农田土壤硝化反硝化作用及其对生物炭添加响应的研究进展

doi:10.3969/j.issn.1000-6362.2018.07.002

摘要/Abstract

摘要： 氧化亚氮（N2O）是重要的温室气体之一，还会破坏大气臭氧层，影响全球气候变化。农田土壤是N2O最主要的排放源，由微生物主导的硝化和反硝化作用是其最主要的排放途径，因此，土壤的硝化和反硝化作用备受关注。在综合国内外相关研究的基础上，就区分硝化和反硝化作用对N2O排放贡献的研究方法、土壤N2O产生途径及其影响因素以及施用生物炭对N2O排放的影响机理进行归纳总结。结果表明：硝化和反硝化作用对生物炭的响应不同，在N2O减排效应上也存在很大的不确定性，其内在机理尚不明确。在此基础上，提出区分硝化和反硝化作用对N2O排放贡献的最佳研究方法，并就农田土壤硝化反硝化作用的影响因素以及对生物炭的响应机制进行研究展望。

关键词: 氧化亚氮, 硝化抑制剂, 土壤微生物, 功能基因

Abstract: Nitrous oxide (N2O) is one of the most important greenhouse gases, and agriculture soils are the main emission sources. Nitrification and denitrification, which are dominated by microbes, are the most important emission pathways. Therefore, the soil nitrification and denitrification have been paid much attention by scientists. Based on a large quantity of literatures, this paper summarizes the methods of distinguishing the contribution of nitrification and denitrification to N2O emission, soil N2O production pathway and its influencing factors, and mechanism of the effects of biochar on N2O emission. The results showed that the response of nitrification and denitrification to biochar was different, and there was still a lot of uncertainty in the effect of biochar on N2O emission reduction. The underlying mechanism was not yet clear. As such, this paper proposed the best research method to distinguish the contribution of nitrification and denitrification to N2O emission. Finally, the research prospect of the influencing factors of nitrification and denitrification and the response mechanism of biochar in farmland soil were also proposed.

Key words: Nitrous oxide, Nitrification inhibitor, Soil microbe, Functional gene

赵光昕，张晴雯，刘杏认，田秀平. 农田土壤硝化反硝化作用及其对生物炭添加响应的研究进展[J]. 中国农业气象, 2018, 39(07): 442-452.

ZHAO Guang-xin, ZHANG Qing-wen, LIU Xing-ren, TIAN Xiu-ping. Nitrification and Denitrification and its Response to Biochar Addition in Agricultural Soil：A Review[J]. Chinese Journal of Agrometeorology, 2018, 39(07): 442-452.

参考文献

[1] IPCC.Climate change 2013:the physical science basis[R]. Cambridge,USA:Cambridge University Press,2013. [2] Hu M,Chen D,Dahlgren R A.Modeling nitrous oxide emission from rivers:a global assessment[J].Global Change Biology, 2016,22(11):3566-3582. [3] Meng Q,Yue S,Peng H,et al.Improving yield and nitrogen use efficiency simultaneously for maize and wheat in China:a review[J].Pedosphere,2016,26(2):137-147. [4] Case S D C,Mcnamara N P,Reay D S,et al.Biochar suppresses N2O emissions while maintaining N availability in a sandy loam soil[J].Soil Biology and Biochemistry,2015,81:178-185. [5] Lehmann J D,Joseph S.Biochar for environmental management[J]. Science and Technology,Earthscan,2015,25(1):15801-15811. [6] Clough T J,Condron L M,Kammann C,et al.A review of biochar and soil nitrogen dynamics[J].Agronomy,2013,3(2): 275-293. [7] 孟梦,吕成文,李玉娥,等.添加生物炭对华南早稻田CH4和N2O排放的影响[J].中国农业气象,2013,34(4):396-402. Meng M,Lv C W,Li Y E,et al.Effect of biochar on CH4 and N2O emissions from early rice field in South China[J]. Chinese Journal of Agrometeorology,2013,34(4):396-402.(in Chinese) [8] 张星,张晴雯,刘杏认,等.施用生物炭对农田土壤氮素转化关键过程的影响[J].中国农业气象,2015,36(6):709-716. Zhang X,Zhang Q W,Liu X R,et al.Effects of biochar on the key soil nitrogen transformation processes in agricultural soil[J]. Chinese Journal of Agrometeorology,2015,36(6):709-716. (in Chinese) [9] 韩雪,范靖尉,白晋华,等.