[en] Levels of N-cycle gene transcripts (nirK, nirS, nosZ, amoA) were measured during an N2O emission peak in an agricultural soil. Automated dynamic closed chambers were used to monitor an N2O emission peak on a maize crop after a natural rainfall. The peak occurred rapidly after the rainfall began. Spatial and temporal variability in N2O emission was observed between chambers. An analysis of N-cycle gene transcript levels revealed an increase in bacterial amoA gene transcripts (but not in archaeal amoA transcripts), correlating strongly with N2O emission. This suggests the involvement of nitrification enzymes, despite a high water-filled pore space (80%). Reverse transcription of bacterial 16S rRNA followed by partial sequencing of the resulting cDNAs revealed few rainfall-induced changes in the potentially active bacterial community, and notably no significant change in the relative abundance of 16S rRNAs from the nitrifier genus Nitrosospira. Expression of the amoA gene appears as a possible proxy for monitoring the N2O emission peak. To our knowledge, this is the first experiment to evaluate the expression of N-cycle genes during an N2O emission peak on an agricultural field.
Disciplines :
Microbiology
Author, co-author :
Theodorakopoulos, Nicolas ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbiologie et génomique
Lognoul, Margaux ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Phytotechnie des régions tempérées
Degrune, Florine ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbiologie et génomique
Broux, François ; Université de Liège > Ingénierie des biosystèmes (Biose) > Echanges Ecosystèmes - Atmosphère
Regaert, Donat
Muys, Céline
Heinesch, Bernard ; Université de Liège > Ingénierie des biosystèmes (Biose) > Echanges Ecosystèmes - Atmosphère
Bodson, Bernard ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Phytotechnie des régions tempérées
Aubinet, Marc ; Université de Liège > Ingénierie des biosystèmes (Biose) > Echanges Ecosystèmes - Atmosphère
Vandenbol, Micheline ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbiologie et génomique
Language :
English
Title :
Increased expression of bacterial amoA during an N2O emission peak in an agricultural field
Ambus, P., Christensen, S., Measurement of N2O emission from a fertilized grassland: an analysis of spatial variability. J. Geophys. Res. 99 (1994), 16549–16555.
Anderson, M.J., A new method for non-parametric multivariate analysis of variance. Aust. Ecol. 26 (2001), 32–48.
Aoi, Y., Masaki, Y., Tsuneda, S., Hirata, A., Quantitative analysis of amoA mRNA expression as a new biomarker of ammonia oxidation activities in a complex microbial community. Lett. Appl. Microbiol. 39 (2004), 477–482.
Avrahami, S., Conrad, R., Braker, G., Effect of soil ammonium concentration on N2O release and on the community structure of ammonia oxidizers and denitrifiers. Appl. Environ. Microbiol. 68 (2002), 5685–5692.
Bakken, L.R., Bergaust, L., Liu, B., Frostegård, Å., Regulation of denitrification at the cellular level: a clue to the understanding of N2O emissions from soils. Philos. Trans. R. Soc. B Biol. Sci. 367 (2012), 1226–1234.
Ball, B.C., Soil structure and greenhouse gas emissions: a synthesis of 20 years of experimentation. Eur. J. Soil Sci. 64 (2013), 357–373.
Barnard, R.L., Osborne, C.A., Firestone, M.K., Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J. 7 (2013), 2229–2241.
Barnard, R.L., Osborne, C.A., Firestone, M.K., Changing precipitation pattern alters soil microbial community response to wet-up under a Mediterranean-type climate. ISME J. 9 (2015), 946–957.
Bollmann, A., Schmidt, I., Saunders, A.M., Nicolaisen, M.H., Influence of starvation on potential ammonia-Oxidizing activity and amoA mRNA levels of Nitrosospira briensis. Appl. Environ. Microbiol. 71 (2005), 1276–1282.
Bremner, J.M., Mulvaney, C.S., Nitrogen-total. Methods of Soil Analysis. Part 2 Chemical and Microbiological Properties. 1982, 595–624.
Brenzinger, K., Dörsch, P., Braker, G., pH-driven shifts in overall and transcriptionally active denitrifiers control gaseous product stoichiometry in growth experiments with extracted bacteria from soil. Front. Microbiol., 6, 2015, 961.
