Advance Search
Wang Bao-Ru, Wang Xu, Wang Wei-Bo, Tang Dong-Shan. Cu-NiR and cd1-NiR: Advances in two kinds of denitrifying nitrite reductase[J]. Plant Science Journal, 2021, 39(3): 324-334. DOI: 10.11913/PSJ.2095-0837.2021.30324
Citation: Wang Bao-Ru, Wang Xu, Wang Wei-Bo, Tang Dong-Shan. Cu-NiR and cd1-NiR: Advances in two kinds of denitrifying nitrite reductase[J]. Plant Science Journal, 2021, 39(3): 324-334. DOI: 10.11913/PSJ.2095-0837.2021.30324

Cu-NiR and cd1-NiR: Advances in two kinds of denitrifying nitrite reductase

Funds: 

This work was supported by grants from the National Natural Science Foundation of China (31870452,12075113) and Hengyang Key Laboratory Project for Soil Contamination Control and Remediation (2018HPT06).

More Information
  • Received Date: April 02, 2021
  • Revised Date: April 24, 2021
  • Available Online: October 31, 2022
  • Published Date: June 27, 2021
  • Nitrite reductase (NiR) is a key enzyme in the natural nitrogen cycle that catalyzes the reduction of nitrite. Cu-NiR and cd1-NiR, which are encoded by the nirK and nirS genes, respectively, are rate-limiting enzymes in denitrification. Although they have similar functions, their structures and cofactors are different. In addition, they exhibit different responses to different environmental gradients. The structural characteristics, microbial population distribution, and detection techniques of these two enzymes are reviewed in this report. Furthermore, the environmental factors that determine the expression and activity of the nirS and nirK genes are examined. Finally, future research directions are proposed.
  • [1]
    Klotz MG, Stein LY. Nitrifier genomics and evolution of the nitrogen cycle[J]. FEMS Microbiol Lett, 2008, 278(2):146-156.
    [2]
    Berks BC, Ferguson SJ, Moir JW, Richardson DJ. Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions[J]. Biochim Biophys Acta, 1995, 1232(3):97-173.
    [3]
    Antonyuk SV, Strange RW, Sawers G, Eady RR, Hasnain SS. Atomic resolution structures of resting-state, substrate- and product-complexed Cu-nitrite reductase provide insight into catalytic mechanism[J]. Proc Natl Acad Sci USA, 2005, 102(34):12041-12046.
    [4]
    Zumft WG. Cell biology and molecular basis of denitrification[J]. Microbiol Mol Biol Rev, 1997, 61(4):533-616.
    [5]
    Moura I, Moura JJ. Structural aspects of denitrifying enzymes[J]. Curr Opin Chem Biol, 2001, 5(2):168-175.
    [6]
    Kuypers MM, Marchant HK, Kartal B. The microbial nitrogen-cycling network[J]. Nat Rev Microbiol, 2018, 16(5):263-276.
    [7]
    Wu J, Chen N, Hong H, Lu T, Wang L, Chen Z. Direct measurement of dissolved N2 and denitrification along a subtropical river-estuary gradient, China[J]. Mar Pollut Bull, 2013, 66(1-2):125-134.
    [8]
    Ward BB, Devol AH, Rich JJ,Chang BX,Bulow SE, et al. Denitrification as the dominant nitrogen loss process in the Arabian Sea[J]. Nature, 2009, 461(7260):78-81.
    [9]
    孙建光, 高俊莲, 马晓彤, 徐晶, 姜瑞. 反硝化微生物分子生态学技术及相关研究进展[J]. 中国土壤与肥料, 2007(2):7-12.

    Sun JG, Gao JL, Ma XT, Xu J, Jiang R. Molecular ecological techniques for the study of denitrifiers and progress in related areas[J]. Soil and Fertilizer in China, 2007(2):7-12.
    [10]
    Chen WB, Peng SL. Land-use legacy effects shape microbial contribution to N2O production in three tropical forests[J]. Geoderma, 2020, 358:113979.
    [11]
    邵志江, 汪涛, 张云霞, 郑斌. 干湿交替对自然沟渠沉积物反硝化速率的影响[J]. 环境科学学报, 2020, 40(11):202-209.

