, Volume 122, Issue 1, pp 35–45 | Cite as

The soil matrix increases microbial C stabilization in temperate and tropical forest soils

  • Heather M. Throckmorton
  • Jeffrey A. Bird
  • Nick Monte
  • Tad Doane
  • Mary K. Firestone
  • William R. Horwath


Microbial biomass represents a substantial source of labile C contributing to soil organic matter (SOM) maintenance. Microbial residues may associate with the soil matrix through a variety of mechanisms, reducing its bioavailability and increasing its persistence in soil. Our objective was to examine soil matrix effects on the stability of non-living microbial C inputs in two contrasting forest ecosystems by following microbial residues (Fungi, Actinobacteria, Gram-positive bacteria (Gm +), Gram-negative bacteria (Gm −)) into SOM fractions in a temperate forest in California (CA) and a tropical forest in Puerto Rico (PR) for 3 and 2 years, respectively. We isolated 3 SOM fractions: (i) free light fraction (FLF), (ii) occluded light fraction (OLF), and (iii) dense fraction (DF). Additionally, we characterized SOM fraction chemistry to infer quality and source of native fraction SOM. Our results showed greater stabilization as mineral-associated microbial C (i.e., as DF and OLF), compared with loose detrital C (i.e., FLF). There was no microbial group effect (i.e., differences in fraction C recovery among different microbial cell types). Our findings suggest that mineral association is more important for stabilizing non-living microbial C in soil than the cellular structure of the initial source of microbial inputs, with site specific edaphic factors as the major controllers of the amount of microbial residues stabilized.


Microorganisms Fungi Bacteria Carbon Soil organic matter Mineral protection Stabilization 



This research was funded by The National Science Foundation’s Division of Environmental Biology, Ecosystem Science Cluster (Award No. 324002), The Kearney Foundation of Soil Science and the J. G. Boswell Endowed Chair in Soil Science. We are grateful for contributions from researchers J. Braun, L. Dane, E. Dubinsky, J. Fortney, D. Herman, J. Pett-Ridge and W. Silver, as well as the research staff of the UC Blodgett Forest Research Station and the Luquillo Experimental Forest.

Supplementary material

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Supplementary material 1 (DOCX 93 kb)