Butterbach-Bahl, K., Baggs, E.M., Dannenmann, M., Kiese, R., ZechmeisterBoltenstern, S., Nitrous oxide emissions from soils: how well do we understand the processes and their controls?. Philos. Trans. R. Soc. B Biol. Sci., 368, 2013.
Davidson, E.A., Sources of nitric oxide and nitrous oxide following wetting of dry soil. Soil Sci. Soc. Am. J. 56 (1992), 95–102.
Di, H., Cameron, K., Shen, J., Winefield, C., O'Callaghan, M., Bowatte, S., He, J., Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat. Geosci. 2 (2009), 621–624.
Gower, J.C., Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53 (1966), 325–338.
Groffman, P.M., Tiedje, J.M., Denitrification hysteris during wetting and drying cycles in soil. Soil Sci. Soc. Am. J. 52 (1988), 1626–1629.
Groffman, P.M., Butterbach-Bahl, K., Fulweiler, R.W., Gold, A.J., Morse, J.L., Stander, E.K., Tague, C., Tonitto, C., Vidon, P., Challenges to incorporating spatially and temporally explicit phenomena (hotspots and hot moments) in denitrification models. Biogeochemistry 93 (2009), 49–77.
Hüppi, R., Felber, R., Neftel, A., Six, J., Leifeld, J., Effect of biochar and liming on soil nitrous oxide emissions from a temperate maize cropping system. Soil 1 (2015), 707–717.
Hiel, M.-P., Chélin, M., Parvin, N., Barbieux, S., Degrune, F., Lemtiri, A., Colinet, G., Degré, A., Bodson, B., Garré, S., Crop residue management in arable cropping systems under temperate climate: part 2: Soil physical properties and crop production. A review. BASE, 20, 2016.
Hink, L., Nicol, G.W., Prosser, J.I., Archaea produce lower yields of N2O than bacteria during aerobic ammonia oxidation in soil. Environ. Microbiol., 2016.
Hu, H.W., Chen, D., He, J.Z., Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol. Rev. 39 (2015), 729–749.
IPCC, Climate Change 2007: The Physical Science Basis, Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change., 2007, IPCC.
Jones, C.M., Graf, D.R.H., Bru, D., Philippot, L., Hallin, S., The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J. 7 (2013), 417–426.
Kim, D.G., Vargas, R., Bond-Lamberty, B., Turetsky, M.R., Effects of soil rewetting and thawing on soil gas fluxes: a review of current literature and suggestions for future research. Biogeosciences 9 (2012), 2459–2483.
Löscher, C.R., Kock, A., Könneke, M., LaRoche, J., Bange, H.W., Schmitz, R.A., Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosci. Discuss. 9 (2012), 2419–2429.
Lakanen, E., Erviö, R., A comparison of eight extractants for the determination of plant available micronutrients in soils. Acta. Agr. Fenn., 1971, 223–232.
Lane, D.J., 16S/23S rRNA sequencing in: stackebrandt. Stackebrandt, E., Goodfellow, M., (eds.) Nucleic Acids Techniques in Bacterial Systematics, 1991, John Wiley & Sons, Chichester, 115–147.
Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G.W., Prosser, J.I., Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442 (2006), 806–809.
Li, Z.A., Zou, B., Xia, H.P., Ding, Y.Z., Tan, W.N., Ma, Z.R., Effect of fertilizer and water content on N2O emission from three plantation soils in south China. J. Environ. Sci. 17 (2005), 970–976.
Liu, B.B., Mørkved, P.T., Frostegård, A., Bakken, L.R., Denitrification gene pools, transcription and kinetics of NO: N2O and N2 production as affected by soil pH. FEMS Microbiol. Ecol. 72 (2010), 407–417.
Liu, S., Vereecken, H., Brüggemann, N., A highly sensitive method for the determination of hydroxylamine in soils. Geoderma 232:-234 (2014), 117–122.
McArdle, B.H., Anderson, M.J., Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82 (2001), 290–297.
Molodovskaya, M., Singurindy, O., Richards, B.K., Warland, J., Johnson, M.S., Steenhuis, T.S., Temporal variability of nitrous oxide from fertilized croplands: hot moment analysis. Soil. Sci. Soc. Am. J. 76 (2012), 1728–1740.
Morales, S.E., Cosart, T., Holben, W.E., Bacterial gene abundances as indicators of greenhouse gas emission in soils. ISME J. 4 (2010), 799–808.
