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The interactive effect of temperature and fertilizer types determines the dominant microbes in nitrous oxide emissions and the dicyandiamide efficacy in a vegetable soil |
Xiaoya Xu1,2, Haiyang Liu1, Yaowei Liu1, Didier Lesueur3,4,5,6,7, Laetitia Herrmann5,6, Hongjie Di1, Caixian Tang8, Jianming Xu1, Yong Li1( ) |
1. Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China 2. College of Geography and Environment, Shandong Normal University, Jinan 250014, China 3. Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), UMR Eco & Sols, Hanoi, Vietnam 4. Eco & Sols, Université de Montpellier (UMR), CIRAD, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut de Recherche pour le Développement (IRD), Montpellier SupAgro, 34060 Montpellier, France 5. Alliance of Biodiversity International and International Center for Tropical Agriculture (CIAT), Asia hub, Common Microbial Biotechnology Platform (CMBP), Hanoi, Vietnam 6. School of Life and Environmental Sciences, Faculty of Science, Engineering and Built Environment–Deakin University, Melbourne, VIC 3125, Australia 7. Rubber Research Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571737, China 8. La Trobe Institute for Sustainable Agriculture and Food, Department of Animal, Plant & Soil Sciences, La Trobe University, Bundoora, Vic 3086, Australia |
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Abstract ● Dicyandiamide decreased N2O emissions even under 40°C. ● Ammonia oxidizers and nirS were well adapted to 40°C in manured soils. ● Fungal nirK tolerated high temperature better in urea than manure treatment. ● Compared to nosZ II, nosZ I adapted to all temperature regardless of fertilization. ● nirS -denitrifier dominated N2O emissions at high temperature in fertilized soil. Heat waves associated with global warming and extreme climates would arouse serious consequences on nitrogen (N) cycle. However, the responses of the functional guilds to different temperatures, especially high temperature and the cascading effect on N2O emissions remain unclear. An incubation study was conducted to examine the effect of different temperatures (20°C, 30°C, and 40°C) and fertilizer types (urea and manure) on N2O-producers and N2O-reducers, as well as the efficacy of dicyandiamide (DCD) on N2O emissions in a vegetable soil. Results showed that ammonia oxidizers and nirS-type denitrifiers were well adapted to high temperature (40°C) with manure application, while the fungal nirK-denitrifiers had better tolerance with urea application. The nosZ clade I microbes had a strong adaptability to various temperatures regardless of fertilization type, while the growth of nosZ clade II group microbes in non-fertilized soil (control) were significantly inhibited at higher temperature. The N2O emissions were significantly decreased with increasing temperature and DCD application (up to 60%, even at 40°C). Under high temperature conditions, fungal denitrifiers play a significant role in N-limited soils (non-fertilized) while nirS-type denitrifiers was more important in fertilized soils in N2O emissions, which should be specially targeted when mitigating N2O emissions under global warming climate.
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Keywords
nitrogen fertilizer
microorganisms
nitrification inhibitor
bacteria
archaea
fungi
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Corresponding Author(s):
Yong Li
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Issue Date: 13 December 2023
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1 |
S., Avrahami, W., Liesack, R., Conrad, 2003. Effects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers. Environmental Microbiology5, 691–705.
https://doi.org/10.1046/j.1462-2920.2003.00457.x
|
2 |
Z., Chen, W., Ding, Y., Xu, C., Müller, T., Rütting, H., Yu, J., Fan, J., Zhang, T., Zhu, 2015. Importance of heterotrophic nitrification and dissimilatory nitrate reduction to ammonium in a cropland soil: Evidences from a 15N tracing study to literature synthesis. Soil Biology & Biochemistry91, 65–75.
https://doi.org/10.1016/j.soilbio.2015.08.026
|
3 |
T.J., Clough, H.J., Di, K.C., Cameron, R.R., Sherlock, A.K., Metherell, H., Clark, G., Rys, 2007. Accounting for the utilization of a N2O mitigation tool in the IPCC inventory methodology for agricultural soils. Nutrient Cycling in Agroecosystems78, 1–14.
https://doi.org/10.1007/s10705-006-9069-z
|
4 |
P., Cui, F., Fan, C., Yin, A., Song, P., Huang, Y., Tang, P., Zhu, C., Peng, T., Li, S.A., Wakelin, Y., Liang, 2016. Long-term organic and inorganic fertilization alters temperature sensitivity of potential N2O emissions and associated microbes. Soil Biology & Biochemistry93, 131–141.
