Skip to main content
Log in

Oxygen and substrate availability interactively control the temperature sensitivity of CO2 and N2O emission from soil

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

We investigated how oxygen availability, substrate amount, and quality affect the temperature dependency of enzymatic processes involved in the production of carbon dioxide (CO2) and nitrous oxide (N2O). Three substrates differing in microbial degradability (glucose with potassium nitrate, glycine, and phenylalanine) were added to a mountain grassland soil at a range of concentrations. Soils were incubated at 21 and 1 % of O2 content and at 10 and 20 °C. Oxygen availability was a main factor controlling the reaction rates and temperature sensitivity of CO2 and N2O production. The temperature sensitivity of CO2 production was higher under aerobic versus oxygen-limited conditions, and the opposite dependency was observed for the N2O production. Substrate availability was a second factor affecting the temperature sensitivity of the processes leading to the production of these gases. The temperature response was reduced under substrate limitation. Apparent activation energy for aerobic CO2 production was similar (E a ~ 30 kJ mol−1) for tested substrates, while E a for anaerobic N2O production increased in the order phenylalanine < glycine < glucose + NO3 having values 45, 75, and 106 kJ mol−1, respectively. Commonly, the temperature sensitivity of N2O production (2 < Q 10 < 4.5) was much higher than that for CO2 (Q 10 ≤ 1.5).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdalla M, Jones M, Smith P, Williams M (2009) Nitrous oxide fluxes and denitrification sensitivity to temperature in Irish pasture soils. Soil Use Manage 25:376–388. doi:10.1111/j.1475-2743.2009.00237.x

    Article  Google Scholar 

  • Blagodatsky SA, Yevdokimov IV (1998) Extractability of microbial N as influenced by C:N ratio in the flush after drying or fumigation. Biol Fertil Soils 28:5–11

    Article  CAS  Google Scholar 

  • Blagodatsky SA, Kesik M, Papen H, Butterbach-Bahl K (2006) Production of NO and N2O by the heterotrophic nitrifier Alcaligenes faecalis parafaecalis under varying conditions of oxygen saturation. Geomicrobiol J 23:165–176

    Article  CAS  Google Scholar 

  • Bond-Lamberty B, Thomson A (2010) Temperature-associated increases in the global soil respiration record. Nature 464:579–582

    Article  CAS  PubMed  Google Scholar 

  • Bradford MA, Davies CA, Frey SD, Maddox TR, Melillo JM, Mohan JE, Reynolds JF, Treseder KK, Wallenstein MD (2008) Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Let 11:1316–1327

    Article  Google Scholar 

  • Braker G, Dorsch P, Bakken LR (2012) Genetic characterization of denitrifier communities with contrasting intrinsic functional traits. FEMS Microbiol Ecol 79:542–554

    Article  CAS  PubMed  Google Scholar 

  • Butterbach-Bahl K, Baggs EM, Dannenmann M, Kiese R, Zechmeister-Boltenstern S (2013) Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos T R Soc B 368:20130122. doi:10.1098/rstb.2013.0122

    Article  Google Scholar 

  • Butterbach-Bahl K, Dannenmann M (2011) Denitrification and associated soil N2O emissions due to agricultural activities in a changing climate. Curr Opin Environ Sust 3:389–395. doi:10.1016/j.cosust.2011.08.004

    Article  Google Scholar 

  • Castaldi S (2000) Responses of nitrous oxide, dinitrogen and carbon dioxide production and oxygen consumption to temperature in forest and agricultural light-textured soils determined by model experiment. Biol Fertil Soils 32:67–72. doi:10.1007/s003740000218

    Article  CAS  Google Scholar 

  • Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440. doi:10.1038/nature04514

  • Davidson EA, Samanta S, Caramori SS, Savage K (2012) The Dual Arrhenius and Michaelis–Menten kinetics model for decomposition of soil organic matter at hourly to seasonal time scales. Glob Change Biol 18:371–384

    Article  Google Scholar 

  • DIN ISO 13878, November 1998. Bodenbeschaffenheit - Bestimmung des Gesamt-Stickstoffs durch trockene Verbrennung (Elementaranalyse) (ISO 13878:1998). Deutsches Institut für Normung e. V. (Herausgeber); Berlin, Beuth Verlag GmbH

  • DIN ISO 10694, August 1996. Bodenbeschaffenheit - Bestimmung von organischem Kohlenstoff und Gesamtkohlenstoff nach trockener Verbrennung (Elementaranalyse) (ISO 10694:1995). Deutsches Institut für Normung e. V. (Herausgeber); Berlin, Beuth Verlag GmbH

  • Gershenson A, Bader NE, Cheng W (2009) Effects of substrate availability on the temperature sensitivity of soil organic matter decomposition. Glob Change Biol 15:176–183

    Article  Google Scholar 

  • Hartley IP, Heinemeyer A, Ineson P (2007) Effects of three years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response. Glob Change Biol 13:1761–1770

    Article  Google Scholar 

  • Hartley IP, Hopkins DW, Sommerkorn M, Wookey PA (2010) The response of organic matter mineralisation to nutrient and substrate additions in sub-arctic soils. Soil Biol Biochem 42:92–100

    Article  CAS  Google Scholar 

  • Heimann M, Reichstein M (2008) Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature (London) 451. doi:10.1038/nature06591

  • Hobbie J, Hobbie E (2012) Amino acid cycling in plankton and soil microbes studied with radioisotopes: measured amino acids in soil do not reflect bioavailability. Biogeochem 107:339–360

    Article  CAS  Google Scholar 

  • Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (2000) Competition between roots and soil micro-organisms for nutrients from nitrogen-rich patches of varying complexity. J Ecol 88:150–164

