Responses of soil N2O emissions to experimental warming regulated by soil moisture in an alpine steppe

doi:10.17521/cjpe.2017.0164

Abstract

Abstract:

Aims Nitrous oxide (N₂O) is one of the most important greenhouse gases, which contributes a lot to global warming. However, considerable variations are observed in the responses of soil N₂O emissions to experimental warming, and the underlying microbial processes remain unknown.

Methods A warming experiment based on open-top chambers (OTCs) was set up in a typical alpine steppe on the Qinghai-Xizang Plateau. The static chamber combined gas chromatography method was applied to investigate soil N₂O flux under control and warming treatments during the growing seasons in 2014 and 2015. Gene abundances of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) were quantified using quantitative real-time PCR.

Important findings Our results showed that the warming treatments increased soil temperature by 1.7 and 1.6 °C and decreased volumetric water content by 2.5% and 3.3% respectively during the growing season (May to October) in 2014 and 2015. However, there were no significant differences in other soil properties. Our results also revealed that, the magnitude of soil N₂O emissions exhibited substantial variations between the two experimental years, which were 3.23 and 1.47 μg·m ^-2·h ^-1in 2014 and 2015, respectively, but no significant difference in N₂O fluxes was observed between control and warming treatments. AOA and AOB abundances are 15.2 × 10 ⁷and 10.0 × 10 ⁵copies·g ^-1 in 2014, and 5.0 × 10 ⁷and 4.7 × 10 ⁵copies·g ^-1in 2015, with no significant differences between control and warming treatments during the experimental period. Furthermore, warming-induced changes in N₂O emissions had no significant relationship with the changes in soil temperature, but showed a significant positive correlation with the changes in soil moisture at seasonal scale. Overall, these results demonstrate that soil moisture regulates the responses of N₂O emissions to experimental warming, highlighting the necessity to consider the warming-induced drying effect when estimating the magnitude of N₂O emissions under future climate warming.

Key words: climate warming, nitrous oxide, ammonia-oxidizing archaea, ammonia-oxidizing bacteria, Qinghai-?Xizang Plateau

WANG Guan-Qin, LI Fei, PENG Yun-Feng, CHEN Yong-Liang, HAN Tian-Feng, YANG Gui-Biao, LIU Li, ZHOU Guo-Ying, YANG Yuan-He. Responses of soil N₂O emissions to experimental warming regulated by soil moisture in an alpine steppe[J]. Chin J Plan Ecolo, 2018, 42(1): 105-115.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2017.0164

https://www.plant-ecology.com/EN/Y2018/V42/I1/105

Figures/Tables 10

Fig. 1 Photos of the study site and warming experiment. A, Photo of the study site. B, Open-top chamber (OTC) warming facility.

Fig. 2 Warming effects on soil temperature (A) and soil moisture (B) at 0-10 cm depth during 2014-2015 (mean ± SE). *, p < 0.05; **, p < 0.01.

年份 Year	处理 Treatment	氨态氮 NH₄⁺-N (mg·kg^-1)	硝态氮 NO₃^--N (mg·kg^-1)	土壤无机氮 SIN (mg·kg^-1)	微生物生物量碳 MBC (mg·kg^-1)	微生物生物量氮 MBN (mg·kg^-1)
2014	对照 Control	1.8 ± 0.38	25.0 ± 1.6	26.8 ± 1.7	890.4 ± 23.7	91.6 ± 4.0
	增温 Warming	3.0 ± 0.60^*	23.5 ± 1.3	26.5 ± 1.5	801.9 ± 40.8^*	68.2 ± 5.8^**
2015	对照 Control	2.2 ± 0.25	5.96 ± 0.4	8.20 ± 0.5	732.6 ± 11.3	42.2 ± 1.5
	增温 Warming	3.0 ± 0.19^*	4.04 ± 0.4^**	7.02 ± 0.3^*	720.1 ± 18.6	41.3 ± 2.4

Fig. 3 N2O fluxes under control and warming treatments during the growing seasons of 2014(A) and 2015 (B), (mean ± SE). *, p < 0.05. C, control; W, warming.