https://doi.org/10.1016/j.soilbio.2015.11.005
|
5 |
A., Daebeler, C.W., Herbold, J., Vierheilig, C.J., Sedlacek, P., Pjevac, M., Albertsen, R.H., Kirkegaard, J.R., de la Torre, H., Daims, M., Wagner, 2018. Cultivation and genomic analysis of “Candidatus Nitrosocaldus islandicus,” an obligately thermophilic, ammonia-oxidizing Thaumarchaeon from a hot spring biofilm in Graendalur Valley, Iceland. Frontiers in Microbiology9, 193.
https://doi.org/10.3389/fmicb.2018.00193
|
6 |
J.R., de la Torre, C.B., Walker, A.E., Ingalls, M., Konneke, D.A., Stahl, 2008. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environmental Microbiology10, 810–818.
https://doi.org/10.1111/j.1462-2920.2007.01506.x
|
7 |
H.J., Di, K.C., Cameron, 2016. Inhibition of nitrification to mitigate nitrate leaching and nitrous oxide emissions in grazed grassland: a review. Journal of Soils and Sediments16, 1401–1420.
https://doi.org/10.1007/s11368-016-1403-8
|
8 |
H.J., Di, K.C. Cameron, 2007. Nitrate leaching losses and pasture yields as affected by different rates of animal urine nitrogen returns and application of a nitrification inhibitor—a lysimeter study. Nutrient Cycling in Agroecosystems79, 281–290.
|
9 |
H.J., Di, K.C., Cameron, A., Podolyan, A., Robinson, 2014. Effect of soil moisture status and a nitrification inhibitor, dicyandiamide, on ammonia oxidizer and denitrifier growth and nitrous oxide emissions in a grassland soil. Soil Biology & Biochemistry73, 59–68.
https://doi.org/10.1016/j.soilbio.2014.02.011
|
10 |
H.J., Di, K.C., Cameron, J.P., Shen, C.S., Winefield, M., O’Callaghan, S., Bowatte, J.Z., He, 2009. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nature Geoscience2, 621–624.
https://doi.org/10.1038/ngeo613
|
11 |
L.A., Domeignoz-Horta, L., Philippot, C., Peyrard, D., Bru, M.C., Breuil, F., Bizouard, E., Justes, B., Mary, J., Leonard, A., Spor, 2018. Peaks of in situ N2O emissions are influenced by N2O-producing and reducing microbial communities across arable soils. Global Change Biology24, 360–370.
https://doi.org/10.1111/gcb.13853
|
12 |
P., Duan, Y., Song, S., Li, Z., Xiong, 2019a. Responses of N2O production pathways and related functional microbes to temperature across greenhouse vegetable field soils. Geoderma355, 113904.
https://doi.org/10.1016/j.geoderma.2019.113904
|
13 |
P., Duan, Z., Wu, Q., Zhang, C., Fan, Z., Xiong, 2018. Thermodynamic responses of ammonia-oxidizing archaea and bacteria explain N2O production from greenhouse vegetable soils. Soil Biology & Biochemistry120, 37–47.
https://doi.org/10.1016/j.soilbio.2018.01.027
|
14 |
P., Duan, J., Zhou, L., Feng, A.B., Jansen-Willems, Z., Xiong, 2019b. Pathways and controls of N2O production in greenhouse vegetable production soils. Biology and Fertility of Soils55, 285–297.
https://doi.org/10.1007/s00374-019-01348-9
|
15 |
X., Fan, C., Yin, H., Chen, M., Ye, Y., Zhao, T., Li, S.A., Wakelin, Y., Liang, 2019. The efficacy of 3,4-dimethylpyrazole phosphate on N2O emissions is linked to niche differentiation of ammonia oxidizing archaea and bacteria across four arable soils. Soil Biology & Biochemistry130, 82–93.
https://doi.org/10.1016/j.soilbio.2018.11.027
|
16 |
H., Gao, H., Tian, Z., Zhang, X., Xia, 2022. Warming-induced greenhouse gas fluxes from global croplands modified by agricultural practices: A meta-analysis. Science of the Total Environment820, 153288.