  1. Aufdenkampe A, Hedges J, Richey J, Krusche A, Llerena C (2001) Sorptive fractionation of dissolved organic nitrogen and amino acids onto fine sediments within the Amazon Basin. Limnology Oceana 46:1921–1935CrossRefGoogle Scholar
  2. Balesdent J, Chenu C, Balabane M (2000) Relationship of soil organic matter dynamics to physical protection and tillage. Soil Tillage Res 53:215–230CrossRefGoogle Scholar
  3. Bird JA, Torn MS (2006) Fine roots vs. needles: a comparison of 13C and 15N dynamics in a ponderosa pine forest soil. Biogeochemistry 79:361–382CrossRefGoogle Scholar
  4. Bird JA, Kleber M, Tor MS (2008) 13C and 15N stabilization dynamics in soil organic matter fractions during needle and fine root decomposition. Org Geochem 39:465–477CrossRefGoogle Scholar
  5. Christensen B (2001) Physical fractionation of soil and structural and functional complexity in organic matter turnover. Eur J Soil Sci 52:345–353CrossRefGoogle Scholar
  6. Dalal RC, Harms BP, Krull E, Wang WJ (2005) Total soil organic matter and its labile pools following mulga (Acacia aneura) clearing for pasture development and cropping 1. Total and labile carbon. Aust J Soil Res 43:13–20CrossRefGoogle Scholar
  7. Derenne S, Largeau C (2001) A review of some important families of refractory macromolecules: composition, origin, and fate in soils and sediments. Soil Sci 166:833–847CrossRefGoogle Scholar
  8. Engelking B, Flessa H, Joergensen RG (2008) Formation and use of microbial residues after adding sugarcane sucrose to a heated soil devoid of soil organic matter. Soil Biol Biochem 40:97–105CrossRefGoogle Scholar
  9. Fan TWM, Bird JA, Brodie EL, Lane AN (2009) 13C-Isotopomer-based metabolomics of microbial groups isolated from two forest soils. Metabolomics 5:108–122CrossRefGoogle Scholar
  10. Gleixner G, Poirier N, Bol R, Balesdent J (2002) Molecular dynamics of organic matter in a cultivated soil. Org Geochem 33:357–366CrossRefGoogle Scholar
  11. Golchin A, Oades JM, Skjemstad JO, Clark P (1994a) Study of free and occluded particulate organic-matter in soils by solid-state C-13 CP/MAS NMR-spectroscopy and scanning electron-microscopy. Aust J Soil Res 32:285–309CrossRefGoogle Scholar
  12. Golchin A, Oades JM, Skjemstad JO, Clarke P (1994b) Soil structure and carbon cycling. Aust J Soil Res 32:1043–1068CrossRefGoogle Scholar
  13. 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 404:297–307CrossRefGoogle Scholar
  14. Grandy AS, Neff JC, Weintrau MN (2007) Carbon structure and enzyme activities in alpine and forest ecosystems. Soil Biol Biochem 39:2701–2711CrossRefGoogle Scholar
  15. Gregorich EG, Beare MH, McKim UF, Skjemstad JO (2006) Chemical and biological characteristics of physically uncomplexed organic matter. Soil Sci Soc Am J 70:975–985CrossRefGoogle Scholar
  16. Hedges JI, Oades JM (1997) Comparative organic geochemistries of soils and marine sediments. Org Geochem 27:319–361CrossRefGoogle Scholar
  17. Jastrow JD, Amonette JE, Bailey VL (2007) Mechanisms controlling soil carbon turnover and their potential application for enhancing carbon sequestration. Clim Change 80:5–23CrossRefGoogle Scholar
  18. Kindler R, Miltner A, Richnow H, Kastner M (2006) Fate of gram-negative bacterial biomass in soil—mineralization and contribution to SOM. Soil Biol Biochem 38:2860–2870CrossRefGoogle Scholar
  19. 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 85:9–24CrossRefGoogle Scholar
  20. Kögel-Knabner I, Guggenberger G, Kleber M, Kandeler E, Kalbitz K, Scheu S, Eusterhues K, Leinweber P (2008) Organo-mineral associations in temperate soils: integrating biology, mineralogy, and organic matter chemistry. J Plant Nutr Soil Sci 171:61–82CrossRefGoogle Scholar
  21. Kölbl A, Kögel-Knabner I (2004) Content and composition of free and occluded particulate organic matter in a differently textured arable Cambisol as revealed by solid-state 13C NMR spectroscopy. J Plant Nutr Soil Sci 167:45–53CrossRefGoogle Scholar
  22. Kracht O, Gleixner G (2000) Isotope analysis of pyrolysis products from Sphagnum peat and dissolved organic matter from bog water. Org Geochem 31:645–654CrossRefGoogle Scholar
  23. Liang C, Balser TC (2010) Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy. Nat Rev Microbiol 8:593–599CrossRefGoogle Scholar
  24. Liu A, Ma BL, Bomke AA (2005) Effects of cover crops on soil aggregate stability, total organic carbon, and polysaccharides. Soil Sci Soc Am J 69:2041–2048CrossRefGoogle Scholar
  25. Mambelli S, Bird JA, Gleixner G, Dawson TE, Torn MS (2011) Relative contribution of needle and fine root pine litter to the molecular composition of soil organic matter after in situ degradation. Org Geochem 42:1099–1108Google Scholar