Table 2 Results of repeated measures ANOVA on the effects of warming (W), measuring date (T), and their interactions (T × W) on soil N2O flux

来源 Source	2014			2015
来源 Source	df	F	p	df	F	p
增温 Warming (W)	1	0.41	0.53	1	0.05	0.83
日期 Date (T)	22	2.16	0.00**	18	2.05	0.00**
T × W	22	0.40	0.99	18	1.32	0.17

Fig. 4 Warming effects on the abundance of AOA-amoA and AOB-amoA during the growing seasons of 2014 (A) and 2015 (B) (mean ± SE). AOA, ammonia-oxidizing archaea; AOB, ammonia-oxidizing bacteria.

Fig. 5 Relationships among warming induced changes (warming-control) in soil N2O fluxes, soil temperature and soil moisture. A, soil moisture and temperature; B, N2O and soil temperature; C, N2O and soil moisture.

Appendix I Daily mean air temperature (lines) and daily precipitation (bars) during 2014-2015 at our experiment site

Appendix II Soil temperature and moisture in control and warming treatments during the growing seasons A, Soil temperature in 2014. B, Soil temperature in 2015. C, Soil moisture in 2014. D, Soil moisture in 2015.

Appendix III Relationships of changes in soil N2O flux with changes in edaphic variables, microbial properties, AOA and AOB A, NH4+-N. B, NO3--N. C, Microbial biomass carbon (MBC). D, Microbial biomass nitrogen (MBN). E, Soil inorganic carbon (SIN). F, Ammonia-oxidizing archaea (AOA). G, Ammonia-oxidizing bacteria (AOB).

