Plant and Soil

, Volume 376, Issue 1–2, pp 61–73 | Cite as

Translocation and turnover of rhizodeposit carbon within soil microbial communities of an extensive grassland ecosystem

  • Wajira K. Balasooriya
  • Karolien Denef
  • Dries Huygens
  • Pascal Boeckx
Regular Article


Background and Aims

A substantial amount of photosynthesized plant-C is allocated belowground in grassland ecosystems where it influences the structure and function of the soil microbial community with potential implications for C cycling and storage. We applied stable isotope probing of microbial PLFAs and repeated soil sampling in a grassland over a period of 1 year to assess the role of microbial communities in the cycling of rhizodeposit-C.


Pulse-labeling with 13CO2 was performed in a grassland site near Gent (Belgium). Soil samples were taken 24 h, 1 week, 1 month, 4 months, 9 months and 1 year following labeling and analyzed for 13C in soil, roots and microbial PLFAs.


C enrichment of PLFAs occurred rapidly (within 24 h) but temporally varied across microbial groups. PLFAs indicative for fungi and gram-negative bacteria showed a faster 13C uptake compared to gram-positive bacteria and actinomycetes. However, the relative 13C concentrations of the latter communities increased after 1 week, while those of fungi decreased and those of gram-negative bacteria remained constant. PLFA 13C mean residence times were much shorter for fungi compared to bacteria and actinomycetes.


Our results indicate temporally varying rhizodeposit-C uptake by different microbial groups, and faster turnover rates of mycorrhizal versus saprotrophic fungi and fungi versus bacteria. Fungi appeared to play a major role in the initial processing and possible rapid channeling of rhizodeposit-C into the soil microbial community. Actinomycetes and gram-positive bacteria appeared to have a delayed utilization of rhizodeposit-C or to prefer other C sources upon rhizodeposition.


13C Pulse-labeling Rhizodeposition Soil microbial community structure SIP-PLFA Microbial carbon turnover 



Phospholipid fatty acid


Fatty acid methyl ester


Stable isotope probing


Gas chromatography combustion isotope ratio mass spectrometry


Mean residence time



The authors wish to thank Dries Roobroeck, Davy Loete, Katja Van Nieuland and Jan Vermeulen for assistance with pulse-labeling, sample collection and laboratory analyses. This study was funded by the special research fund (BOF) of Ghent University. Dries Huygens is a postdoctoral fellow of the Fund for Scientific Research—Flanders (FWO).