减氮和施生物炭对华北夏玉米-冬小麦田土壤CO2和N2O排放的影响[J].中国农业气象,2016, 17(2):2800-2808. Han X,Fan J W,Bai J H,et al.Effects of reducing nitrogen and biochar application on CO2 and N2O emissions from summer maize-winter wheat field in North China[J].Chinese Journal of Agrometeorology,2016,17(2):2800-2808.(in Chinese) [10] Cayuela M L,Jeffery S,Zwieten L V.The molar H:corg ratio of biochar is a key factor in mitigating N2O emissions from soil[J].Agriculture,Ecosystems and Environment,2015,202 (135-138):135-138. [11] Yi Q,Tang S,Fan X,et al.Effects of nitrogen application rate,nitrogen synergist and biochar on nitrous oxide emissions from vegetable field in south China[J].PloS ONE,2017,12(4):e0175325. [12] Cayuela M L,Zwieten L V,Singh B P,et al.Biochar's role in mitigating soil nitrous oxide emissions:a review and meta- analysis[J].Agriculture,Ecosystems and Environment,2014, 191: 5-16. [13] Chen C R,Phillips I R,Goloran L M,et al.Impacts of greenwaste biochar on ammonia volatilisation from bauxite processing residue sand[J].Plant and Soil,2013,367(1-2): 301-312. [14] Dai H N,Scheer C,Rowlings D W,et al.Rice husk biochar and crop residue amendment in subtropical cropping soils:effect on biomass production, nitrogen use efficiency and greenhouse gas emissions[J].Biology and Fertility of Soils,2016,52(2):261-270. [15] 黄树辉,吕军.区分土壤中硝化与反硝化对N2O产生贡献的方法[J].农业工程学报,2005,21(s1):48-51. Huang S H,Lv J.Methods for the contributions of nitrification and denitrification to the production of nitrous oxide from soil[J].Transactions of the CSAE,2005,21(s1):48-51.(in Chinese) [16] Webster F A,Hopkins D W.Contributions from different microbial processes to N2O emission from soil under different moisture regimes[J].Biology and Fertility of Soils,1996, 22(4): 331-335. [17] Wrage N,Velthof G L,Oenema O,et al.Acetylene and oxygen as inhibitors of nitrous oxide production in Nitrosomonas europaea and Nitrosospira briensis:a cautionary tale[J]. Fems Microbiology Ecology,2004,47(1):13-18. [18] 阎宏亮,张璇,谢立勇,等.菜地土壤施用铵态氮肥后N2O排放来源及其动态[J].中国农业气象,2014,35(2):141-148. Yan H L,Zhang X,Xie L Y,et al.Study on the pathway and dynamics of N2O emissions from the vegetable soil fertilized with ammonium nitrogen[J].Chinese Journal of Agrometeorology,2014,35(2):141-148.(in Chinese) [19] Ryden J C,Dawson K P.Evaluation of the acetylene-inhibition technique for the measurement of denitrification in grassland soils[J].Journal of the Science of Food & Agriculture,2010, 33(12):1197-1206.(in Chinese) [20] Felber R,Conen F,Flechard C R,et al.Theoretical and practical limitations of the acetylene inhibition technique to determine total denitrification losses[J].Biogeosciences,2012, 9(10):4125-4138. [21] Kool D M,Wrage N,Zechmeisterboltenstern S,et al.Nitrifier denitrification can be a source of N2O from soil: a revised approach to the dual-isotope labelling method[J].European Journal of Soil Science,2010,61(5):759-772. [22] Pedersen H,Dunkin K A,Firestone M K.The relative importance of autotrophic and heterotrophic nitrification in a conifer forest soil as measured by 15N tracer and pool dilution techniques[J].Biogeochemistry,1999,44(2):135-150. [23] Li W,Sun Y,Li G,et al.Contributions of nitrification and denitrification to N2O emissions from aged refuse bioreactor at different feeding loads of ammonia substrates[J].Waste Management,2017,68:319-328. [24] Zhang Z,Wang J J,Lu X.Fingerprint natural soil N2O emission from nitration and denitrification by dual isotopes (15N and 18O) and site preferences[J].Acta Ecologica Sinica, 2016,36(5):356-360. [25] 付素静.