References 46

[1]	Bijoor NS, Czimczik CI, Pataki DE, Billings SA ( 2008). Effects of temperature and fertilization on nitrogen cycling and community composition of an urban lawn. Global Change Biology, 14, 2119-2131. DOI URL
[2]	Brookes PC, Landman A, Pruden G, Jenkinson DS ( 1985). Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biology & Biochemistry, 17, 837-842. DOI URL
[3]	Brzostek ER, Blair JM, Dukes JS, Frey SD, Hobbie SE, Melillo JM, Mitchell RJ, Pendall E, Reich PB, Shaver GR ( 2012). The effect of experimental warming and precipitation change on proteolytic enzyme activity: Positive feedbacks to nitrogen availability are not universal. Global Change Biology, 18, 2617-2625. DOI URL
[4]	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? Philosophical Transactions of the Royal Society B: Biological Sciences, 368, 20130122. DOI: 10.1098/rstb.2013.0122. DOI URL
[5]	Cantarel AAM, Bloor JMG, Pommier T, Guillaumaud N, Moirot C, Soussana JF, Poly F ( 2012). Four years of experimental climate change modifies the microbial drivers of N2O fluxes in an upland grassland ecosystem. Global Change Biology, 18, 2520-2531. DOI URL
[6]	Chapin III FS, Matson PA, Vitousek PM ( 2011). Principles of Terrestrial Ecosystem Ecology. Springer, New York.
[7]	Chapin III FS, Shaver GR ( 1985). Individualistic growth response of tundra plant species to environmental manipulations in the field. Ecology, 66, 564-576. DOI URL
[8]	Chapuis-Lardy L, Wrage N, Metay A, Chotte JL, Bernoux M ( 2007). Soils, a sink for N2O? A review. Global Change Biology, 13, 1-17. DOI URL
[9]	Chen H, Zhu Q, Peng CH, Wu N, Wang YF, Fang XQ, Gao YH, Zhu D, Yang G, Tian JQ, Kang XM, Piao SL, Ouyang H, Xiang WH, Luo ZB, Jiang H, Song XZ, Zhang Y, Yu GR, Zhao XQ, Gong P, Yao TD, Wu JH ( 2013 a). The impacts of climate change and human activities on biogeochemical cycles on the Qinghai-Tibetan Plateau. Global Change Biology, 19, 2940-2955. DOI URL PMID
[10]	Chen YL, Xu ZW, Hu HW, Hu YJ, Hao ZP, Jiang Y, Chen BD ( 2013 b). Responses of ammonia-oxidizing bacteria and archaea to nitrogen fertilization and precipitation increment in a typical temperate steppe in Inner Mongolia. Applied Soil Ecology, 68, 36-45. DOI URL
[11]	Daebeler A, Bodelier PLE, Hefting MM, Rütting T, Laanbroek HJ, Jia Z ( 2017). Soil warming and fertilization altered rates of nitrogen transformation processes and selected for adapted ammonia-oxidizing archaea in sub-arctic grassland soil. Soil Biology & Biochemistry, 107, 114-124. DOI URL
[12]	Ding JZ, Li F, Yang GB, Chen LY, Zhang B, Liu L, Fang K, Qin SQ, Chen YL, Peng YF, Ji C, He H, Smith P, Yang YH ( 2016). The permafrost carbon inventory on the Tibetan Plateau: A new evaluation using deep sediment cores. Global Change Biology, 22, 2688-2701. DOI URL PMID
[13]	Flechard CR, Ambus P, Skiba U, Rees RM, Hensen A, van Amstel A, Pol-Van Dasselaar AV, Soussana JF, Jones M, Clifton-Brown J, Raschi A, Horvath L, Neftel A, Jocher M, Ammann C, Leifeld J, Fuhrer J, Calanca P, Thalman E, Pilegaard K, Di Marco C, Campbell C, Nemitz E, Hargreaves KJ, Levy PE, Ball BC, Jones SK, Van De Bulk WCM, Groot T, Blom M, Domingues R, Kasper G, Allard V, Ceschia E, Cellier P, Laville P, Henault C, Bizouard F, Abdalla M, Williams M, Baronti S, Berretti F, Grosz B ( 2007). Effects of climate and management intensity on nitrous oxide emissions in grassland systems across Europe. Agriculture Ecosystems & Environment, 121, 135-152. DOI URL
[14]	Gu JX, Yuan MX, Liu JX, Hao YX, Zhou YT, Qu D, Yang XY ( 2017). Trade-off between soil organic carbon sequestration and nitrous oxide emissions from winter wheat-?summer maize rotations: Implications of a 25-year fertilization experiment in Northwestern China. Science of the Total Environment, 595, 371-379. DOI URL PMID
[15]	Guo LY, Shi F, Yang LY ( 2011). Advances in functional genes and molecular ecology in denitrifiers. Microbiology China, 38, 583-590.