  1. Bago B, Azcon-Aguilar C, Goulet A, Piché Y (1998) Branched absorbing structures (BAS): a feature of the extraradical mycelium of symbiotic arbuscular mycorrhizal fungi. New Phytol 139:375–388CrossRefGoogle Scholar
  2. Bailey VL, Smith JL, Bolton H (2002) Fungal-to-bacterial ratios in soils investigated for enhanced C sequestration. Soil Biol Biochem 34(7):997–1007Google Scholar
  3. Balasooriya WK, Denef K, Peters J, Verhoest N, Boeckx P (2008) Vegetation composition and soil microbial community structural changes along a wetland hydrological gradient. Hydrol Earth Syst Sc 12:277–291Google Scholar
  4. Bird JA, Herman DJ, Firestone MK (2011) Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biol Biochem 43(4):718–725. doi: 10.1016/j.soilbio.2010.08.010 CrossRefGoogle Scholar
  5. Bossio DA, Scow KM (1995) Impact of carbon and flooding on the metabolic diversity of microbial communities in soils. Appl Environ Microbiol 61:4043–4050PubMedCentralPubMedGoogle Scholar
  6. Butler JL, Williams MA, Bottomley PJ, Myrold DD (2003) Microbial community dynamics associated with rhizosphere carbon flow. Appl Environ Microbiol 69:6793–6800PubMedCentralPubMedCrossRefGoogle Scholar
  7. Butler JL, Bottomley PJ, Griffith SM, Myrold DD (2004) Distribution and turnover of recently fixed photosynthate in ryegrass rhizospheres. Soil Biol Biochem 36:371–382CrossRefGoogle Scholar
  8. Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci U S A 104(12):4990–4995. doi: 10.1073/pnas.0610045104 PubMedCentralPubMedCrossRefGoogle Scholar
  9. Decock C, Denef K, Bode S, Six J, Boeckx P (2009) Critical assessment of the applicability of gas chromatography-combustion-isotope ratio mass spectrometry to determine amino sugar dynamics in soil. Rapid Commun Mass Sp 23(8):1201–1211. doi: 10.1002/rcm.3990
  10. De Deyn GB, Quirk H, Oakley S, Ostle N, Bardgett RD (2011) Rapid transfer of photosynthetic carbon through the plant-soil system in differently managed species-rich grasslands. Biogeosciences 8(5):1131–1139. doi: 10.5194/bg-8-1131-2011 CrossRefGoogle Scholar
  11. Denef K, Bubenheim H, Lenhart K, Vermeulen J, Van Cleemput O, Boeckx P, Muller C (2007) Community shifts and carbon translocation within metabolically-active rhizosphere microorganisms in grasslands under elevated CO2. Biogeosciences 4:769–779CrossRefGoogle Scholar
  12. Denef K, Roobroeck D, Wadu M, Lootens P, Boeckx P (2009) Microbial community composition and rhizodeposit-carbon assimilation in differently managed temperate grassland soils. Soil Biol Biochem 41(1):144–153. doi: 10.1016/j.soilbio.2008.10.008 CrossRefGoogle Scholar
  13. Drigo B, Pijl AS, Duyts H, Kielak A, Gamper HA, Houtekamer MJ (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO. Proc Natl Acad Sci USA 107:10938–10942PubMedCrossRefGoogle Scholar
  14. Frostegård A, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65CrossRefGoogle Scholar
  15. Grayston SJ, Griffith GS, Mawdsley JL, Campbell CD, Bardgett RD (2001) Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol Biochem 33:533–551CrossRefGoogle Scholar
  16. Guggenberger G, Frey SD, Six J, Paustian K, Elliott ET (1999) Bacterial and fungal cell-wall residues in conventional and no-tillage agroecosystems. Soil Sci Soc Am J 63(5):1188–1198Google Scholar
  17. Hamilton EW, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82(9):2397–2402. doi: 10.1890/0012-9658(2001) 082[2397:cpssma];2 CrossRefGoogle Scholar
  18. He HB, Li XB, Zhang W, Zhang XD (2011) Differentiating the dynamics of native and newly immobilized amino sugars in soil frequently amended with inorganic nitrogen and glucose. Eur J Soil Sci 62(1):144–151. doi: 10.1111/j.1365-2389.2010.01324.x Google Scholar
  19. Hedrick DB, Peacock AD, Lovley DR, Woodard TL, Nevin KP, Long PE, White DC (2009) Polar lipid fatty acids, LPS-hydroxy fatty acids, and respiratory quinones of three Geobacter strains, and variation with electron acceptor. J Ind Microbiol Biotechnol 36:205–209PubMedCrossRefGoogle Scholar
  20. Hogberg P, Hogberg MN, Gottlicher SG, Betson NR, Keel SG, Metcalfe DB, Campbell C, Schindlbacher A, Hurry V, Lundmark T, Linder S, Nasholm T (2008) High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytol 177(1):220–228. doi: 10.1111/j.1469-8137.2007.02238.x PubMedGoogle Scholar
  21. Hütsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition—an important source for carbon turnover in soils. J Plant Nutr Soil Sci 165:397–407CrossRefGoogle Scholar
