Responses of denitrifying functional gene abundance to long-term fertilization regimes in an upland Ultisol

doi:10.13287/j.1001-9332.202011.024

Abstract

Abstract: Fertilization affects soil nitrogen cycling and nitrous oxide (N₂O) emissions, which are mainly driven by microbes. A 32-year field experiment was conducted to investigate the effects of chemical fertilizers and their combination with organic materials on the abundance of denitrifying functional genes (nirS, nirK, nosZ I and nosZ II) in Ultisol. The treatments comprised no fertilizer (CK), chemical fertilizer, chemical fertilizer+peanut straw, chemical fertilizer+rice straw, chemical fertilizer+radish and chemical fertilizer+pig manure. Compared with the single chemical fertilizer treatment, soil pH and organic carbon content increased in the chemical fertilizer plus organic material treatments, with chemical fertilizer+pig manure having the strongest effect. Long-term fertilization did not affect the abundance of nirK gene, but significantly altered the nirS gene abundance. Compared to CK, long-term chemical fertilizer application increased the abundance of nirS gene by 426%. However, partial replacement of chemical fertilizer by organic materials decreased the abundance of nirS gene. The abundance of nosZ I gene was one order of magnitude higher than that of nosZ II, indicating the domination of nosZ I in the acidic Ultisol. Long-term fertilization did not affect the abundance of nosZ II, whereas chemical fertilizer+pig manure increased the abundance of nosZ I by 138%. Results of stepwise regression analysis showed that available phosphorus content was the primary factor regulating the abundance of nosZ I gene, whereas the abundance of the nosZ II gene was mainly regulated by nitrate content. Moreover, the lowest (nirS+nirK)/(nosZ I+nosZ II) value in the chemical fertilizer+pig manure treatment indicated that long-term manure application might reduce N₂O emission potential in Ultisols.

Key words: Ultisols, long-term fertilization, denitrifiers, nosZ I, nosZ II

WAN Song, DUAN Chun-jian, FAN Jian-bo, YE Gui-ping, WANG Quan-cheng, HE Ji-zheng, LIN Yong-xin. Responses of denitrifying functional gene abundance to long-term fertilization regimes in an upland Ultisol[J]. Chinese Journal of Applied Ecology, 2020, 31(11): 3729-3736.