    Shao ZJ, Wang T, Zhang YX, Zheng B. Effect of wet and dry alternation in natural ditch sediments[J]. Acta Scien-tiae Circumstantiae, 2020, 40(11):202-209.
    [12]
    Knapp CW, Dodds WK, Wilson KC, O'Brien JM, Graham DW. Spatial heterogeneity of denitrification genes in a highly homogenous urban stream[J]. Environ Sci Tech-nol, 2009, 43(12):4273-4279.
    [13]
    Wang WY, Yang M, Shen PF, Zhang RY, Qin XL, et al. Conservation tillage reduces nitrous oxide emissions by regulating functional genes for ammonia oxidation and denitrification in a winter wheat ecosystem[J]. Soil Tillage Res, 2019, 194:104347.
    [14]
    陈志浩, 覃云斌, 丁帮璟, 胡优优, 陈湜, 李正魁. 宛山荡农田土壤氮迁移过程反硝化与厌氧氨氧化[J]. 环境科学, 2020(1):412-419.

    Chen ZH, Qin YB, Ding BJ, Hu YY, Chen S, Li ZK. Denitrification and anaerobic ammonium oxidation in soil nitrogen migration process in a farmland of wanshandang lake[J]. Environmental Science, 2020(1):412-419.
    [15]
    Jones CM, Hallin S. Ecological and evolutionary factors underlying global and local assembly of denitrifier communities[J]. ISME J, 2010, 4(5):633-641.
    [16]
    Suzuki S, Kataoka K, Yamaguchi K. Metal coordination and mechanism of multicopper nitrite reductase[J]. Acc Chem Res, 2000, 31(10):728-735.
    [17]
    Tocheva EI, Rosell FI, Mauk AG, Murphy ME. Side-on copper-nitrosyl coordination by nitrite reductase[J]. Science, 2004, 304(5672):867-870.
    [18]
    Jacobson F, Pistorius A, Farkas D, Grip WD, Hansson O, et al. pH dependence of copper geometry, reduction potential, and nitrite affinity in nitrite reductase[J]. J Biol Chem, 2007, 282(9):6347-6355.
    [19]
    Yokoyama H, Yamaguchi K, Sugimoto M, Suzuki S. Cu[STBZ]Ⅰ and Cu complexes containing nitrite and tridentate aromatic amine ligand as models for the substrate-binding type-2 Cu site of nitrite reductase[J]. Eur J Inorg Chen, 2005, 2005(8):1435-1441.
    [20]
    Usov OM, Sun Y, Grigoryants VM, Shapleigh JP, Scho-les CP. EPR-ENDOR of the Cu(I)NO complex of nitrite reductase[J]. J Am Chem Soc, 2006, 128(40):13102-13111.
    [21]
    Rudolf M. Cytochrome c nitrite reductase:further investigations of the multiheme enzyme by X-Ray crystallography, site-directed mutagenesis, and EPR spectroscopy[D]. Konstanz:University of Konstanz, 2004.
    [22]
    Zhang HM, Boulanger MJ, Mauk AG, Murphy M. Carbons monoxide binding to copper-containing nitrite reductase from Alcaligenes faecalist[J]. J Phys Chem B, 2000, 104(46):10738-10742.
    [23]
    Kataoka K, Furusawa H, Takagi K, Yamaguchi K, Suzuki S. Functional analysis of conserved aspartate and histidine residues located around the type 2 copper site of copper-containing nitrite reductase[J]. J Biochem, 2000, 127(2):345-350.
    [24]
    Horrell S, Kekilli D, Strange RW, Hough MA. Recent structural insights into the function of copper nitrite reductases[J]. Metallomics, 2017, 9(11):1470-1482.
    [25]
    Lehnert N, Cornelissen U, Neese F, Ono T, Noguchi Y, et al. Synthesis and spectroscopic characterization of copper(Ⅱ)-nitrito complexes with hydrotris(pyrazolyl)borate and related coligands[J]. Inorg Chem, 2007, 46(10):3916-3933.
    [26]
    Williams PA, Fül p V, Garman EF, Saunders NF, Ferguson SJ, Hajdu J. Haem-ligand switching during catalysis in crystals of a nitrogen-cycle enzyme[J]. Nature, 1997, 389(6649):406-412.
    [27]
    Nurizzo D, Cutruzzolà F, Arese M, D Bourgeois, Brunori M, et al. Conformational changes occurring upon reduction and NO binding in nitrite reductase from Pseudomonas aeruginosa[J]. Biochemistry, 1998, 37(40):13987-13996.
    [28]
    杨航, 黄钧, 刘博. 异养硝化-好氧反硝化菌Paracoccus pantotrophus ATCC 35512的研究进展[J]. 应用与环境生物学报, 2008, 14(4):585-592.

