芽孢杆菌的耐盐促生机制研究进展

doi:10.13560/j.cnki.biotech.bull.1985.2020-0746

摘要/Abstract

摘要： 土壤盐渍化严重制约着农业的发展,是我国亟待解决的问题之一。芽孢杆菌的抗逆性强并具有优良的耐盐特性,可缓解盐胁迫对植物造成的损伤,从而提高植株的耐盐生长能力。简要概述了芽孢杆菌的基本生物学特性与应用及其相关耐盐基因,并以盐胁迫对植物的影响为切入点,从7个方面综述了芽孢杆菌对植物的耐盐促生机制。另外也讨论了芽孢杆菌研究与应用中存在的一些问题,并展望了其作为植物根际促生细菌与植物、土壤间的相互作用,以期为盐碱地的改良、微生物菌种的应用及农作物促生方面提供理论参考。

关键词: 芽孢杆菌, 耐盐机制, 盐胁迫, 促生, PGPR

Abstract: Soil salinization seriously restricts the development of agriculture and this is one of urgent problems to be solved in China. Bacillus has strong stress resistance and excellent salt tolerance,thus which can alleviate the damage caused by salt stress and improve the salt tolerance of plants. This paper briefly summarizes the general characteristics and application of Bacillus as well as the salt-tolerant genes of Bacillus,and reviews the salt-tolerant and growth-promoting mechanism of Bacillus on plant growth from seven aspects. In addition,this paper also discusses some issues in the research and development of Bacillus,and prospects the interactions between Bacillus as plant rhizosphere growth-promoting bacterium and plants or soil,aiming to provide theoretical reference for the improvement of saline-alkali land,the industrial application of microbial strains,and the growth promotion of crops.

Key words: Bacillus, salt tolerance mechanism, salt stress, growth promotion, PGPR

胡玉婕, 朱秀玲, 丁延芹, 杜秉海, 汪城墙. 芽孢杆菌的耐盐促生机制研究进展[J]. 生物技术通报, 2020, 36(9): 64-74.

HU Yu-jie, ZHU Xiu-ling, DING Yan-qin, DU Bing-hai, WANG Cheng-qiang. Research Progress on Salt Tolerance and Growth-promoting Mechanism of Bacillus[J]. Biotechnology Bulletin, 2020, 36(9): 64-74.