	[ 郭丽芸, 时飞, 杨柳燕 ( 2011). 反硝化菌功能基因及其分子生态学研究进展. 微生物学通报, 38, 583-590.]
[16]	Hu HW, Trivedi P, He JZ, Singh BK ( 2017). Microbial nitrous oxide emissions in dryland ecosystems: Mechanisms, microbiome and mitigation. Environmental Microbiology, 19, 4808-4828. DOI URL PMID
[17]	Hu YG, Chang XF, Lin XW, Wang YF, Wang SP, Duan JC, Zhang ZH, Yang XX, Luo CY, Xu GP, Zhao XQ ( 2010). Effects of warming and grazing on N2O fluxes in an alpine meadow ecosystem on the Tibetan Plateau. Soil Biology & Biochemistry, 42, 944-952. DOI URL
[18]	Huang JX, Xiong DC, Liu XF, Yang ZJ, Xie JS, Yang YS ( 2017). Effects of warming on soil organic carbon mineralization: A review. Acta Ecologica Sinica, 37, 12-24. DOI URL
	[ 黄锦学, 熊德成, 刘小飞, 杨智杰, 谢锦升, 杨玉盛 ( 2017). 增温对土壤有机碳矿化的影响研究综述. 生态学报, 37, 12-24.] DOI URL
[19]	IPCC (Intergovernmental Panel on Climate Change) ( 2013). Climate Change 2013: the Scientific Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK.
[20]	Kaufman M ( 1994). Soil-atmosphere exchange in nitrous oxide, nitric oxide, and methane under secondary succession of pasture to forest in the Atlantic lowlands of Costa Rica. Global Biogeochemical Cycles, 8, 399-410. DOI URL PMID
[21]	Liu LT, Hu CS, Yang PP, Ju ZQ, Olesen JE, Tang JW ( 2016). Experimental warming-driven soil drying reduced N2O emissions from fertilized crop rotations of winter wheat-soybean/fallow, 2009-2014. Agriculture, Ecosystems & Environment, 219, 71-82. DOI URL
[22]	Liu XH, Shao XM, Wang L, Liang E, Qin DH, Ren JW ( 2008). Response and dendroclimatic implications of δ 13C in tree rings to increasing drought on the northeastern Tibetan Plateau. Journal of Geophysical Research: Biogeosciences, 113, 112-118. DOI URL
[23]	Liu ZH, Li DH ( 2015). Ammonia-oxidizing archaea and their contribution to global nitrogen cycling: A review. Microbiology China, 42, 774-782. DOI URL
	[ 刘正辉, 李德豪 ( 2015). 氨氧化古菌及其对氮循环贡献的研究进展. 微生物学通报, 42, 774-782.] DOI URL
[24]	Maestre FT, Delgado-Baquerizo M, Jeffries TC, Eldridge DJ, Ochoa V, Gozalo B, Quero JL, Garcia-Gomez M, Gallardo A, Ulrich W, Bowker MA, Arredondo T, Barraza-Zepeda C, Bran D, Florentino A, Gaitan J, Gutierrez JR, Huber- Sannwald E, Jankju M, Mau RL, Miriti M, Naseri K, Ospina A, Stavi I, Wang DL, Woods NN, Yuan X, Zaady E, Singh BK ( 2015). Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proceedings of the National Academy of Sciences of the United States of America, 112, 15684-15689. DOI URL PMID
[25]	Maljanen M, Yli-Moijala H, Biasi C, Leblans NIW, de Boeck HJ, Bjarnadóttir B, Sigurdsson BD ( 2017). The emissions of nitrous oxide and methane from natural soil temperature gradients in a volcanic area in southwest Iceland. Soil Biology & Biochemistry, 109, 70-80. DOI URL
[26]	Mosier AR, Parton WJ, Martin RE, Valentine DW, Ojima DS, Schimel DS, Burke IC, Adair EC, Del Grosso SJ ( 2008). Soil-atmosphere exchange of trace gases in the Colorado shortgrass steppe. In: Lauenroth WK,? Burke IC eds. Ecology of the Shortgrass Steppe: A Long Term Perspective. Oxford University Press, Oxford.
[27]	Peng YF, Li F, Zhou GY, Fang K, Zhang DY, Li CB, Yang GB, Wang GQ, Wang J, Yang YH ( 2017). Linkages of plant stoichiometry to ecosystem production and carbon fluxes with increasing nitrogen inputs in an alpine steppe. Global Change Biology, 23, 5249-5259. DOI URL PMID
[28]	Ravishankara A, Daniel JS, Portmann RW ( 2009). Nitrous oxide (N2O): The dominant ozone-depleting substance emitted in the 21st Century. Science, 326, 123-125. DOI URL
[29]	Robertson GP ( 1982). Nitrification in forested ecosystems. Philosophical Transactions of the Royal Society B: Biological Sciences, 296, 445-457. DOI URL
[30]	Rotthauwe JH, Witzel KP, Liesack W ( 1997). The ammonia monooxygenase structural gene amoA as a functional marker: Molecular fine-scale analysis of natural ammonia-?oxidizing populations. Applied & Environmental Microbiology, 63, 4704-4712.