    Yang H, Huang J, Liu B. Advances in research of heterotrophic nitrification-aerobic denitrification strain Paracoccus pantotrophus ATCC 35512[J]. Chin J Appl Environ Biol, 2008, 14(4):585-592.
    [29]
    Horio T, Higashi T, Yamanka T, Matsubara H, Okunuki K. Purification and properties of cytochrome oxidase from Pseudomonas aeruginosa[J]. J Biol Chem, 1961, 236:944-951.
    [30]
    Pedroso HA, Silveira CM, Almeida RM, Almeida A, Besson S, et al. Electron transfer and docking between cytochrome cd1 nitrite reductase and different redox partners-a comparative study[J]. Biochim Biophys Acta, 2016, 1857(9):1412-1421.
    [31]
    Sudhamsu J, Crane BR. Bacterial nitric oxide synthases:what are they good for?[J]. Trends Microbiol, 2009, 17(5):212-218.
    [32]
    Radoul M, Bykov D, Rinaldo S, Cutruzzolà F, Neese F, Goldfarb D. Dynamic hydrogen-bonding network in the distal pocket of the nitrosyl complex of Pseudomonas aeruginosa cd1 nitrite reductase[J]. J Am Chem Soc, 2011, 133(9):3043-3055.
    [33]
    Holzenburg A, Scrutton NS. Enzyme-Catalyzed Electron and Radical Transfer[M]. New York:Kluwer Academic/Plenum Publishers, 2000.
    [34]
    Richter CD, Allen JW, Higham CW, Koppenhofer A, Zajicek RS, et al. Cytochrome cd1, reductive activation and kinetic analysis of a multifunctional respiratory enzyme[J]. J Biol Chem, 2002, 277(5):3093-3100.
    [35]
    Moir JW, Baratta D, Richardson DJ, Ferguson SJ. The purification of a cd1-type nitrite reductase from, and the absence of a copper-type nitrite reductase from, the aerobic denitrifier Thiosphaera pantotropha; the role of pseu-doazurin as an electron donor[J]. Eur J Biochem, 1993, 212(2):377-385.
    [36]
    贺纪正, 张丽梅. 土壤氮素转化的关键微生物过程及机制[J]. 微生物学通报, 2013, 40(1):98-108.

    He JZ, Zhang LM. Key processes and microbial mechanisms of soil nitrogen transformation[J]. Microbiology China, 2013, 40(1):98-108.
    [37]
    Boulanger MJ, Murphy MEP. Alternate substrate binding modes to two mutant (D98N and H255N) forms of nitrite reductase from Alcaligenes faecalis S-6:structural model of a transient catalytic intermediate[J]. Biochemistry, 2001, 40(31):9132-9141.
    [38]
    Priemé A, Braker G, Tiedje JM. Diversity of nitrite reductase (nirK and nirS) gene fragments in forested upland and wetland soils[J]. Appl Environ Microbiol, 2002, 8(4):1893-1900.
    [39]
    蔡小龙, 罗剑飞, 林炜铁, 田国梁. 珠三角养殖水体中参与氮循环的微生物群落结构[J]. 微生物学报, 2012, 52(5):645-653.

    Cai XL, Luo JF, Lin YT, Tian GL. Microbial community in nitrogen cycle of aquaculture water of the Pearl River Delta[J]. Acta Microbiologica Sinica, 2012, 52(5):645-653.
    [40]
    辛玉峰, 赵天颖, 曲晓华. 两类产NO的亚硝酸盐还原酶的分布,结构与序列比较及宏基因组分析[J]. 微生物学报, 2017, 57(4):597-608.