参考文献

[1] 李光超. 黄河三角洲土壤盐渍化研究综述[J]. 安徽农学通报, 2020, 26(Z1):113-115.
Li GC.A summary on soil salinization of Yellow River Delta[J]. Anhui Agricilltarul Sciere Bulletin, 2020, 26(Z1):113-115.
[2] 翟彩娇, 邓先亮, 张蛟, 等. 盐分胁迫对稻米品质性状的影响[J]. 中国稻米, 2020, 26(2):44-48.
Zhai CJ, Deng XL, Zhang J, et al.Effects of salt stress on quality traits of japonica rice[J]. Chinese Rice, 2020, 26(2):44-48.
[3] 努尔沙吾列·哈斯木汉. 新疆土壤盐渍化成因及其防治对策[J]. 科学技术创新, 2020(9):52-53.
Nurshawulie KH.Causes of soil salinization in Xinjiang and its control measures[J]. Scientific and Technological Innovation, 2020(9):52-53.
[4] 赵娇, 谢慧君, 张建. 黄河三角洲盐碱土根际微环境的微生物多样性及理化性质分析[J]. 环境科学, 2020, 41(3):1449-1455.
Zhao J, Xie HJ, Zhang J.Microbial diversity and physicochemical properties of rhizosphere microenvironment in saline-alkali of the Yellow River Delta[J]. Environmental Science, 2020, 41(3):1449-1455.
[5] Madhurankhi G, Suresh D.Plant growth-promoting rhizobacteria-alleviators of abiotic stresses in soil:a review[J]. Pedosphere, 2020, 30(1):40-61.
[6] Wu TY, Wu XQ, Xu XQ, et al.Salt tolerance mechanism and species identification of the plant rhizosphere bacterium JYZ-SD₂[J]. Curr Microbiol, 2020, 77(3):388-395.
[7] Patel RR, Patel DD, Thakor P, et al.Alleviation of salt stress in germination of vigna radiataL. by two halotolerant Bacilli sp. isolated from saline habitats of Gujarat[J]. Plant Growth Regulation, 2015, 76(1):51-60.
[8] Paul S, Aggarwal C, Thakur JK, et al.Induction of osmoadaptive mechanisms and modulation of cellular physiology help Bacillus licheniformis strain SSA61 adapt to salt stress[J]. Curr Microbiol, 2015, 70(4):610-617.
[9] 东秀珠, 蔡妙英. 常见细菌系统鉴定手册[M]. 北京:科学出版社, 2001.
Dong XZ, Cai MY.Handbook of systematic identification of common bacteria[M]. Beijing:Science Press, 2001.
[10] Marta T, Inmaculada L, Borja T, et al.Growth promotion on horticultural crops and antifungal activity of Bacillus velezensis XT1[J]. Applied Soil Ecology, 2020, 150:103453.
[11] 翟世玉, 殷辉, 周建波, 等. 枯草芽孢杆菌与钾联用对黑腐皮菌的抑制作用[J]. 山西农业科学, 2019, 47(4):660-664.
Zhai SY, Yin H, Zhou JB, et al.Inhibitory effect of Bacillus subtilis combined with potassium against valsa mali[J]. Journal of Shanxi Agricultural Science, 2019, 47(4):660-664.
[12] Azabou MC, Gharbi Y, Medhioub I, et al.The endophytic strain Bacillus velezensis OEE1:an efficient biocontrol agent against verticillium wilt of olive and a potential plant growth promoting bacteria[J]. Biological Control, 2020, 142:104168.
[13] 徐宁, 程海娇, 刘清岱, 等. 细菌Na+/H+逆向转运蛋白的研究进展[J]. 微生物学通报, 2015, 42(10):2002-2011.
Xu N, Cheng HJ, Liu QD, et al.Research progress of the Na+/H+ antiporters in bacteria[J]. Microbiology China, 2015, 42(10):2002-2011.
[14] Ito M, Guffanti AA, Zemsky J, Ivey DM, et al.Role of the nhaC-encoded Na+/H+ antiporter of alkaliphilic Bacillus firmus OF4[J]. Bacteriol, 1997, 179(12):3851-3857.
[15] Yang LF, Zhang B, Wang L, et al.The short C-terminal hydrophilic domain of NhaH Na+/H+ antiporter from Halobacillus dabanensis with roles in resistance to salt and in pH sensing[J]. Chinese Science Bulletin, 2008, 53(21):3311-3316.
[16] Fujisawa M, Kusumoto A, Wada Y, et al.NhaK, a novel monovalent cation/H+ antiporter of Bacillus subtilis[J]. Archives of Microbiology, 2005, 183(6):411-420.
[17] Morino M, Suzuki T, Ito M, et al.Purification and functional reconstitution of a seven-subunit mrp-type na+/h+ antiporter[J]. Journal of Bacteriology, 2014, 196(1):28-35.
[18] Cheng B, Meng Y, Cui Y, et al.Alkaline response of a halotolerant alkaliphilic halomonas strain and functional diversity of its Na+(K+)/H+ antiporters[J]. Journal of Biological Chemistry, 2016, 291(50):26056-26065.
[19] 张薇, 魏海雷, 高洪文, 等. 中度嗜盐菌四氢嘧啶合成基因的克隆与功能分析[J]. 生物工程学报, 2008(3):395-400.
