Biogeochemistry

, Volume 113, Issue 1–3, pp 271–281 | Cite as

Empirical evidence that soil carbon formation from plant inputs is positively related to microbial growth

  • Mark A. Bradford
  • Ashley D. Keiser
  • Christian A. Davies
  • Calley A. Mersmann
  • Michael S. Strickland
Biogeochemistry Letters

Abstract

Plant-carbon inputs to soils in the form of dissolved sugars, organic acids and amino acids fuel much of heterotrophic microbial activity belowground. Initial residence times of these compounds in the soil solution are on the order of hours, with microbial uptake a primary removal mechanism. Through microbial biosynthesis, the dissolved compounds become dominant precursors for formation of stable soil organic carbon. How the chemical class (e.g. sugar) of a dissolved compound influences stabilization in field soils is unknown and predictions from our understanding of microbial metabolism, turnover and identity are contradictory. We show that soil carbon formation, from chronic amendments of dissolved compounds to fertilized and unfertilized grasslands, is 2.4-times greater from a sugar than an amino acid. Formation rates are negatively correlated with respiration rates of the compounds, and positively correlated with their recovery in microbial biomass. These relationships suggest that the efficiency of microbial growth on a compound is positively related to formation rates of soil organic carbon. Fertilization does not alter these findings, but together nitrogen and phosphorus additions reduce soil carbon formation. Our results highlight the need to consider both nutrient enrichment and global-change induced shifts in the form of dissolved root inputs to soils to predict future soil carbon stocks and hence phenomena such as climate warming and food security to which these stock sizes are intimately tied.

Keywords

Soil organic carbon Soil carbon formation Microbial biomass Root exudation Low molecular weight carbon compounds Dissolved organic carbon 