[31]	Shi FS, Chen H, Chen HF, Wu Y, Wu N ( 2012). The combined effects of warming and drying suppress CO2 and N2O emission rates in an alpine meadow of the eastern Tibetan Plateau. Ecological Research, 27, 725-733. DOI URL
[32]	Sistla SA, Rastetter EB, Schimel JP ( 2014). Responses of a tundra system to warming using SCAMPS: A stoichiometrically coupled, acclimating microbe-plant-soil model. Ecological Monographs, 84, 151-170. DOI URL
[33]	Stewart KJ, Brummell ME, Farrell RE, Siciliano SD ( 2012). N2O flux from plant-soil systems in polar deserts switch between sources and sinks under different light conditions. Soil Biology & Biochemistry, 48, 69-77. DOI URL
[34]	Szukics U, Abell GC, H?dl V, Mitter B, Sessitsch A, Hackl E, Zechmeister-Boltenstern S ( 2010). Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiology Ecology, 72, 395-406. DOI URL PMID
[35]	Tang XL, Liu SG, Zhou GY, Zhang DQ, Zhou CY ( 2006). Soil-atmospheric exchange of CO2, CH4, and N2O in three subtropical forest ecosystems in southern China. Global Change Biology, 12, 546-560. DOI URL
[36]	Tischer A, Potthast K, Hamer U ( 2014). Land-use and soil depth affect resource and microbial stoichiometry in a tropical mountain rainforest region of southern Ecuador. Oecologia, 175, 375-393. DOI URL PMID
[37]	Vance ED, Brookes PC, Jenkinson DS ( 1987). An extraction method for measuring soil microbial biomass C. Soil Biology & Biochemistry, 19, 703-707. DOI URL
[38]	Voigt C, Lamprecht RE, Marushchak ME, Lind SE, Novakovskiy A, Aurela M, Martikainen PJ, Biasi C ( 2016). Warming of subarctic tundra increases emissions of all three important greenhouse gases—Carbon dioxide, methane, and nitrous oxide. Global Change Biology, 23, 3121-3138. DOI URL PMID
[39]	Wang J, Zhang JB, Müller C, Cai ZC ( 2016). Temperature sensitivity of gross N transformation rates in an alpine meadow on the Qinghai-Tibetan Plateau. Journal of Soils and Sediments, 17, 423-431. DOI URL
[40]	Wang WL, Kong WD, Zeng H ( 2015). A meta-analysis of responses of soil microbes to warming. Journal of Agro-Environment Science, 34, 2169-2175. DOI URL
	[ 王文立, 孔维栋, 曾辉 ( 2015). 土壤微生物对增温响应的Meta分析. 农业环境科学学报, 34, 2169-2175.] DOI URL
[41]	Ward SE, Ostle NJ, Oakley S, Quirk H, Henrys PA, Bardgett RD ( 2013). Warming effects on greenhouse gas fluxes in peatlands are modulated by vegetation composition. Ecology Letters, 16, 1285-1293. DOI URL PMID
[42]	Wu JS, Lin QM, Huang QY, Xiao HA ( 2006). Soil Microbial Biomass——Methods and Application. China Meteorological Press, Beijing.
	[ 吴金水, 林启美, 黄巧云, 肖和艾 ( 2006). 土壤微生物生物量测定方法及其应用. 气象出版社, 北京.]
[43]	Xu BX, Hu YG, Zhang ZS, Chen YL, Peng Z, Li G ( 2014). Effects of experimental warming on CO2, CH4 and N2O fluxes of biological soil crust and soil system in a desert region. Chinese Journal of Plant Ecology, 38, 809-820. DOI URL
	[ 徐冰鑫, 胡宜刚, 张志山, 陈永乐, 张鹏, 李刚 ( 2014). 模拟增温对荒漠生物土壤结皮-土壤系统CO2、CH4和N2O通量的影响. 植物生态学报, 38, 809-820.] DOI URL
[44]	Xu XY, Liu XR, Li Y, Ran Y, Liu YP, Zhang QC, Li Z, He Y, Xu JM, Di HJ ( 2017). Legacy effects of simulated short-term climate change on ammonia oxidisers, denitrifiers, and nitrous oxide emissions in an acid soil. Environmental Science and Pollution Research, 24, 11639-11649. DOI URL PMID
[45]	Yan JH, Zhang W, Wang KY, Qin F, Wang WT, Dai HT, Li PX ( 2014). Responses of CO2, N2O and CH4 fluxes between atmosphere and forest soil to changes in multiple environmental conditions. Global Change Biology, 20, 300-312. DOI URL
[46]	Zhang XZ, Shen ZX, Fu G ( 2015). A meta-analysis of the effects of experimental warming on soil carbon and nitrogen dynamics on the Tibetan Plateau. Applied Soil Ecology, 87, 32-38. DOI URL

Responses of soil N₂O emissions to experimental warming regulated by soil moisture in an alpine steppe

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