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).
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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
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
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
Bond-Lamberty B, Thomson A (2010) Temperature-associated increases in the global soil respiration record. Nature 464:579–582
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
Braker G, Dorsch P, Bakken LR (2012) Genetic characterization of denitrifier communities with contrasting intrinsic functional traits. FEMS Microbiol Ecol 79:542–554
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
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
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
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
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
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
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
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
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
Hoffmann G (1991) Methodenbuch Band 1, Die Untersuchung von Böden, 4th edn. VDLUFA Verlag, Darmstadt
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
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
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
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
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
Kirschbaum MUF (2006) The temperature dependence of organic-matter decomposition—still a topic of debate. Soil Biol Biochem 38:2510–2518
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
Larionova AA, Yevdokimov IV, Bykhovets SS (2007) Temperature response of soil respiration is dependent on concentration of readily decomposable C. Biogeosciences 4:1073–1081
McLain JET, Martens DA (2005) Nitrous oxide flux from soil amino acid mineralization. Soil Biol Biochem 37:289–299
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
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
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
Paul EA (2007) Soil microbiology, ecology, and biochemistry. Academic, Amsterdam
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602
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
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
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
von Lützow M, Kögel-Knabner I (2009) Temperature sensitivity of soil organic matter decomposition—what do we know? Biol Fertil Soils 46:1–15
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
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.
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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
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DOI: https://doi.org/10.1007/s00374-014-0899-6