  22. Jefferies RL, Walker NA, Edwards KA, Dainty J (2010) Is the decline of soil microbial biomass in late winter coupled to changes in the physical state of cold soils? Soil Biol Biochem 42(2):129–135. doi: 10.1016/j.soilbio.2009.10.008 Google Scholar
  23. Jin VL, Evans RD (2010) Microbial 13C utilization patterns via stable isotope probing of phospholipid biomarkers in Mojave Desert soils exposed to ambient and elevated atmospheric CO2. Glob Change Biol 16(8):2334–2344. doi: 10.1111/j.1365-2486.2010.02207.x CrossRefGoogle Scholar
  24. Johnson D, Leake JR, Read DJ (2002) Transfer to recent photosynthate into mycorrhizal mycelium of an upland grassland: short-term respiratory losses and accumulation of 14 C. Soil Biol Biochem 34:1521–1524CrossRefGoogle Scholar
  25. Kaiser C, Frank A, Wild B, Koranda M, Richter A (2010) Negligible contribution from roots to soil-borne phospholipid fatty acid fungal biomarkers 18:2ω6,9 and 18:1ω9. Soil Biol Biochem 42:1650–1652PubMedCentralPubMedCrossRefGoogle Scholar
  26. Kaštovská E, Šantrůčková H (2007) Fate and dynamics of recently fixed C in pasture plant-soil system under field conditions. Plant Soil 300:61–69CrossRefGoogle Scholar
  27. Klironomos JN, Ursic M (1998) Density-dependent grazing on the extraradical hyphal network of the arbuscular mycorrhizal fungus, Glomus intraradices, by the collembolan, Folsomia candida. Biol Fertil Soils 26:250–253CrossRefGoogle Scholar
  28. Kuzyakov Y (2002) Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci-Zeitschrift Fur Pflanzenernahrung Und Bodenkunde 165(4):382–396. doi: 10.1002/1522-2624(200208)165:4<382::aid-jpln382>;2-# CrossRefGoogle Scholar
  29. Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42(9):1363–1371. doi: 10.1016/j.soilbio.2010.04.003 CrossRefGoogle Scholar
  30. Kuzyakov Y, Cheng W (2001) Photosynthesis controls of rhizosphere respiration and organic matter decomposition. Soil Biol Biochem 33:1915–1925CrossRefGoogle Scholar
  31. Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. J Plant Nutr Soil Sci 163:421–431CrossRefGoogle Scholar
  32. Laczko E, Boller T, Wiemken V (2004) Lipids in roots of Pinus sylvestris seedlings and in mycelia of Pisolithus tinctorius during ectomycorrhiza formation: changes in fatty acid and sterol composition in a beech forest soil. Plant Cell Environ 27:27–40CrossRefGoogle Scholar
  33. Leake JR, Ostle NJ, Rangel-Castro JI, Johnson D (2006) Carbon fluxes from plants through soil organisms determined by field (CO2)-C-13 pulse-labeling in an upland grassland. Appl Soil Ecol 33:152–175CrossRefGoogle Scholar
  34. Lu Y, Watanabe A, Kimura M (2002) Contributions of plant derived carbon to soil microbial biomass dynamics in a paddy rice microcosm. Biol Fertil Soils 36:136–142CrossRefGoogle Scholar
  35. Lu Y, Murase J, Watanabe A, Sugimoto A, Kimura M (2004) Linking microbial community dynamics to rhizosphere carbon flow in a wetland rice soil. FEMS Microbiol Ecol 48:179–186PubMedCrossRefGoogle Scholar
  36. Olsson PA, Johnson NC (2005) Tracking carbon from the atmosphere to the rhizosphere. Ecol Lett 8:1264–1270CrossRefGoogle Scholar
  37. Olsson PA, Bååth E, Jacobsen I, Soderstrom B (1995) The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol Res 99:623–629CrossRefGoogle Scholar
  38. Ostle N, Ineson P, Benham D, Sleep D (2000) Carbon assimilation and turnover in grassland vegetation using an in situ 13CO2 pulse labelling system. Rapid Comm Mass Spectrom 14:1345–1350CrossRefGoogle Scholar
  39. Ostle N, Whiteley AS, Bailey MJ, Sleep D, Ineson P, Mane-field M (2003) Active microbial RNA turnover in a grassland soil estimated using a 13CO2 spike. Soil Biol Biochem 35:877–885CrossRefGoogle Scholar
  40. Ostle NJ, Levy PE, Evans CD, Smith P (2009) UK land use and soil carbon sequestration. Land Use Policy 26:S274–S283. doi: 10.1016/j.landusepol.2009.08.006 CrossRefGoogle Scholar
  41. Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173(3):600–610. doi: 10.1111/j.1469-8137.2006.01931.x PubMedCrossRefGoogle Scholar
  42. Paterson E, Midwood AJ, Millard P (2009) Through the eye of the needle: a review of isotope approaches to quantify microbial processes mediating soil carbon balance. New Phytol 184(1):19–33. doi: 10.1111/j.1469-8137.2009.03001.x PubMedCrossRefGoogle Scholar