https://doi.org/10.1016/j.scitotenv.2022.153288
|
17 |
Y., Guo, A., Naeem, S., Becker‐Fazekas, B., Pitann, K.H., Mühling, 2021. Efficacy of four nitrification inhibitors for the mitigation of nitrous oxide emissions under different soil temperature and moisture. Journal of Plant Nutrition and Soil Science185, 60–68.
https://doi.org/10.1002/jpln.202000367
|
18 |
Y.J., Guo, H.J., Di, K.C., Cameron, B., Li, 2014. Effect of application rate of a nitrification inhibitor, dicyandiamide (DCD), on nitrification rate, and ammonia-oxidizing bacteria and archaea growth in a grazed pasture soil: An incubation study. Journal of Soils and Sediments14, 897–903.
https://doi.org/10.1007/s11368-013-0843-7
|
19 |
G.L., Hutchinson, A.R., Mosier, 1981. Improved soil cover method for field measurement of nitrous oxide fluxes. Soil Science Society of America Journal45, 311–316.
https://doi.org/10.2136/sssaj1981.03615995004500020017x
|
20 |
IPCC, 2007. Climate Change 2007−The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland
|
21 |
IPCC, 2014. Climatie Change 2014−Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland
|
22 |
J.K., Jansson, K.S., Hofmockel, 2020. Soil microbiomes and climate change. Nature Reviews. Microbiology18, 35–46.
https://doi.org/10.1038/s41579-019-0265-7
|
23 |
F.M., Kelliher, C., van Koten, M.J., Kear, M.S., Sprosen, S.F., Ledgard, C.A.M., de Klein, S.A., Letica, J., Luo, G., Rys, 2014. Effect of temperature on dicyandiamide (DCD) longevity in pastoral soils under field conditions. Agriculture, Ecosystems & Environment186, 201–204.
https://doi.org/10.1016/j.agee.2014.01.026
|
24 |
M.M.M., Kuypers, H.K., Marchant, B., Kartal, 2018. The microbial nitrogen-cycling network. Nature Reviews Microbiology16, 263–276.
https://doi.org/10.1038/nrmicro.2018.9
|
25 |
T.V., Lai, R., Farquharson, M.D., Denton, 2019. High soil temperatures alter the rates of nitrification, denitrification and associated N2O emissions. Journal of Soils and Sediments19, 2176–2189.
https://doi.org/10.1007/s11368-018-02238-7
|
26 |
L.E., Lehtovirta-Morley, J., Ross, L., Hink, E.B., Weber, C., Gubry-Rangin, C., Thion, J.I., Prosser, G.W., Nicol, 2016. Isolation of ‘Candidatus Nitrosocosmicus franklandus’, a novel ureolytic soil archaeal ammonia oxidiser with tolerance to high ammonia concentration. FEMS Microbiology Ecology92, fiw057.
https://doi.org/10.1093/femsec/fiw057
|
27 |
L., Li, Z., Zheng, W., Wang, J.A., Biederman, X., Xu, Q., Ran, R., Qian, C., Xu, B., Zhang, F., Wang, S., Zhou, L., Cui, R., Che, Y., Hao, X., Cui, Z., Xu, Y., Wang, 2020. Terrestrial N2O emissions and related functional genes under climate change: A global meta-analysis. Global Change Biology26, 931–943.
https://doi.org/10.1111/gcb.14847
|
28 |
X., Li, Y., Wang, Y., Zhang, M., Lang, P., Christie, S., Bei, J., Zhang, 2021. Dynamics of ammonia oxidizers in response to different fertilization inputs in intensively managed agricultural soils. Applied Soil Ecology157, 103729.
https://doi.org/10.1016/j.apsoil.2020.103729
|
29 |
H.Y., Liu, Y., Ding, Q.C., Zhang, X.M., Liu, J.M., Xu, Y., Li, H.J., Di, 2019. Heterotrophic nitrification and denitrification are the main sources of nitrous oxide in two paddy soils. Plant and Soil445, 39–53.
https://doi.org/10.1007/s11104-018-3860-x
|
30 |
H., Mukhtar, Y.P., Lin, C.M., Lin, Y.R., Lin, 2019. Relative abundance of ammonia oxidizing archaea and bacteria influences soil nitrification responses to temperature. Microorganisms7, 7110526.