    Article  Google Scholar 

  • Hoffmann G (1991) Methodenbuch Band 1, Die Untersuchung von Böden, 4th edn. VDLUFA Verlag, Darmstadt

    Google Scholar 

  • Holtan-Hartwig L, Dorsch P, Bakken LR (2000) Comparison of denitrifying communities in organic soils: kinetics of NO3 and N2O reduction. Soil Biol Biochem 32:833–843

    Article  CAS  Google Scholar 

  • Holtan-Hartwig L, Dorsch P, Bakken LR (2002) Low temperature control of soil denitrifying communities: kinetics of N2O production and reduction. Soil Biol Biochem 34:1797–1806

    Article  CAS  Google Scholar 

  • Hopkins DW, Sparrow AD, Elberling B, Gregorich EG, Novis PM, Greenfield LG, Tilston EL (2006) Carbon, nitrogen and temperature controls on microbial activity in soils from an Antarctic dry valley. Soil Biol Biochem 38:3130–3140. doi:10.1016/j.soilbio.2006.01.012

    Article  CAS  Google Scholar 

  • Jones DL, Kielland K (2002) Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils. Soil Biol Biochem 34:209–219

    Article  CAS  Google Scholar 

  • Khalili B, Nourbakhsh F, Nili N, Khademi H, Sharifnabi B (2011) Diversity of soil cellulase isoenzymes is associated with soil cellulase kinetic and thermodynamic parameters. Soil Biol Biochem 43:1639–1648

    Article  CAS  Google Scholar 

  • Kirschbaum MUF (2006) The temperature dependence of organic-matter decomposition—still a topic of debate. Soil Biol Biochem 38:2510–2518

    Article  CAS  Google Scholar 

  • Kool DM, Dolfing J, Wrage N, Van Groenigen JW (2011) Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biol Biochem 43:174–178

    Article  CAS  Google Scholar 

  • Larionova AA, Yevdokimov IV, Bykhovets SS (2007) Temperature response of soil respiration is dependent on concentration of readily decomposable C. Biogeosciences 4:1073–1081

    Article  CAS  Google Scholar 

  • McLain JET, Martens DA (2005) Nitrous oxide flux from soil amino acid mineralization. Soil Biol Biochem 37:289–299

    Article  CAS  Google Scholar 

  • ModelMaker (1997) ModelMaker© Version 3.0.3 Software. Cherwell Scientific Publishing Limited, Oxford.

  • O’Down RW, Hopkins DW (1998) Mineralization of carbon from D- and L-amino acids and D-glucose in two contrasting soils. Soil Biol Biochem 30:2009–2016

    Article  Google Scholar 

  • Oquist MG, Nilsson M, Sorensson F, Kasimir-Klemedtsson A, Persson T, Weslien P, Klemedtsson L (2004) Nitrous oxide production in a forest soil at low temperatures—processes and environmental controls. FEMS Microbiol Ecol 49:371–378

    Article  CAS  PubMed  Google Scholar 

  • Panikov NS, Blagodatsky SA, Blagodatskaya JV, Glagolev MV (1992) Determination of microbial mineralization activity in soil by modified Wright and Hobbie method. Biol Fertil Soils 14:280–287

    Article  CAS  Google Scholar 

  • Paul EA (2007) Soil microbiology, ecology, and biochemistry. Academic, Amsterdam

    Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602

    Article  Google Scholar 

  • Smith KA (1997) The potential for feedback effects induced by global warming on emissions of nitrous oxide by soils. Glob Change Biol 3:327–338

    Google Scholar 

  • Unteregelsbacher S, Gasche R, Lipp L, Sun W, Kreyling O, Geitlinger H, Kögel-Knabner I, Papen H, Kiese R, Schmid HP, Dannenmann M (2013) Increased methane uptake but unchanged nitrous oxide flux in pre-alpine grasslands under simulated climate change conditions. Eur J Soil Sci 64:586–596. doi:10.1111/ejss.12092

    Article  CAS  Google Scholar 

  • Veraart AJ, de Klein JJM, Scheffer M (2011) Warming can boost denitrification disproportionately due to altered oxygen dynamics. Plos One 6. doi:10.1371/journal.pone.0018508

  • Vinolas LC, Vallejo VR, Jones DL (2001) Control of amino acid mineralization and microbial metabolism by temperature. Soil Biol Biochem 33:1137–1140

    Article  CAS  Google Scholar 

  • von Lützow M, Kögel-Knabner I (2009) Temperature sensitivity of soil organic matter decomposition—what do we know? Biol Fertil Soils 46:1–15

    Article  Google Scholar 

  • Zhu T, Zhang J, Yang W, Cai Z (2013) Effects of organic material amendment and water content on NO, N2O, and N2 emissions in a nitrate-rich vegetable soil. Biol Fertil Soils 49:153–164

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Olivia Kreyling (Technical University of Munich) for analysis of soil C and N content and two anonymous reviewers for helpful comments. We are highly indebted to Editor-in-Chief Professor Paolo Nannipieri for substantial improvement of the manuscript. This work was supported by Russian Foundation of Basic Research (Project No 12-04-01170-а), by the Chinese Academy of Sciences (Visiting Professor Fellowship for EB) and by the Helmholtz Society program ATMO. Further support was provided by the TERENO initiative of Helmholtz Society and BMBF and by the FORKAST project funded by the Bavarian Government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Blagodatsky.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blagodatskaya, Е., Zheng, X., Blagodatsky, S. et al. Oxygen and substrate availability interactively control the temperature sensitivity of CO2 and N2O emission from soil. Biol Fertil Soils 50, 775–783 (2014). https://doi.org/10.1007/s00374-014-0899-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-014-0899-6

Keywords

Navigation