Nelson, D.W., Sommers, L.E., Total carbon, organic carbon, and organic matter. Methods Soil Anal. Part 2 Chem. Microbiol. Prop. Agron. Monogr., 1982, 539–579.
Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Stevens, M.H.H., Oksanen, M.J., Suggests, M., The vegan package. Commun. Ecol. Package, 2007, 631–637.
Parkin, T.B., Effect of sampling frequency on estimates of cumulative nitrous oxide emissions. J. Environ. Qual. 37 (2008), 1390–1395.
Placella, S.A., Firestone, M.K., Transcriptional response of nitrifying communities to wetting of dry soil. Appl. Environ. Microbiol. 79 (2013), 3294–3302.
Priemé, A., Christensen, S., Natural perturbations, drying-wetting and freezing-thawing cycles and the emission of nitrous oxide, carbon dioxide and methane from farmed organic soils. Soil Biol. Biochem. 33 (2001), 2083–2091.
Robertson, G.P., Grace, P.R., Greenhouse gas fluxes in tropical agriculture: the need for a full-cost accounting of global warming potentials. Environ. Dev. Sustain. 6 (2004), 51–63.
Rosolem, C.A., Calonego, J.C., Foloni, J.S.S., Leaching of nitrate and ammonium from cover crop straws as affected by rainfall. Commun. Soil. Sci. Plant. Anal. 36 (2005), 819–831.
Rubasinghege, G.R.G., Spak, S.N., Stanier, C.O., Carmichael, G.R., Grassian, V.H., Abiotic mechanism for the formation of atmospheric nitrous oxide from ammonium nitrate. Environ. Sci. Technol. 45 (2011), 2691–2697.
Saleh-Lakha, S., Shannon, K.E., Henderson, S.L., Goyer, C., Trevors, J.T., Zebarth, B.J., Burton, D.L., Effect of pH and temperature on denitrification gene expression and activity in Pseudomonas mandelii. Appl. Environ. Microbiol. 75 (2009), 3903–3911.
Stolk, P.C., Jacobs, C.M.J., Moors, E.J., Hensen, A., Velthof, G.L., Kabat, P., Significant non-linearity in nitrous oxide chamber data and its effect on calculated annual emissions. Biogeosci. Discuss., 2009, 115–141.
Uchida, Y., Wang, Y., Akiyama, H., Nakajima, Y., Hayatsu, M., Expression of denitrification genes in response to a waterlogging event in a Fluvisol and its relationship with large nitrous oxide pulses. FEMS Microbiol. Ecol. 88 (2014), 407–423.
Willems, A., Rosenberg, E., DeLong, E., Lory, S., Stackebrandt, E., Thompson, F., (eds.) The Family Comamonadaceae, 2014, Springer, Berlin Heidelberg, 777–851.
Wrage, N., Velthof, G.L., van Beusichem, M.L., Oenema, O., Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol. Biochem. 33 (2001), 1723–1732.
Xu, W., Liu, G., Liu, W., Effects of precipitation and soil moisture on N2O emissions from upland soils in Guizhou. Chin. J. Appl. Ecol. 13 (2002), 67–70.
Yang, Y., Zhang, J., Cai, Z., Nitrification activities and N mineralization in paddy soils are insensitive to oxygen concentration. Acta. Agric. Scand. Sect. B 66 (2016), 272–281.
Yu, R., Chandran, K., Strategies of Nitrosomonas europaea 19718 to counter low dissolved oxygen and high nitrite concentrations. BMC. Microbiol. 10 (2010), 1–11.
Zhalnina, K., de Quadros, P.D., Camargo, F.A.O., Triplett, E.W., Drivers of archaeal ammonia-oxidizing communities in soil. Front. Microbiol., 3, 2012, 210.
Zhang, Y., Lin, F., Jin, Y., Wang, X., Liu, S., Zou, J., Response of nitric and nitrous oxide fluxes to N fertilizer application in greenhouse vegetable cropping systems in southeast China. Sci. Rep., 6, 2016, 20700.
Zheng, J., Doskey, P.V., Simulated rainfall on agricultural soil reveals enzymatic regulation of short-term nitrous oxide profiles in soil gas and emissions from the surface. Biogeochemistry 128 (2016), 327–338.
Zhu, X., Burger, M., Doane, T.A., Horwath, W.R., Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 6328–6333.