  43. Potthoff M, Steenwerth KL, Jackson LE, Drenovsky RE, Scow KM, Joergensen RG (2006) Soil microbial community composition as affected by restoration practices in California grassland. Soil Biol Biochem 38:1851–1860CrossRefGoogle Scholar
  44. Quinton JN, Govers G, Van Oost K, Bardgett RD (2010) The impact of agricultural soil erosion on biogeochemical cycling. Nat Geosci 3(5):311–314. doi: 10.1038/ngeo838 CrossRefGoogle Scholar
  45. Rangel-Castro JI, Prosser JI, Scrimgeour CM, Smith P, Ostle N, Ineson P, Meharg AA, Killham K (2004) Carbon flow in an upland grassland: effect of liming on the flux of recently photosynthesized carbon to rhizosphere soil. Glob Change Biol 10:2100–2108CrossRefGoogle Scholar
  46. Rangel-Castro JI, Killham K, Ostle N, Nicol GW, Anderson IC, Scrimgeour CM, Ineson P, Meharg A, Prosser JI (2005a) Stable isotope probing analysis of the influence of liming on root exudate utilization by soil microorganisms. Environ Microbiol 7(6):828–838PubMedCrossRefGoogle Scholar
  47. Rangel-Castro JI, Prosser JI, Ostle N, Scrimgeour CM, Killham K, Meharg AA (2005b) Flux and turnover of fixed carbon in soil microbial biomass of limed and unlimed plots of an upland grassland ecosystem. Environ Microbiol 7:544–552PubMedCrossRefGoogle Scholar
  48. Rattray EAS, Paterson E, Killham K (1995) Characterization of the dynamics of C-partitioning within Lolium perenne and to the rhizosphere microbial biomass using 14 C pulse chase. Biol Fertil Soils 19:280–286CrossRefGoogle Scholar
  49. Rousk J, Baath E (2007) Fungal biomass production and turnover in soil estimated using the acetate-in-ergosterol technique. Soil Biol Biochem 39(8):2173–2177. doi: 10.1016/j.soilbio.2007.03.023 CrossRefGoogle Scholar
  50. Ruess L, Chamberlain PM (2010) The fat that matters: soil food web analysis using fatty acids and their carbon stable isotope signature. Soil Biol Biochem 42:1898–1910CrossRefGoogle Scholar
  51. Saggar S, Hedley CB (2001) Estimating seasonal and annual carbon inputs, and root decomposition rates in a temperate pasture following field 14 C pulse-labelling. Plant Soil 236:91–103CrossRefGoogle Scholar
  52. Simpson RT, Frey SD, Six J, Thiet RK (2004) Preferential accumulation of microbial carbon in aggregate structures of no-tillage soils. Soil Sci Soc Am J 68(4):1249–1255Google Scholar
  53. Singh BK, Millard P, Whiteley AS, Murrell JC (2004) Unravelling rhizosphere-microbial interactions: opportunities and limitations. Trends Microbiol 12:386–393PubMedCrossRefGoogle Scholar
  54. 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 Till Res 79(1):7–31Google Scholar
  55. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70(2):555–569CrossRefGoogle Scholar
  56. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, San DiegoGoogle Scholar
  57. Staddon PL, Ostle N, Dawson LA, Fitter AH (2003) The speed of soil carbon throughput in an upland grassland is increased by liming. J Exp Bot 54:1461–1469PubMedCrossRefGoogle Scholar
  58. Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils—Methods, controls, and ecosystem implications. Soil Biol Biochem 42(9):1385–1395. doi: 10.1016/j.soilbio.2010.05.007 CrossRefGoogle Scholar
  59. Treonis AM, Ostle NJ, Stott AW, Primrose R, Graystone SJ, Ineson P (2004) Identification of groups of metabolicallyactive rhizosphere microorganisms by stable isotope probing of PLFAs. Soil Biol Biochem 36:533–537CrossRefGoogle Scholar
  60. Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ (1999) Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Evol Microbiol 49:705–724Google Scholar
  61. Waldrop MP, Firestone MK (2004) Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138:275–284PubMedCrossRefGoogle Scholar
  62. Zelles L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35:275–294PubMedCrossRefGoogle Scholar
  63. Zhang CLL, Li YL, Ye Q, Fong J, Peacock AD, Blunt E (2003) Carbon isotope signatures of fatty acids in Geobacter metallireducens and Shewanella algae. Chem Geol 195:17–28CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Wajira K. Balasooriya
    • 1
  • Karolien Denef
    • 2
  • Dries Huygens
    • 1
    • 3
  • Pascal Boeckx
    • 1
  1. 1.Isotope Bioscience Laboratory—ISOFYSGhent UniversityGhentBelgium
  2. 2.Natural Resource Ecology LaboratoryColorado State UniversityFort CollinsUSA
  3. 3.Institute of Agricultural Engineering and Soil Science, Faculty of Agricultural SciencesUniversidad Austral de ChileValdiviaChile

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