https://doi.org/10.3390/microorganisms7110526
|
31 |
Y., Ouyang, J.M., Norton, J.M., Stark, 2017. Ammonium availability and temperature control contributions of ammonia oxidizing bacteria and archaea to nitrification in an agricultural soil. Soil Biology & Biochemistry113, 161–172.
https://doi.org/10.1016/j.soilbio.2017.06.010
|
32 |
J.I., Prosser, L., Hink, C., Gubry-Rangin, G.W., Nicol, 2020. Nitrous oxide production by ammonia oxidizers: Physiological diversity, niche differentiation and potential mitigation strategies. Global Change Biology26, 103–118.
https://doi.org/10.1111/gcb.14877
|
33 |
A.R., Ravishankara, J.S. and Portmann Daniel, , R.W. 2009. Nitrous oxide (N2O): The dominant ozone-depleting substance emitted in the 21st Century. Science 326, 123–125
|
34 |
E.V.L., Roland Hatzenpichler, E., Spieck, K., Stoecker, A., Richter, H., Daims, M., Wagner, 2008. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proceedings of the National Academy of Sciences of the United States of America105, 2134–2139.
|
35 |
M.S., Samad, L.R., Bakken, S., Nadeem, T.J., Clough, C.A., de Klein, K.G., Richards, G.J., Lanigan, S.E., Morales, 2016. High-resolution denitrification kinetics in pasture soils link N2O emissions to pH, and denitrification to C mineralization. PLoS One11, e0151713.
https://doi.org/10.1371/journal.pone.0151713
|
36 |
Z.P., Sha, T.T., Lv, M., Staal, X., Ma, Z., Wen, Q.Q., Li, G., Pasda, T., Misselbrook, X.J., Liu, 2020a. Effect of combining urea fertilizer with P and K fertilizers on the efficacy of urease inhibitors under different storage conditions. Journal of Soils and Sediments20, 2130–2140.
https://doi.org/10.1007/s11368-019-02534-w
|
37 |
Z.P., Sha, X., Ma, J.X., Wang, T.T., Lv, Q.Q., Li, T., Misselbrook, X.J., Liu, 2020b. Effect of N stabilizers on fertilizer-N fate in the soil-crop system: A meta-analysis. Agriculture, Ecosystems & Environment290, 106763.
https://doi.org/10.1016/j.agee.2019.106763
|
38 |
L.Y., Stein, 2019. Insights into the physiology of ammonia-oxidizing microorganisms. Current Opinion in Chemical Biology49, 9–15.
https://doi.org/10.1016/j.cbpa.2018.09.003
|
39 |
L.Y., Stein, 2020. The long-term relationship between microbial metabolism and greenhouse gases. Trends in Microbiology28, 500–511.
https://doi.org/10.1016/j.tim.2020.01.006
|
40 |
A.E., Taylor, A.T., Giguere, C.M., Zoebelein, D.D., Myrold, P.J., Bottomley, 2017. Modeling of soil nitrification responses to temperature reveals thermodynamic differences between ammonia-oxidizing activity of archaea and bacteria. ISME Journal11, 896–908.
https://doi.org/10.1038/ismej.2016.179
|
41 |
R.L., Thompson, L., Lassaletta, P.K., Patra, C., Wilson, K.C., Wells, A., Gressent, E.N., Koffi, M.P., Chipperfield, W., Winiwarter, E.A., Davidson, H., Tian, J.G., Canadell, 2019. Acceleration of global N2O emissions seen from two decades of atmospheric inversion. Nature Climate Change9, 993–998.
https://doi.org/10.1038/s41558-019-0613-7
|
42 |
C., Voigt, M.E., Marushchak, B.W., Abbott, C., Biasi, B., Elberling, S.D., Siciliano, O., Sonnentag, K.J., Stewart, Y., Yang, P.J., Martikainen, 2020. Nitrous oxide emissions from permafrost-affected soils. Nature Reviews Earth & Environment1, 420–434.
https://doi.org/10.1038/s43017-020-0063-9
|
43 |
Z., Wang, K., Li, X., Shen, F., Yan, X., Zhao, Y., Xin, L., Ji, Q., Xiang, X., Xu, D., Li, J., Ran, X., Xu, Q., Chen, 2023. Soil nitrogen substances and denitrifying communities regulate the anaerobic oxidation of methane in wetlands of Yellow River Delta, China. Science of the Total Environment857, 159439.