干旱荒漠区典型土壤硝酸盐分布特征及硝化反硝化作用研究[D].兰州:兰州大学,2012. Fu S J.Nitrate distribution and nitrification-denitrification in the soils of desert areas,Northwest China[D].Lanzhou: Lanzhou University,2012.(in Chinese) [26] Frame C H,Casciotti K L.Biogeochemical controls and isotopic signatures of nitrous oxide production by a marine ammonia-oxidizing bacterium[J].Biogeosciences,2010,7(2): 2695-2709. [27] 朱永官,王晓辉,杨小茹,等.农田土壤N2O产生的关键微生物过程及减排措施[J].环境科学,2014,35(2):792-800. Zhu Y G,Wang X H,Yang X R,et al.Key microbial processes in nitrous oxide emissions of agricultural soil and mitigation strategies[J].Environmental Science,2014,35(2):792-800.(in Chinese) [28] Wrage N,van Groenigen J W,Oenema O,et al.A novel dual-isotope labelling method for distinguishing between soil sources of N2O[J].Rapid Communications in Mass Spectrometry Rcm,2005,19(22):3298-3306. [29] Caranto J D,Vilbert A C,Lancaster K M.Nitrosomonas europaea cytochrome P460 is a direct link between nitrification and nitrous oxide emission[J].Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(51):14704-14709. [30] Daims H,Lebedeva E V,Pjevac P,et al.Complete nitrification by nitrospira bacteria[J].Nature,2015,528:504-509. [31] Laughlin R J,Ru?Tting T,Mu?Ller C,et al.Effect of acetate on soil respiration,N2O emissions and gross N transformations related to fungi and bacteria in a grassland soil[J].Applied Soil Ecology,2009,42(1):25-30. [32] Shen J P,Zhang L M,Zhu Y G,et al.Abundance and composition of ammonia-oxidizing bacteria and ammonia- oxidizing archaea communities of an alkaline sandy loam[J].Environmental Microbiology,2008,10(6):1601-1611. [33] Mertens J,Broos K,Wakelin S A,et al.Bacteria,not archaea, restore nitrification in a zinc-contaminated soil[J].The ISME Journal,2009,3(8):916-923. [34] Di H J,Cameron K C,Shen J P,et al.Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils[J].Nature Geoscience,2009,2(9):621-624. [35] Papen H, Berg R V.A Most Probable Number method (MPN) for the estimation of cell numbers of heterotrophic nitrifying bacteria in soil[J].Plant and Soil,1998,199(1):123-130. [36] Richardson D J,Wehrfritz J M,Keech A,et al.The diversity of redox proteins involved in bacterial heterotrophic nitrification and aerobic denitrification[J].Biochemical Society Transactions, 1998,26(3):401-8. [37] Marusenko Y,Huber D P,Hall S J.Fungi mediate nitrous oxide production but not ammonia oxidation in arid land soils of the southwestern US[J].Soil Biology and Biochemistry, 2013,63(4):24-36. [38] 章伟,高人,陈仕东,等.米槠天然林土壤真菌对N2O产生的贡献[J].亚热带资源与环境学报,2013,8(2):28-34. Zhang W,Gao R,Chen S D,et al.Fungal contribution to N2O production in soil for a natural Castanopsis carlesii forest in Wuyi nature reserve,Southeastern[J].China Journal of Subtropical Resources and Environment,2013,8(2):28-34.(in Chinese) [39] 黄莹,龙锡恩.真菌对土壤N2O释放的贡献及其研究方法[J].