References

[1] Ravishankara AR, Daniel JS, Portmann RW. Nitrous oxide (N₂O): The dominant ozone-depleting substance emitted in the 21st century. Science, 2009, 326: 123-125
[2] Kool DM, Dolfing J, Wrage N, et al. Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biology and Biochemistry, 2011, 43: 174-178
[3] Kuypers MM, Marchant HK, Kartal B. The microbial nitrogen-cycling network. Nature Reviews Microbiology, 2018, 16: 263-276
[4] Hallin S, Philippot L, Loffler FE, et al. Genomics and ecology of novel N₂O-reducing microorganisms. Trends in Microbiology, 2018, 26: 43-55
[5] Jones CM, Graf DR, Bru D, et al. The unaccounted yet abundant nitrous oxide-reducing microbial community: A potential nitrous oxide sink. The ISME Journal, 2013, 7: 417-426
[6] Jones CM, Spor A, Brennan FP, et al. Recently identified microbial guild mediates soil N₂O sink capacity. Nature Climate Change, 2014, 4: 801-805
[7] Assémien FL, Cantarel AA, Florio A, et al. Different groups of nitrite-reducers and N₂O-reducers have distinct ecological niches and functional roles in West African cultivated soils. Soil Biology and Biochemistry, 2019, 129: 39-47
[8] Domeignoz-Horta LA, Spor A, Bru D, et al. The diversity of the N₂O reducers matters for the N₂O:N₂ denitrification end-product ratio across an annual and a perennial cropping system. Frontiers in Microbiology, 2015, 6: 971
[9] St.Clair SB, Lynch JP. The opening of Pandora's Box: Climate change impacts on soil fertility and crop nutrition in developing countries. Plant and Soil, 2010, 335: 101-115
[10] 洪曦, 高菊生, 罗尊长, 等. 不同施肥措施对红壤稻田氮磷平衡及生态经济效益的影响. 应用生态学报, 2018, 29(1): 158-166 [Hong X, Gao J-S, Luo Z-Z, et al. Effects of different fertilization regimes on nitrogen and phosphorus balance and eco-economic benefits in red paddy field. Chinese Journal of Applied Ecology, 2018, 29(1): 158-166]
[11] Huang S, Zhang WJ, Yu XC, et al. Effects of long-term fertilization on corn productivity and its sustainability in an Ultisol of southern China. Agriculture, Ecosystems and Environment, 2010, 138: 44-50
[12] 鲁如坤. 土壤农业化学分析方法. 北京: 中国农业科技出版社, 2000 [Lu R-K. Soil and Agricultural Che-mistry Analysis. Beijing: China Agricultural Science and Technology Press, 2000]
[13] Throback IN, Enwall K, Jarvis A, et al. Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiology Ecology, 2004, 49: 401-417
[14] Henry S, Bru D, Stres B, et al. Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Applied and Environmental Microbiology, 2006, 72: 5181-5189
[15] Hooper DU, Adair EC, Cardinale BJ, et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature, 2012, 486: 105-108
[16] 龚雪蛟, 秦琳, 刘飞, 等. 有机类肥料对土壤养分含量的影响. 应用生态学报, 2020, 31(4): 1403-1416 [Gong X-J, Qin L, Liu F, et al. Effects of organic manure on soil nutrient content: A review. Chinese Journal of Applied Ecology, 2020, 31(4): 1403-1416]
[17] Ye GP, Lin YX, Liu DY, et al. Long-term application of manure over plant residues mitigates acidification, builds soil organic carbon and shifts prokaryotic diversity in acidic Ultisols. Applied Soil Ecology, 2019, 133: 24-33
[18] Yan X, Wei ZQ, Wang DJ, et al. Phosphorus status and its sorption-associated soil properties in a paddy soil as affected by organic amendments. Journal of Soils and Sediments, 2015, 15: 1882-1888
[19] Materechera SA, Mkhabela TS. The effectiveness of lime, chicken manure and leaf litter ash in ameliorating acidity in a soil previously under black wattle (Acacia mearnsii) plantation. Bioresource Technology, 2002, 85: 9-16
[20] 孙凤霞, 张伟华, 徐明岗, 等. 长期施肥对红壤微生物生物量碳氮和微生物碳源利用的影响. 应用生态学报, 2010, 21(11): 2792-2798 [Sun F-X, Zhang W-H, Xu M-G, et al. Effects of long-term fertilization on microbial biomass carbon and nitrogen and on carbon source utilization of microbes in a red soil. Chinese Journal of Applied Ecology, 2010, 21(11): 2792-2798]
[21] Hyvonen R, Persson T, Andersson S, et al. Impact of long-term nitrogen addition on carbon stocks in trees and soils in northern Europe. Biogeochemistry, 2008, 89: 121-137
[22] Hallin S, Jones CM, Schloter M, et al. Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. The ISME Journal, 2009, 3: 597-605
[23] Maul JE, Cavigelli MA, Vinyard B, et al. Cropping system history and crop rotation phase drive the abundance of soil denitrification genes nirK, nirS and nosZ in conventional and organic grain agroecosystems. Agriculture, Ecosystems and Environment, 2019, 273: 95-106
[24] Luo XS, Qian H, Wang L, et al. Fertilizer types shaped the microbial guilds driving the dissimilatory nitrate reduction to ammonia process in a Ferralic Cambisol. Soil Biology and Biochemistry, 2020, 141: 107677
[25] Yin C, Fan FL, Song A, et al. Different denitrification potential of aquic brown soil in Northeast China under inorganic and organic fertilization accompanied by distinct changes of nirS- and nirK-denitrifying bacterial community. European Journal of Soil Biology, 2014, 65: 47-56
[26] Liu BB, Morkved PT, Frostegard A, et al. Denitrification gene pools, transcription and kinetics of NO, N₂O and N₂ production as affected by soil pH. FEMS Microbio-logy Ecology, 2010, 72: 407-417
[27] Sanford RA, Wagner DD, Wu QZ, et al. Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109: 19709-19714
[28] Samad MS, Biswas A, Bakken LR, et al. Phylogenetic and functional potential links pH and N₂O emissions in pasture soils. Scientific Reports, 2016, 6: 35990
[29] Wei XM, Hu YJ, Peng PQ, et al. Effect of P stoichio-metry on the abundance of nitrogen-cycle genes in phosphorus-limited paddy soil. Biology and Fertility of Soils, 2017, 53: 767-776
[30] Levy-Booth DJ, Prescott CE, Grayston SJ. Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biology and Biochemistry, 2014, 75: 11-25
[31] 刘德鸿, 文帅龙, 龚琬晴, 等. 太湖沉积物反硝化功能基因丰度及其与N₂O通量的关系. 生态环境学报, 2019, 28(1): 136-142 [Liu D-H, Wen S-L, Gong W-Q, et al. The denitrifying functional gene abundance and its relation with sediment N₂O flux in Taihu Lake. Ecology and Environmental Sciences, 2019, 28(1): 136-142]
[32] 李双双, 陈晨, 段鹏鹏, 等. 生物质炭对酸性菜地土壤N₂O排放及相关功能基因丰度的影响. 植物营养与肥料学报, 2018, 24(2): 414-423 [Li S-S, Chen C, Duan P-P, et al. Effects of biochar application on N₂O emissions and abundance of nitrogen related functional genes in an acidic vegetable soil. Journal of Plant Nutrition and Fertilizers, 2018, 24(2): 414-423]
[33] 李梦雅, 徐明岗, 王伯仁, 等. 长期不同施肥下我国旱地红壤N₂O释放特征及其对土壤性质的响应. 农业环境科学学报, 2009, 28(12): 2645-2650 [Li M-Y, Xu M-G, Wang B-R, et al. Effect of long-term fertilizations on N₂O emission and its relationship with soil properties in red soil of Southern China. Journal of Agro-Environment Science, 2009, 28(12): 2645-2650]