  26. Marin-Spiotta E, Swanston CW, Torn MS, Silver WL, Burton SD (2008) Chemical and mineral control of soil carbon turnover in abandoned tropical pastures. Geoderma 143:49–62CrossRefGoogle Scholar
  27. Nierop KGJ, Jansen B (2009) Extensive transformation of organic matter and excellent lipid preservation at the upper, superhumid Guandera páramo. Geoderma 151:357–369CrossRefGoogle Scholar
  28. Oades J, Waters A (1991) Aggregate hierarchy in soils. Aust J Soil Res 29:815–828CrossRefGoogle Scholar
  29. Or D, Smets BF, Wraith JM, Dechesne A, Friedman SP (2007) Physical constraints affecting bacterial habitats and activity in unsaturated porous media – a review. Adv Water Resour 30:1505–1527CrossRefGoogle Scholar
  30. Poirier N, Sohi SP, Gaunt JL, Mahieu N, Randall EW, Powlson DS, Evershed RP (2005) The chemical composition of measurable soil organic matter pools. Org Geochem 36:1174–1189CrossRefGoogle Scholar
  31. Pouwels AD, Eijkel GB, Boon JJ (1989) Curie-point pyrolysis-capillary gas chromatography-high-resolution mass spectrometry of microcrystalline cellulose. J Anal Appl Pyrol 14:237–280CrossRefGoogle Scholar
  32. Rasmussen C, Torn M, Southard R (2005) Mineral assemblage and aggregates control carbon dynamics in a California conifer forest. Soil Sci Soc Am J 69:1711–1721CrossRefGoogle Scholar
  33. Rasmussen C, Southard R, Horwath W (2006) Mineral control of organic carbon mineralization in a range of temperate conifer forest soils. Glob Change Biol 12:834–847CrossRefGoogle Scholar
  34. Schulten HR, Schnitzer M (1998) The chemistry of soil organic nitrogen: a review. Biol Fertil Soils 26:1–15CrossRefGoogle Scholar
  35. Simpson AJ, Simpson MS, Smith E, Kelleher BP (2007) Microbially derived inputs to soil organic matter: are current estimates too low? Environ Sci Technol 41:8070–8076CrossRefGoogle Scholar
  36. Six J, Bossuyt H, De Gryze S, Denef K (2004) A history of research on the link between aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31CrossRefGoogle Scholar
  37. Skjemstad JO, Taylor JA, Smernik RJ (1999) Estimation of charcoal (char) in soils. Commun Soil Sci Plant Anal 30:2283–2298CrossRefGoogle Scholar
  38. 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 42:79–88CrossRefGoogle Scholar
  39. Sohi SP, Mahieu N, Arah JRM, Powlson DS, Madari B, Gaunt JL (2001) A procedure for isolating soil organic matter fractions suitable for modeling. Soil Sci Soc Am J 65:1121–1128CrossRefGoogle Scholar
  40. Sollins P, Kramer MG, Swanston C, Lajtha K, Filley T, Aufdenkampe AK, Wagai R, Bowden R (2009) Sequential density fractionation across soils of contrasting mineralogy: evidence for both microbial- and mineral-controlled soil organic matter stabilization. Biogeochemistry 96:209–231CrossRefGoogle Scholar
  41. Sutton R, Sposito G (2005) Molecular structure in soil humic substances: the new view. Environ Sci Technol 39:9009–9015CrossRefGoogle Scholar
  42. Swanston CW, Torn MS, Hanson PJ, Southon JR, Garten CT, Hanlon EM, Ganio L (2005) Initial characterization of processes of soil carbon stabilization using forest stand level radiocarbon enrichment. Geoderma 128:52–62CrossRefGoogle Scholar
  43. Tang J, Mo Y, Zhang J, Zhang R (2011) Influence of biological aggregating agents associated with microbial population on soil aggregate stability. Appl Soil Ecol 47:152–159CrossRefGoogle Scholar
  44. Templer P, Silver W, Pett-Ridge J, DeAngelis K, Firestone M (2008) Plant and microbial controls on nitrogen retention and loss in a humid tropical forest. Ecology 89:3030–3040CrossRefGoogle Scholar
  45. Throckmorton HM, Bird JA, Dane LD, Firestone MK (2012) The source of microbial C has little impact on organic matter stabilization in forest ecosystems. Ecol Lett. doi: 10.1111/j.1461-0248.2012.01848.x Google Scholar
  46. Wagai R, Mayer LM, Kitayama K, Knicker H (2008) Climate and parent material controls on organic matter storage in surface soils: a three-pool, density-separation approach. Geoderma 147:23–33CrossRefGoogle Scholar
  47. Wagai R, Mayer LM, Kitayama K (2009) Nature of the ‘‘occluded’’ low-density fraction in soil organic matter studies: a critical review. Soil Sci Plant Nutr 55:13–25CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Heather M. Throckmorton
    • 1
  • Jeffrey A. Bird
    • 2
  • Nick Monte
    • 3
  • Tad Doane
    • 3
  • Mary K. Firestone
    • 4
  • William R. Horwath
    • 3
  1. 1.Los Alamos National LabLos AlamosUSA
  2. 2.Queens College CUNYFlushingUSA
  3. 3.University of CaliforniaDavisUSA
  4. 4.University of CaliforniaBerkeleyUSA

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