    Xin YF, Zhao TY, Qu XH. Distribution, structure and sequence alignment, and metagenomics analysis of two nitrite reductases with NO forming[J]. Acta Microbiologica Sinica, 2017, 57(4):597-608.
    [41]
    Braker G, Zhou J, Wu L, Devol AH, Tiedje JM. Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in pacific northwest marine sediment communities[J]. Appl Environ Microbiol, 2000, 66(5):2096-2104.
    [42]
    刘建国, 刘卫国. 微生物介导的氮循环过程研究进展[J]. 草地学报, 2018, 26(2):277-283.

    Liu JG, Liu WG. Advances in microbial-mediated nitrogen cycling[J]. Acta Agrestia Sinica, 2018, 26(2):277-283.
    [43]
    Wei W, Isobe K, Nishizawa T, Zhu L, Shiratori Y, et al. Higher diversity and abundance of denitrifying microorga-nisms in environments than considered previously[J]. ISME J, 2015, 9(9):1954-1965.
    [44]
    Shi RJ, Huang HH, Qi ZH, Han TT. Distribution patterns of nirS-encoding and nirK-encoding denitrifiers in the surface sediment of the Pearl river estuary[J]. Russ J Mar Biol, 2019, 45(6):453-463.
    [45]
    Aalto SL, Saarenheimo J, Arvola L, Arvola L, Tiirola M, Rissanen AJ. Denitrifying microbial communities along a boreal stream with varying land-use[J]. Aquatic Sci, 2019, 81(4):59.
    [46]
    Smith JM, Ogram A. Genetic and functional variation in denitrifier populations along a short-term restoration chronosequence[J]. Appl Environ Microbiol, 2008, 74(18):5615-5620.
    [47]
    Desnues C, Michotey VD, Wieland A, Cui Z, Fourcans A, et al. Seasonal and diel distributions of denitrifying and bacterial communities in a hypersaline microbial mat (Camargue, France)[J]. Water Res, 2007, 41(15):3407-3419.
    [48]
    Yi N, Gao Y, Zhang Z, Wang Y, Liu X, et al. Response of spatial patterns of denitrifying bacteria communities to water properties in the stream inlets at dianchi lake, China[J]. Int J Genomics, 2015, 2015(9):1-11.
    [49]
    Coyne MS, Arunakumari A, Averill BA, Tiedje JM. Immunological identification and distribution of dissimilatory heme cd1 and nonheme copper nitrite reductases in denitrifying bacteria[J]. Appl Environ Microbiol, 1989, 55(11):2924-2931.
    [50]
    陈刚亮, 李建华, 王育来. 河岸带土壤反硝化作用研究进展[J]. 安徽农业科学, 2012, 40(391):14799-14803.

    Chen GL, Li JH, Wang YL. Research advances in riparian soil denitrification[J]. Journal of Anhui Agri Sci, 2012, 40(391):14799-14803.
    [51]
    Ju F, Beck K, Yin X, Maccagnan A, Mcardell CS, et al. Wastewater treatment plant resistomes are shaped by bacterial composition, genetic exchange, and upregulated expression in the effluent microbiomes[J]. ISME J, 2019, 13(2):346-360.
    [52]
    Jia Z, Conrad R. Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil[J]. Environ Microbiol, 2009, 11(7):1658-1671.
    [53]
    Eichorst SA, Strasser F, Woyke T, Schintlmeister A, Wagner M, Woebken D. Advancements in the application of NanoSIMS and Raman microspectroscopy to investigate the activity of microbial cells in soils[J]. FEMS Microbiol Ecol, 2015, 91(10):fiv106.
  • Related Articles