https://doi.org/10.1016/j.scitotenv.2022.159439
|
44 |
D., Wu, M., Senbayram, R., Well, N., Brüggemann, B., Pfeiffer, N., Loick, B., Stempfhuber, K., Dittert, R., Bol, 2017. Nitrification inhibitors mitigate N2O emissions more effectively under straw-induced conditions favoring denitrification. Soil Biology & Biochemistry104, 197–207.
https://doi.org/10.1016/j.soilbio.2016.10.022
|
45 |
X.Y., Xing, Y.F., Tang, H.F., Xu, H.L., Qin, Y., Liu, W.Z., Zhang, A.L., Chen, B.L., Zhu, 2021. Warming shapes nirS-and nosZ-type denitrifier communities and stimulates N2O emission in acidic paddy soil. Applied and Environmental Microbiology87, e02965.
https://doi.org/10.1128/AEM.02965-20
|
46 |
X., Xu, X., Liu, Y., Li, Y., Ran, Y., Liu, Q., Zhang, Z., Li, Y., He, J., Xu, H., Di, 2017. High temperatures inhibited the growth of soil bacteria and archaea but not that of fungi and altered nitrous oxide production mechanisms from different nitrogen sources in an acidic soil. Soil Biology & Biochemistry107, 168–179.
https://doi.org/10.1016/j.soilbio.2017.01.003
|
47 |
X., Xu, Y., Liu, B.P., Singh, Q., Yang, Q., Zhang, H., Wang, Z., Xia, H., Di, B.K., Singh, J., Xu, Y., Li, 2020. NosZ clade II rather than clade I determine in situ N2O emissions with different fertilizer types under simulated climate change and its legacy. Soil Biology & Biochemistry150, 107974.
https://doi.org/10.1016/j.soilbio.2020.107974
|
48 |
X., Xu, Z., Xia, Y., Liu, E., Liu, K., Müller, H., Wang, J., Luo, X., Wu, J., Beiyuan, Z., Fang, J., Xu, H., Di, Y., Li, 2021. Interactions between methanotrophs and ammonia oxidizers modulate the response of in situ methane emissions to simulated climate change and its legacy in an acidic soil. Science of the Total Environment752, 142225.
https://doi.org/10.1016/j.scitotenv.2020.142225
|
49 |
C., Yin, F., Fan, A., Song, X., Fan, H., Ding, W., Ran, H., Qiu, Y., Liang, 2017. The response patterns of community traits of N2O emission-related functional guilds to temperature across different arable soils under inorganic fertilization. Soil Biology & Biochemistry108, 65–77.
https://doi.org/10.1016/j.soilbio.2017.01.022
|
50 |
Y., Yin, Z., Wang, X., Tian, Y., Wang, J., Cong, Z., Cui, 2022. Evaluation of variation in background nitrous oxide emissions: A new global synthesis integrating the impacts of climate, soil, and management conditions. Global Change Biology28, 480–492.
https://doi.org/10.1111/gcb.15860
|
51 |
J., Zhang, H., Tian, H., Shi, J., Zhang, X., Wang, S., Pan, J., Yang, 2020. Increased greenhouse gas emissions intensity of major croplands in China: Implications for food security and climate change mitigation. Global Change Biology26, 6116–6133.
https://doi.org/10.1111/gcb.15290
|
52 |
J., Zhao, M.O., Bello, Y., Meng, J.I., Prosser, C., Gubry-Rangin, 2020. Selective inhibition of ammonia oxidising archaea by simvastatin stimulates growth of ammonia oxidising bacteria. Soil Biology & Biochemistry141, 107673.
https://doi.org/10.1016/j.soilbio.2019.107673
|
53 |
M., Zhou, B., Zhu, S., Wang, X., Zhu, H., Vereecken, N., Bruggemann, 2017. Stimulation of N2O emission by manure application to agricultural soils may largely offset carbon benefits: a global meta-analysis. Global Change Biology23, 4068–4083.
https://doi.org/10.1111/gcb.13648
|
54 |
X., Zhou, D., Fornara, E.A., Wasson, D., Wang, G., Ren, P., Christie, Z., Jia, 2015. Effects of 44 years of chronic nitrogen fertilization on the soil nitrifying community of permanent grassland. Soil Biology & Biochemistry91, 76–83.
https://doi.org/10.1016/j.soilbio.2015.08.031
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