应用生态学报,2014,25(4):1213-1220. Huang Y,Long X E.Contribution of fungi to soil nitrous oxide emission and their research methods:a review[J].Chinese Journal of Applied Ecology,2014,25(4):1213-1220.(in Chinese) [40] Zhang Q,Li F,Tang C.Quantifying of soil denitrification potential in a wetland ecosystem,ochi experiment site,Japan[J]. Journal of Resources and Ecology,2012,3(1):93-96. [41] Shoun H.Denitrification and anaerobic energy producing mechanisms by fungi[J].Tanpakushitsu Kakusan Koso Protein Nucleic Acid Enzyme,2006,51(5):419-29. [42] Zhe C,Luo X,Hu R,et al.Impact of long-term fertilization on the composition of denitrifier communities based on nitrite reductase analyses in a paddy soil[J].Microbial Ecology, 2010, 60(4):850-861. [43] Liu J, Hou H, Sheng R, et al. Denitrifying communities differentially respond to flooding drying cycles in paddy soils[J].Applied Soil Ecology,2012,62(62):155-162. [44] Bakken L R,?sa Frosteg?rd.Regulation of denitrification at the cellular level:a clue to the understanding of N2O emissions from soils[J].Philosophical Transactions of the Royal Society B Biological Sciences,2012,367(1593):1226-34. [45] Shaw L J,Nicol G W,Smith Z,et al.Nitrosospira spp.can produce nitrous oxide via a nitrifier denitrification pathway [J].Environmental Microbiology, 2006, 8(2):214-222. [46] Kandeler E,Deiglmayr K,Tscherko D,et al.Abundance of narG,nirS,nirK,and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland[J].Applied and Environmental Microbiology,2006,72(9):5957-5962. [47] Baggs E M.A review of stable isotope techniques for N2O source partitioning in soils:recent progress, remaining challenges and future considerations[J].Rapid Communications in Mass Spectrometry,2010,22(11):1664-1672. [48] Yin S X,Chen D,Chen L M,et al.Dissimilatory nitrate reduction to ammonium and responsible microorganisms in two Chinese and Australian paddy soils[J].Soil Biology and Biochemistry,2002, 34(8):1131-1137. [49] Schmidt C S,Richardson D J,Baggs E M.Constraining the conditions conducive to dissimilatory nitrate reduction to ammonium in temperate arable soils[J].Soil Biology and Biochemistry,2011,43(7):1607-1611. [50] Rütting T,Boeckx P,Müller C,et al.Assessment of the importance of dissimilatory nitrate reduction to ammonium for the terrestrial nitrogen cycle[J].Biogeosciences,2011, 8(7):1779-1791. [51] Baggs E M.Soil microbial sources of nitrous oxide:recent advances in knowledge, emerging challenges and future direction[J].Current Opinion in Environmental Sustainability, 2011,3(5):321-327. [52] Wu Y P,Ma B,Zhou L,et al.Changes in the soil microbial community structure with latitude in eastern China,based on phospholipid fatty acid analysis[J].Applied Soil Ecology,2009, 43(2):234-240. [53] Spott O,Russow R,Stange C F.Formation of hybrid N2O and hybrid N2 due to codenitrification:first review of a barely considered process of microbially mediated N-nitrosation[J]. Soil Biology and Biochemistry,2011,43(10):1995-2011. [54] Herold M B,Baggs E M,Daniell T J.Fungal and bacterial denitrification are differently affected by long-term pH amendment and cultivation of arable soil[J].Soil Biology and Biochemistry,2012,54(6):25-35. [55] Masulili A,Utomo W H,Syechfani M S.Rice husk biochar for rice based cropping system in acid soil I:the characteristics of rice husk biochar and its influence on the properties of acid sulfate soils and rice growth in west Kalimantan,Indonesia [J]. Journal of Agricultural Science, 2010,2(1):39-47. [56] 张星,刘杏认,林国林,等.