References

  1. Ågren GI, Bosatta E (2002) Reconciling differences in predictions of temperature response of soil organic matter. Soil Biol Biochem 34:129–132CrossRefGoogle Scholar
  2. Allen SE (ed) (1989) Chemical analysis of ecological materials, 2nd edn. Blackwell Scientific, OxfordGoogle Scholar
  3. Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340CrossRefGoogle Scholar
  4. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266CrossRefGoogle Scholar
  5. Bradford MA, Wookey PA, Ineson P, Lappin-Scott HM (2001) Controlling factors and effects of chronic nitrogen and sulphur deposition on methane oxidation in a temperate forest soil. Soil Biol Biochem 33:93–102CrossRefGoogle Scholar
  6. Bradford MA, Fierer N, Reynolds JF (2008) Soil carbon stocks in experimental mesocosms are dependent on the rate of labile carbon, nitrogen and phosphorous input to soil. Func Ecol 22:964–974CrossRefGoogle Scholar
  7. Cabrera ML, Beare MHJ (1993) Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57:1007–1012CrossRefGoogle Scholar
  8. Cambardella CA, Elliott ET (1992) Particulate soil organic-matter changes across a grassland cultivation sequence. Soil Sci Soc Am J 56:777–783CrossRefGoogle Scholar
  9. Cleveland CC, Townsend AR (2006) Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Nat Soc Sci 103:10316–10321CrossRefGoogle Scholar
  10. Conant RT, Ryan MG, Ågren GI, Birge HE, Davidson EA, Eliasson PE, Evans SE, Frey SD, Giardina CP, Hopkins F, Hyvönen R, Kirschbaum MUF, Lavallee JM, Leifeld J, Parton WJ, Steinweg JM, Wallenstein MD, Wetterstedt JÅM, Bradford MA (2011) Temperature and soil organic matter decomposition rates – synthesis of current knowledge and a way forward. Global Change Biol 17:3392–3404CrossRefGoogle Scholar
  11. Cotrufo MF, Wallenstein MD, Boot C, Denef K, Paul E (2012) 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? Global Change Biol. doi:10.1111/gcb.12113
  12. Fierer N, Schimel JP (2002) Effects of drying-rewetting frequency on soil carbon and nitrogen transformations. Soil Biol Biochem 34:777–787CrossRefGoogle Scholar
  13. Fierer N, Schimel JP (2003) A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil. Soil Sci Soc Am J 67:798–805CrossRefGoogle Scholar
  14. Fischer H, Meyer A, Fischer K, Kuzyakov Y (2007) Carbohydrate and amino acid composition of dissolved organic matter leached from soil. Soil Biol Biochem 39:2926–2935CrossRefGoogle Scholar
  15. Fry B (2006) Stable isotope ecology. Springer, New YorkCrossRefGoogle Scholar
  16. 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
  17. Gulledge J, Doyle AP, Schimel JP (1997) Different NH4 +-inhibition patterns of soil CH4 consumption: a result of distinct CH4-oxidizer populations across sites. Soil Biol Biochem 29:13–21CrossRefGoogle Scholar
  18. Högberg P, Read DJ (2006) Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol 21:548–554CrossRefGoogle Scholar
  19. Hurlbert SH, Lomabardi CM (2009) Final collapse of the Neyman-Pearson decision theoretic framework and rise of the neoFisherian. Ann Zool Fenn 46:311–349CrossRefGoogle Scholar
  20. Ineson P, Cotrufo MF, Bol R, Harkness DD, Blum H (1996) Quantification of soil carbon inputs under elevated CO2: C3 plants in a C4 soil. Plant Soil 187:345–350CrossRefGoogle Scholar
  21. Jans-Hammermeister DC, McGill WB, Izaurralde RC (1997) Management of soil C by manipulation of microbial metabolism: daily vs. pulsed C additions. In: Lal R, Kimble JM, Follett RF, Stewart BA (eds) Soil processes and the carbon cycle. CRC Press, Boca Raton, pp 321–333Google Scholar
  22. Jones DL, Murphy DV (2007) Microbial response time to sugar and amino acid additions to soil. Soil Biol Biochem 39:2178–2182CrossRefGoogle Scholar
  23. Kuzyakov Y, Demin V (1998) CO2 efflux by rapid decomposition of low molecular organic substances in soils. Sciences of Soils 3:11–22CrossRefGoogle Scholar
  24. Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–1627CrossRefGoogle Scholar
  25. Lundberg P, Ekblad A, Nilsson M (2001) 13C NMR spectroscopy studies of forest soil microbial activity: glucose uptake and fatty acid biosynthesis. Soil Biol Biochem 33:621–632CrossRefGoogle Scholar
  26. Mack MC, Schuur EAG, Bret-Harte MS, Shaver GR, Chapin FS III (2004) Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431:440–443CrossRefGoogle Scholar
  27. Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2011) SOM genesis: microbial biomass as a significant source. Biogeochem. doi:10.1007/s10533-011-9658-z Google Scholar
  28. Neff JC, Townsend AR, Gleixner G, Lehman SJ, Turnbull J, Bowman WD (2002) Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419:915–917CrossRefGoogle Scholar
  29. Olk DC, Gregorich EG (2006) Overview of the symposium proceedings, “Meaningful pools in determining soil carbon and nitrogen dynamics”. Soil Sci Soc Am J 70:967–974CrossRefGoogle Scholar
  30. Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phyt 173:600–610CrossRefGoogle Scholar
  31. Paul EA, Morris SJ, Böhm S (2001) The determination of soil C pool sizes and turnover rates: biophysical fractionation and tracers. In: Lal R, Kimble JM, Follett RF, Stewart BA (eds) Assessment methods for soil carbon. CRC Press LLC, Boca Raton, pp 193–205Google Scholar
  32. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer Verlag, New YorkCrossRefGoogle Scholar
  33. Rinnan R, Bååth E (2009) Differential utilization of carbon substrates by bacteria and fungi in tundra soil. Appl Environ Microbiol 75:3611–3620CrossRefGoogle Scholar
  34. Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theorectical model. Soil Biol Biochem 35:549–563CrossRefGoogle Scholar
  35. Schlesinger WH, Lichter J (2001) Limited carbon storage in soil and litter of experimental forest plots under increased CO2. Nature 411:466–469CrossRefGoogle Scholar
  36. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56CrossRefGoogle Scholar
  37. Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils – Methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395CrossRefGoogle Scholar
  38. Strickland MS, Callaham MA Jr, Davies CA, Lauber CL, Ramirez K, Richter DD Jr, Fierer N, Bradford MA (2010) Rates of in situ carbon mineralization in relation to land-use, microbial community and edaphic characteristics. Soil Biol Biochem 42:260–269CrossRefGoogle Scholar
  39. Strickland MS, Wickings K, Bradford MA (2012) The fate of glucose, a low molecular weight compound of root exudates, in the belowground foodweb of forests and pastures. Soil Biol Biochem 42:23–29CrossRefGoogle Scholar
  40. Trumbore S (2009) Radiocarbon and soil carbon dynamics. Annu Rev Earth Planet Sci 37:47–66CrossRefGoogle Scholar
  41. Unteregelsbacher S, Hafner S, Guggenberger G, Miehe G, Xu X, Liu J, Kuzyakov Y (2011) Response of long-, medium- and short-term processes of the carbon budget to overgrazing-induced crusts in the Tibetan Plateau. Biogeochem. doi:10.1007/s10533-011-9632-9 Google Scholar
  42. van Hees PAW, Jones DL, Finlay R, Godbold DL, Lundström US (2005) The carbon we do not see-the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13CrossRefGoogle Scholar
  43. von Lützow M, Kögel-Knabner I, Ekschmitt K, Flessa H, Guggenberger G, Matzner E, Marschner B (2007) SOM fractionation methods: relevance to functional pools and to stabilization mechanisms. Soil Biol Biochem 39:2183–2207CrossRefGoogle Scholar
  44. Voroney RP, Paul EA, Anderson DW (1989) Decomposition of wheat straw and stabilization of microbial products. Can J Soil Sci 69:63–77CrossRefGoogle Scholar
  45. Wardle DA, Ghani A (1995) A critique of the microbial metabolic quotient (qCO2) as a bioindicator of disturbance and ecosystem development. Soil Biol Biochem 27:1601–1610CrossRefGoogle Scholar
  46. Webster EA, Chudek JA, Hopkins DW (1997) Fates of 13C from enriched glucose and glycine in an organic soil determined by solid-state NMR. Biol Fertil Soils 25:389–395CrossRefGoogle Scholar
  47. West AW, Sparling GP (1986) Modifications to the substrate-induced respiration method to permit measurement of microbial biomass in soils of differing water contents. J Microbiol Meth 5:177–189CrossRefGoogle Scholar
  48. Yang HS, Janssen BH (2002) Relationship between substrate initial reactivity and residues ageing speed in carbon mineralization. Plant Soil 239:215–224CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Mark A. Bradford
    • 1
  • Ashley D. Keiser
    • 1
  • Christian A. Davies
    • 2
    • 4
  • Calley A. Mersmann
    • 2
    • 5
  • Michael S. Strickland
    • 3
  1. 1.School of Forestry and Environmental StudiesYale UniversityNew HavenUSA
  2. 2.Odum School of EcologyUniversity of GeorgiaAthensUSA
  3. 3.Department of Biological SciencesVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  4. 4.Greater ManchesterUK
  5. 5.School of Public & Environmental AffairsIndiana UniversityBloomingtonUSA

Personalised recommendations