes MHB, Malcolm RL (2001) Considerations of compositions and aspects of the structures of humic substances. In: Clapp CE, Hayes MHB, Senesi N, Bloom PR, Jardine PM (eds) Humic substances and chemical contaminants. Soil Science Society of America, Madison, Wisconsin, pp 3–39
Haynes RJ, Beare MH (1997) Influence of six crop species on aggregate stability and some labile organic matter fractions. Soil Biol Biochem 29:1647–1653
Hedges JI (1988) Polymerization of humic substances in natural environments. In: Frimmel FH, Christman RF (eds) Humic substances and their role in the environment. Wiley, New York, pp 45–57
Hill GT, Mitkowski NA, Aldrich-Wolfe L, Emele LR, Jurkonie DD, Ficke A, Maldonado-Ramirez S, Lynch ST, Nelson EB (2000) Methods for assessing the composition and diversity of soil microbial communities. Appl Soil Ecol 15:25–36
Holland EA, Coleman DC (1987) Litter placement effects on microbial and organic matter dynamics in an agroecosystem. Ecology 68:425–433
Hu SJ, van Bruggen AHC, Grünwald NJ (1999) Dynamics of bacterial populations in relation to carbon availability in a residue-amended soil. Appl Soil Ecol 13:21–30
Jastrow JD, Miller RM (1998) Soil aggregate stabilization and carbon sequestration: feedbacks through organomineral associations. In: Lal R, Kimble JM, Follett RF, Stewart BA (eds) Soil processes and the carbon cycle. CRC, Boca Raton, Florida, pp 207–223
Jastrow JD, Miller RM, Lussenhop J (1998) Contributions of interacting biological mechanisms to soil aggregate stabilization in restored prairie. Soil Biol Biochem 30:905–916
Jenny H (1941) Factors of soil formation. McGraw-Hill, New York
Johnson DW, Curtis PS (2001) Effects of forest management on soil C and N storage: meta analysis. For Ecol Manag 140:227–238
Kaiser K, Guggenberger G (2003) Mineral surfaces and soil organic matter. Eur J Soil Sci 54:219–236
Kay BD (1990) Rates of change of soil structure under different cropping systems. Adv Soil Sci 12:1–52
Kononova MM (1961) Soil organic matter. Nowakowski TZ, Greenwood GA (transl.) Pergamon, Oxford
Luo Y, White LW, Canadell JG, DeLucia EH, Ellsworth DS, Finzi A, Lichter J, Schlesinger WH (2003) Sustainability of terrestrial carbon sequestration: a case study in Duke Forest with inversion approach. Glob Biogeochem Cycles 17(1):1021
Maillard LC (1916) Synthese de matieres humiques par action des acides amines sur les sucres reducteures. Ann Chem Phys 5:528–317
Marilley L, Hartwig UA, Aragno M (1999) Influence of an elevated atmospheric CO2 content on soil and rhizosphere bacterial communities beneath Lolium perenne and Trifolium repens under field conditions. Microb Ecol 38:39–49
Martin JP, Haider K (1971) Microbial activity in relation to soil humus formation. Soil Sci 111:54–63
Martin JP, Haider K, Bondietti E (1975) Properties of model humic acids synthesized by phenoloxidase and autoxidation of phenols and other compounds formed by soil fungi. In: Povoledo D, Golterman HL (eds) Humic substances: their structure and function in the biosphere. Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, pp 171–186
Martin A, Marinissen JCY (1993) Biological and physico–chemical processes in excrements of soil animals. Geoderma 56:331–347
Mikola J, Bardgett RD, Hedlund K (2002) Biodiversity, ecosystem functioning and soil decomposer food webs. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning–synthesis and perspectives. Oxford University Press, Oxford, pp 169–180
Miller RM, Jastrow JD (1990) Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biol Biochem 22:579–584
Miller RM, Jastrow JD (2000) Mycorrhizal fungi influence soil structure. In: Kapulnik Y, Douds DD Jr (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, The Netherlands, pp 3–18
Naidja A, Huang PM, Bollag J-M (1998) Comparison of reaction products from the transformation of catechol catalyzed by birnessite or tyrosinase. Soil Sci Soc Am J 62:188–195
Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670
Oades JM (1984) Soil organic matter and structural stability: mechanisms and implications for management. Plant Soil 76:319–337
Oades JM (1993) The role of biology in the formation, stabilization and degradation of soil structure. Geoderma 56:377–400
Oades JM, Waters AG (1991) Aggregate hierarchy in soils. Aust J Soil Res 29:815–828
Payne WJ (1970) Energy yields and growth of heterotrophs. Annu Rev Microbiol 24:17–52
Pelz O, Cifuentes LA, Hammer BT, Kelley CA, Coffin RB (1998) Tracing the assimilation of organic compounds using δ13C analysis of unique amino acids in the bacterial peptidoglycan cell wall. FEMS Microbiol Ecol 25:229–240
Plante AF, McGill WB (2002) Soil aggregate dynamics and the retention of organic matter in laboratory-incubated soil with differing simulated tillage frequencies. Soil Tillage Res 66:79–92
Rees RM, Bingham IJ, Baddeley JA, Watson CA (2005) The role of plants and land management in sequestering soil carbon in temperate arable and grassland ecosystems. Geoderma 128:130–154
Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363
Rillig MC, Allen MF (1999) What is the role of arbuscular mycorrhizal fungi in plant-to-ecosystem responses to elevated atmospheric CO2? Mycorrhiza 9:1–8
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602
Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563