生物炭和秸秆对华北农田表层土壤矿质氮和pH值的影响[J].中国农业气象,2016,37(2): 131-142. Zhang X,Liu X R,Lin G L,et al.Effects of biochar and straw return on mineral nitrogen and pH of the surface soil in farmland of the North China Plain[J].Chinese Journal of Agrometeorology,2016,37(2):131-142.(in Chinese) [57] Ball P N,Mackenzie M D,Deluca T H,et al.Wildfire and charcoal enhance nitrification and ammonium-oxidizing bacterial abundance in dry montane forest soils[J].Journal of Environmental Quality,2010,39(4):1243-1253. [58] Taketani R G,Tsai S M.The influence of different land uses on the structure of archaeal communities in Amazonian anthrosols based on 16S rRNA and amoA genes[J]. Microbial Ecology,2010,59(4):734-743. [59] Steinbeiss S,Gleixner G,Antonietti M.Effect of biochar amendment on soil carbon balance and soil microbial active- ity [J]. Soil Biology and Biochemistry,2009,41(6):1301-1310. [60] Deluca T H,MacKenzie M D,Gundale M J,et al.Biochar effects on soil nutrient transformations[A].Biochar for environmental management: science and technology[C].London,UK: Earthscan, 2009: 251-270. [61] He L,Zhao X,Wang S,et al.The effects of rice-straw biochar addition on nitrification activity and nitrous oxide emissions in two oxisols[J].Soil and Tillage Research,2016,164:52-62. [62] Kookana R S,Sarmah A K,Zwieten L V,et al.Biochar application to soil: agronomic and environmental benefits and unintended consequences[J].Advances in Agronomy, 2011,112:103-143. [63] Gundale M J,Deluca T H.Temperature and source material influence ecological attributes of ponderosa pine and Douglas-fir charcoal[J].Forest Ecology and Management, 2006,231(1):86-93. [64] Strauss E A,Lamberti G A.Regulation of nitrification in aquatic sediments by organic carbon[J].Limnology and Oceanography,2000,45(8):1854-1859. [65] Yoo G,You J K,Yong O L,et al.Investigation of greenhouse gas emissions from the soil amended with rice straw biochar[J]. Ksce Journal of Civil Engineering,2016,20(6): 2197-2207. [66] Gul S,Whalen J K,Thomas B W,et al.Physico-chemical properties and microbial responses in biochar-amended soils:mechanisms and future directions[J].Agriculture, Ecosystems and Environment,2015,206:46-59. [67] Sánchez-García M,Roig A,Sanchez-Monedero M A,et al.Biochar increases soil N2O emissions produced by nitrification-mediated pathways[J].Frontiers in Environmental Science,2014,2(2):1-10. [68] Singh B P,Hatton B J,Balwant S,et al.Influence of biochars on nitrous oxide emission and nitrogen leaching from two contrasting soils[J].Journal of Environmental Quality,2010, 39(4):1224-1235. [69] Karhu K,Mattila T,Bergstr?m I,et al.Biochar addition to agricultural soil increased CH4 uptake and water holding capacity-results from a short-term pilot field study[J].Agriculture, Ecosystems and Environment,2011,140(1-2):309-313. [70] Lehmann J,Gaunt J,Rondon M,et al.Biochar sequestration in terrestrial ecosystems-a review[J].Mitigation & Adaptation Strategies for Global Change,2006,11(2):395-419. [71] 颜永毫,王丹丹,郑纪勇.生物炭对土壤N2O和CH4排放影响的研究进展[J].