    [1]Li Li-Jun, Miao Ling-Feng, Li Da-Dong, Yang Fan. Effects of drought and nitrogen application on the growth and chlorophyll fluorescence characteristics of Dalbergia odorifera T. Chen - Hevea brasiliensis Muell. Arg seedlings[J]. Plant Science Journal, 2023, 41(3): 358-369. DOI: 10.11913/PSJ.2095-0837.22196
    [2]Guo Lu-Yao, Miao Ling-Feng, Li Da-Dong, Xiang Li-Shan, Yang Fan. Effects of nitrogen addition and warming on growth, development, and physiological characteristics of Dalbergia odorifera T. Chen seedlings[J]. Plant Science Journal, 2022, 40(2): 259-268. DOI: 10.11913/PSJ.2095-0837.2022.20259
    [3]Cai Yuan-Bao, Yang Xiang-Yan. Codon usage bias and its influencing factors in the chloroplast genome of Macadamia integrifolia Maiden & Betche[J]. Plant Science Journal, 2022, 40(2): 229-239. DOI: 10.11913/PSJ.2095-0837.2022.20229
    [4]Wang Yu-Chen, Wang Wen-Juan, Zhong Yue-Ming, Lei Shan-Qing, Li Jing-Wen. Study on the foraging behavior of clonal roots and its influencing factors in Populus euphratica Oliv.[J]. Plant Science Journal, 2020, 38(3): 410-417. DOI: 10.11913/PSJ.2095-0837.2020.30410
    [5]Pu Yu-Jin, Zhang Li-Jia, Miao Ling-Feng, Yang Fan. Effects of different calcium concentrations on the growth and physiological characteristics of Dalbergia odorifera under low temperatures[J]. Plant Science Journal, 2019, 37(2): 251-259. DOI: 10.11913/PSJ.2095-0837.2019.20251
    [6]Wang Yue-Lin, Xu Da-Ping, Yang Zeng-Jiang, Liu Xiao-Jin, Hong Zhou, Zhang Ning-Nan. Effects of transplantation and potassium fertilizer on the photosynthetic characteristics and chlorophyll content of Dalbergia odorifera[J]. Plant Science Journal, 2018, 36(6): 879-887. DOI: 10.11913/PSJ.2095-0837.2018.60879
    [7]ZHU Xia-Xia, ZHANG Hua, ZHU Yan, LIU Jian-Gang, ZHU Ye-Ping, LÜ Rui, WANG Ying, MA Ming-Jun. Forest Community Species Diversity and the Influencing Factors in the Rock Stream Periglacial Landforms of Mt. Laotudingzi[J]. Plant Science Journal, 2016, 34(1): 67-77. DOI: 10.11913/PSJ.2095-0837.2016.10067
    [8]YANG Qi-He, YE Wan-Hui, LIAO Fu-Lin, LIU Zhi-Wei, YIN Xiao-Juan. Experimental Factors Affecting Studying Characteristics of Seed Storage[J]. Plant Science Journal, 2006, 24(5): 469-475.
    [9]HUANG Xuan, XU Zi-Qin, HAO Jian-Guo, LI Jing. Factors Affecting Wheat(Triticum aestivum L.)Transformation Mediated by Biolistic Bombardment[J]. Plant Science Journal, 2004, 22(2): 111-115.
    [10]Zhang Youde, Zhang Junzhi, Mei Fangzhu, Zhou Daming, Hu Delin, Wang Yuanfu. THE TILLERING RULE ON EULALIOPSlS BINATA AND ITS CONTROLLING FACTORS[J]. Plant Science Journal, 1993, 11(2): 185-192.
  • Cited by

    Periodical cited type(6)

    1. Hui Wang,Jiping Zhang,Benyong Wei,Qing Qiao,Wentao Zhang,Yangcui Ning,Chunlan Liu. The effects of climate change on Pinus tabulaeformis radial growth in the Xiaowutai Mountains, northern China. Journal of Forestry Research. 2025(01): 115-125 .
    2. 常素玲. 山西省关帝山林区油松径向生长对气候的响应. 山西林业科技. 2024(01): 24-27 .
    3. 韦晓旭,彭剑峰,彭猛,李轩,崔佳月,李金宽,魏亚飞. 中国南北过渡带油松径向生长对气候因子的响应研究——以鸡公山国家级自然保护区为例. 地理科学. 2024(09): 1643-1652 .
    4. 李镇江,于晨一,刘升云,闫瑞环,黄心邓,刘晓静,陈志成,王婷. 伏牛山南坡3种针叶树径向生长对气候变化的响应. 应用生态学报. 2023(05): 1178-1186 .
    5. 李夏榕,陈怡歆,陈静飞,朱济友,孙广鹏,韦柳端,张新娜,徐程扬. 气候变化对北京近远郊地区油松径向生长影响的比较研究. 北京林业大学学报. 2022(01): 19-28 .
    6. 乔梁,陈雪,高梦竹,王子洋. 气候旅游资源-植被观赏气象指数研究. 黑龙江气象. 2022(03): 18-21 .

    Other cited types(4)

Catalog

    Article views (1186) PDF downloads (566) Cited by(10)

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return