Schimel JP, Gulledge JM, Clein-Curley JS, Lindstrom JE, Braddock JF (1999) Moisture effects on microbial activity and community structure in decomposing birch litter in the Alaskan taiga. Soil Biol Biochem 31:831–838
Schubert WJ (1965) Lignin biochemistry. Academic, New York
Seastedt TR (1984) The role of arthropods in decomposition and mineralization processes. Annu Rev Entomol 29:25–46
Sexstone AJ, Revsbech NP, Parkin TB, Tiedje JM (1985) Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Sci Soc Am J 49:645–651
Shen S, Tu S, Taylor RM (2002) Interactions of enzymes with clays and applications in bioremediation. In: Dixon JB, Schulze DG (eds) Soil mineralogy with environmental applications, SSSA Book Series 7. Soil Science Society of America, Madison, Wisconsin, pp 795–817
Shindo H, Huang PM (1984) Catalytic effects of manganese(IV), iron(III), aluminum, and silicon-oxides on the formation of phenolic polymers. Soil Sci Soc Am J 48:927–934
Six J, Jastrow JD (2002) Organic matter turnover. In: Lal R (ed) Encyclopedia of soil science. Marcel Dekker, New York, pp 936–942
Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31
Six J, Conant RT, Paul EA, Paustian K (2002a) Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–176
Six J, Elliott ET, Paustian K (2000) Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol Biochem 32:2099–2103
Six J, Feller C, Denef K, Ogle SM, de Moraes Sa JC, Albrecht A (2002b) Soil organic matter, biota and aggregation in temperate and tropical soils – effects of no-tillage. Agronomie 22:755–775
Sjoblad RD, Bollag J-M (1981) Oxidative coupling of aromatic compounds by enzymes from soil microorganisms. In: Paul EA, Ladd JN (eds) Soil biochemistry, vol 5. Marcel Dekker, New York, pp 113–152
Sollins P, Homann P, Caldwell BA (1996) Stabilization and destabilization of soil organic matter: mechanisms and controls. Geoderma 74:65–105
Steinberg PD, Rillig MC (2003) Differential decomposition of arbuscular mycorrhizal fungal hyphae and glomalin. Soil Biol Biochem 35:191–194
Stevenson FJ (1994) Humus chemistry: genesis, composition, reactions, 2nd edn. Wiley, New York
Stevenson FJ, Cole MA (1999) Cycles of soil: carbon, nitrogen, phosphorus, sulfur, micronutrients. Wiley, New York
Strong DT, DeWever H, Merckx R, Recous S (2004) Spatial location of carbon decomposition in the soil pore system. Eur J Soil Sci 55:739–750
Suberkropp K, Weyers H (1996) Application of fungal and bacterial production methodologies to decomposing leaves in streams. Appl Environ Microbiol 62:1610–1615
Sutton R, Sposito G (2005) Molecular structure in soil humic substances: the new view. Environ Sci Technol 39:9009–9015
Tan KH (2003) Humic matter in soil and the environment: principles and controversies. Marcel Dekker, New York
Tate RL III (1992) Soil organic matter: biological and ecological effects. Krieger, Malabar, Florida
ten Have R, Teunissen PJM (2001) Oxidative mechanisms involved in lignin degradation by white-rot fungi. Chem Rev 101:3397–3413
Tiedje JM, Asuming-Brempong S, Nüsslein K, Marsh TL, Flynn SJ (1999) Opening the black box of soil microbial diversity. Appl Soil Ecol 13:109–122
Tisdall JM (1996) Formation of soil aggregates and accumulation of soil organic matter. In: Carter MR, Stewart BA (eds) Structure and organic matter storage in agricultural soils. CRC, Boca Raton, Florida, pp 57–96
Tisdall JM, Oades JM (1982) Organic matter and water stable aggregates in soils. J Soil Sci 33:141–163
Treseder KK, Allen MF (2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol 147:189–200
van der Wal A, van Veen JA, Smant W, Boschker HTS, Bloem J, Kardol P, van der Putten WH, de Boer W (2006) Fungal biomass development in a chronosequence of land abandonment. Soil Biol Biochem 38:51–60
Vetter YA, Deming JW, Jumars PA, Krieger-Brockett BB (1998) A predictive model of bacterial foraging by means of freely released extracellular enzymes. Microb Ecol 36:75–92
Waksman SA (1932) Humus. Williams & Wilkins, Baltimore, Maryland
Wang MC, Huang PM (2005) Cleavage of 14C-labeled glycine and its polycondensation with pyrogallol as catalyzed by birnessite. Geoderma 124:415–426
West AW, Sparling GP, Grant WD (1987) Relationships between mycelial and bacterial populations in stored, air-dried and glucose-amended arable and grassland soils. Soil Biol Biochem 19:599–605
Wolfaardt GM, Lawrence JR, Robarts RD, Caldwell DE (1994) The role of interactions, sessile growth, and nutrient amendments on the degradative efficiency of a microbial consortium. Can J Microbiol 40:331–340
Young IM, Ritz K (2000) Tillage, habitat space and function of soil microbes. Soil Tillage Res 53:201–213
Zech W, Sensei N, Guggenberger G, Kaiser K, Lehmann J, Miano TM, Miltner A, Schroth G (1997) Factors controlling humification and mineralization of soil organic matter in the tropics. Geoderma 79:117–161
Zhu YG, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil–plant systems. Trends Plant Sci 8:407–409
Zimmerman AR, Chorover J, Goyne KW, Brantley SL (2004) Protection of mesopore-adsorbed organic matter from enzymatic degradation. Environ Sci Technol 38:4542–4548
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Jastrow, J.D., Amonette, J.E. & Bailey, V.L. Mechanisms controlling soil carbon turnover and their potential application for enhancing carbon sequestration. Climatic Change 80, 5–23 (2007). https://doi.org/10.1007/s10584-006-9178-3
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DOI: https://doi.org/10.1007/s10584-006-9178-3