中国农学通报,2013,29(8):140-146. Yan Y H,Wang D D,Zheng J Y,et al.Advances in effects of biochar on the soil N2O and CH4 emissions[J].Chinese Agricultural Science Bulletin,2013,29(8):140-146.(in Chinese) [72] Wang J,Pan X,Liu Y,et al.Effects of biochar amendment in two soils on greenhouse gas emissions and crop production [J].Plant and Soil,2012,360(1-2):287-298. [73] Cayuela M L,Oenema O,Kuikman P J,et al.Bioenergy by-products as soil amendments? implications for carbon sequestration and greenhouse gas emissions[J].GCB Bioenergy, 2010,2 (4):201-213. [74] Deluca T H,Aplet G H.Charcoal and carbon storage in forest soils of the rocky mountain west[J].Frontiers in Ecology and the Environment,2008,6(1):18-24. [75] Harter J,Guzmanbustamante I,Kuehfuss S,et al.Gas entrapment and microbial N2O reduction reduce N2O emissions from a biochar-amended sandy clay loam soil[J].Scientific Reports, 2016,6:39574. [76] Harter J,Weigold P,El-Hadidi M,et al.Soil biochar amendment shapes the composition of N2O-reducing microbial communities[J].Science of the Total Environment,2016,562: 379-390. [77] Thomson A J,Giannopoulos G,Pretty J,et al.Biological sources and sinks of nitrous oxide and strategies to mitigate emissions[J].Philosophical Transactions of the Royal Society of London,2012,367(1593):1157-1168. [78] Cayuela M L,Sánchezmonedero M A,Roig A,et al.Biochar and denitrification in soils:when,how much and why does biochar reduce N2O emissions [J].Scientific Reports,2013, 3:1732. [79] Ameloot N,Maenhout P,Neve S D,et al.Biochar-induced N2O emission reductions after field incorporation in a loam soil[J].Geoderma,2016,267:10-16. [80] Lin X,Spokas K A,Venterea R T,et al.Assessing microbial contributions to N2O impacts following biochar additions[J]. Agronomy,2014,4(4):478-496. [81] Yao Y,Gao B,Zhang M,et al.Effect of biochar amendment on sorption and leaching of nitrate,ammonium, and phosphate in a sandy soil[J].Chemosphere,2012,89(11):1467-71. [82] Verhoeven E,Six J.Biochar does not mitigate field-scale N2O emissions in a northern California vineyard:an assessment across two years[J].Agriculture,Ecosystems and Environment, 2014,191(15):27-38. [83] Li X.Evidence for denitrification as main source of N2O emission from residue-amended soil[J].Soil Biology and Biochemistry,2016,92:153-160. [84] Pereira E I P,Suddick E C,Mansour I,et al.Biochar alters nitrogen transformations but has minimal effects on nitrous oxide emissions in an organically managed lettuce mesocosm[J].Biology and Fertility of Soils,2015,51(5): 573-582. [85] Sigua G C,Novak J M,Watts D W,et al.Carbon mineral- ization in two ultisols amended with different sources and particle sizes of pyrolyzed biochar[J].Chemosphere, 2014, 103(5):313-321. [86] Nguyen T T N,Xu C Y,Tahmasbian I,et al.Effects of biochar on soil available inorganic nitrogen:a review and meta- analysis[J].Geoderma,2017,288:79-96. [87] Janus A,Pelfrêne A,Heymans S,et al.Elaboration, characteristics and advantages of biochars for the management of contaminated soils with a specific overview on miscanthus biochars[J].Journal of Environmental Management,2015,162: 275-289. [88] Sima X F,Wang Y Y,Shen X C,et al.Robust biochar-assisted alleviation of membrane fouling in MBRs by indirect mechanism[J].Separation and Purification Technology,2017, 184:195-204.