Abstract
The fate of low molecular weight organic substances (LMWOSs) in soil is regulated by microbial uptake. However, C oxidation state, the number of C atoms and –COOH groups in the LMWOS can affect their microbial utilization. Thus, the aim of this study was to reveal the effects of substance chemical properties on initial uptake and utilization of sugars, carboxylic and amino acids by microorganisms. Soil solution, spiked with 14C-labelled glucose, fructose, malate, succinate, formate, alanine or glycine, was added to the soil and 14C was traced in the soil solution, CO2, cytosol, and soil organic carbon (SOC) over 24 h. The half-life time of all LMWOS in the soil solution varied between 0.6 min (formic acid) and 5.0 min (sugars), indicating its dependence on C oxidation state of the substances. The half-life time of 14C in the fast mineralized pool in microorganisms, ranged between 30 (malic acid) and 80 (glycine) min and was independent on either C oxidation state, the number of C atoms, or number of –COOH groups. This suggests that intercellular metabolic pathways are more important for LMWOS transformation in soil than their basic chemical properties. The portion of mineralized LMWOS increased with their C oxidation state (20% for sugars vs. 90% for formic acid) corresponding to the decrease of C incorporated into the cytosol and SOC pools. Concluding, the physicochemical properties of the common LMWOS allow predicting their microbial uptake from soil solution and subsequent partitioning of C within microbial biomass.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmed IU, Smith AR, Jones DL, Godbold DL (2016) Tree species identity influences the vertical distribution of labile and recalcitrant carbon in a temperate deciduous forest soil. Special Section: Forests, Roots and Soil Carbon. For Ecol Manag 359:352–360
Apostel C, Dippold MA, Glaser B, Kuzyakov Y (2013) Biochemical pathways of amino acids in soil. Assessment by position-specific labeling and 13C-PLFA analysis. Soil Biol Biochem 67:31–40
Apostel C, Dippold M, Kuzyakov Y (2015) Biochemistry of hexose and pentose transformations in soil analyzed by position-specific labeling and 13C-PLFA. Soil Biol Biochem 80:199–208
Blagodatskaya E, Kuzyakov Y (2013) Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol Biochem 67:192–211
Boddy E, Hill PW, Farrar J, Jones DL (2007) Fast turnover of low molecular weight components of the dissolved organic carbon pool of temperate grassland field soils. Soil Biol Biochem 39:827–835
Dijkstra P, Dalder JJ, Selmants PC, Hart SC, Koch GW, Schwartz E, Hungate BA (2011) Modeling soil metabolic processes using isotopologue pairs of position-specific 13C-labeled glucose and pyruvate. Soil Biol Biochem 43:1848–1857
Dippold MA, Kuzyakov Y (2013) Biogeochemical transformations of amino acids in soil assessed by position-specific labelling. Plant Soil. doi:10.1007/s11104-013-1764-3
Dippold MA, Boesel S, Gunina A, Kuzyakov Y, Glaser B (2014) Improved delta C-13 analysis of amino sugars in soil by ion chromatography-oxidation-isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 28:569–576
Fischer H, Kuzyakov Y (2010) Sorption, microbial uptake and decomposition of acetate in soil. Transformations revealed by position-specific 14C labeling. Soil Biol Biochem 42:186–192
Fischer H, Ingwersen J, Kuzyakov Y (2010) Microbial uptake of low-molecular-weight organic substances out-competes sorption in soil. Eur J Soil Sci 61:504–513
Glanville H, Rousk J, Golyshin P, Jones DL (2012) Mineralization of low molecular weight carbon substrates in soil solution under laboratory and field conditions. Soil Biol Biochem 48:88–95
Glanville HC, Hill PW, Schnepf A, Oburger E, Jones DL (2016) Combined use of empirical data and mathematical modelling to better estimate the microbial turnover of isotopically labelled carbon substrates in soil. Soil Biol Biochem 94:154–168
Grayston SJ, Vaughan D, Jones D (1997) Rhizosphere carbon flow in trees, in comparison with annual plants. The importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56
Gunina A, Kuzyakov Y (2015) Sugars in soil and sweets for microorganisms. Review of origin, content, composition and fate. Soil Biol Biochem. doi:10.1016/j.soilbio.2015.07.021
Gunina A, Dippold M, Glaser B, Kuzyakov Y (2014) Fate of low molecular weight organic substances in an arable soil. From microbial uptake to utilisation and stabilisation. Soil Biol Biochem 77:304–313
Herlihy LJ, Galloway JN, Mills AL (1987) Bacterial utilization of formic and acetic acid in rainwater. Atmos Environ (1967) 21:2397–2402
Hill PW, Farrar JF, Jones DL (2008) Decoupling of microbial glucose uptake and mineralization in soil. Soil Biol Biochem 40:616–624
Hill PW, Farrell M, Jones DL (2012) Bigger may be better in soil N cycling: does rapid acquisition of small peptides by soil microbes dominate fluxes of protein-derived N in soil. Soil Biol Biochem 48:106–112
Jones DL, Edwards AC (1998) Influence of sorption on the biological utilization of two simple carbon substrates. Soil Biol Biochem 30:1895–1902
Jones DL, Hodge A (1999) Biodegradation kinetics and sorption reactions of three differently charged amino acids in soil and their effects on plant organic nitrogen availability. Soil Biol Biochem 31:1331–1342
Keseler I, Bonavides-Martinez C, Collado-Vides J, Gama-Castro S, Gunsalus R, Johnson D, Krummenacker M, Nolan L, Paley S, Paulsen I, Peralta-Gil M, Santos-Zavaleta A, Shearer A, Karp P (2009) A comprehensive view of Escherichia coli biology. Nucleic Acids Res 37:D464–D470
Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199
Lengeler JW, Drews G, Schlegel HG (1999) Biology of the prokaryotes. Georg Thieme Verlag, Stuttgart
Roels JA (1980) Application of macroscopic principles to microbial metabolism. Biotechnol Bioeng 22:2457–2514
Smith A, Lukac M, Hood R, Healey JR, Miglietta F, Godbold DL (2013) Elevated CO2 enrichment induces a differential biomass response in a mixed species temperate forest plantation. N Phytol 198:156–168
van Hees PAW, Jones DL, Godbold DL (2002) Biodegradation of low molecular weight organic acids in coniferous forest podzolic soils. Soil Biol Biochem 34:1261–1272
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 37:1–13
World reference base (WRB) for soil resources (2006) World Soil Resources Reports No. 103. FAO, Rome
Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass C by fumigation extraction—an automated procedure. Soil Biol Biochem 22:1167–1169
Acknowledgements
This study was supported by a Scholarship from the Erasmus Mundus Joint Doctoral Programme “Forest and Nature for Society” (FONASO) awarded to A. Gunina. This study was supported by the German Research Foundation (FOR 918) within the Research Unit “Carbon Flow in Belowground Food Webs assessed by Isotope Tracers” (Project KU 1184/13-2).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Edward Brzostek.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gunina, A., Smith, A.R., Kuzyakov, Y. et al. Microbial uptake and utilization of low molecular weight organic substrates in soil depend on carbon oxidation state. Biogeochemistry 133, 89–100 (2017). https://doi.org/10.1007/s10533-017-0313-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-017-0313-1