Zhang W, Wei HL, Gao HW, et al.Cloning and characterization of ectABC cluster from Bacillus alcalophilus DTY1[J]. Chinese Journal of Biotechnology, 2008(3):395-400.
[20] 鞠建松, 徐书景, 宋瑞甜, 等. 一种合成四氢嘧啶的三基因共表达载体及应用:中国, CN201710820910. 8[P].2017-09-13.
Ju JS, Xu SJ, Song RT, et al. Synthesis and application of three-gene co-expression vector of tetrahydropyrimidine:China, CN201710820910. 8[P].2017-09-13.
[21] Brill J, Hoffmann T, Bleisteiner M, et al.Osmotically controlled synthesis of the compatible solute proline is critical for cellular defense of Bacillus subtilis against high osmolarity[J]. Journal of Bacteriology, 2011, 193(19):5335-5346.
[22] Hoffmann T, Bleisteiner M, Sappa PK, et al.Synthesis of the compatible solute proline by Bacillus subtilis:point mutations rendering the osmotically controlled proHJ promoter hyperactive[J]. Environmental Microbiology, 2017, 19(9):3700-3720.
[23] Hecker M, Völker U.General stress response of Bacillus subtilis and other bacteria[J]. Advances in Microbial Physiology, 2001, 44(4):35.
[24] Krüger E, Völker U, Hecker M.Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance[J]. Journal of Bacteriology, 1994, 176(11):3360-3367.
[25] Hantke I, Schäfer H, Janczikowski A, et al.YocM a small heat shock protein can protect Bacillus subtilis cells during salt stress[J]. Molecular Microbiology, 2019, 111(2):423-440.
[26] Hecker M, Völker U.Non-specific, general and multiple stress resistance of growth-restricted Bacillus subtilis cells by the expression of the sigmaB regulon[J]. Molecular Microbiology, 1998, 29(5):1129-1136.
[27] Hahne H, Mäder U, Otto A, et al.A comprehensive proteomics and transcriptomics analysis of Bacillus subtilis salt stress adaptation[J]. Bacteriol, 2010, 192(3):870-882.
[28] Kunst F, Rapoport G.Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis[J]. Bacteriol, 1995, 177(9):2403-2407.
[29] Kaiumov AR, Balaban NP, Mardanova AM, et al.Biosynthesis of the subtilisin-like serine proteinase of Bacillus intermedius under salt stress conditions[J]. Mikrobiologiia, 2006, 75(5):642.
[30] Dartois V, Débarbouillé M, Kunst F, et al.Characterization of a novel member of the DegS-DegU regulon affected by salt stress in Bacillus subtilis[J]. Bacteriol, 1998, 180(7):1855-1861.
[31] Kharitonova MA, Kipenskaya LV, Ilinskaya ON.Activation of biosynthesis of guanyl-specific ribonuclease secreted by Bacillus circulans under salt stress[J]. Molecular Biology, 2016, 50(6):874-879.
[32] Yin L, Xue Y, Ma Y.Global microarray analysis of alkaliphilic halotolerant bacterium Bacillus sp. N16-5 salt stress adaptation[J]. PLoS One, 2015, 10(6):e0128649.
[33] Lee JM, Kim YR, Kim JK, et al.Characterization of salt-tolerant beta-glucosidase with increased thermostability under high salinity conditions from Bacillus sp SJ-10 isolated from jeotgal, a traditional Korean fermented seafood[J]. Bioprocess & Biosystems Engineering, 2015, 38(7):1335-1346.
[34] Zhang W, Xu H, Wu Y, et al.A new cold-adapted, alkali-stable and highly salt-tolerant esterase from Bacillus licheniformis[J]. International Journal of Biological Macromolecules, 2018, 111:1183-1193.
[35] Wang TT, Ding P, Chen P, et al.Complete genome sequence of endophyte Bacillus flexus KLBMP 4941 reveals its plant growth promotion mechanism and genetic basis for salt tolerance[J]. Journal of Biotechnology, 2017, 260:38-41.
[36] 金河坡. 分离于酱油渣蜡样芽胞杆菌的耐盐机制研究[D]. 广州:华南理工大学, 2016.
Jin HP.Isolation and salt tolerance mechanism of Bacillus cereus from soy bean sauce residue[D]. Guangzhou:South China University of Science and Engineering, 2016.
[37] 江晓慧, 高阳, 王广帅, 等. 基于FvCB模型分析盐分胁迫对棉花叶片光合作用的影响[J]. 应用生态学报, 2020, 31(5):1653-1659.
Jiang XH, Gao Y, Wang GS, et al.Examining effects of salt stress on leaf photosynthesis of cotton based on the FvCB model[J]. Chinese Journal of Applied Ecology, 2020, 31(5):1653-1659.
[38] 李有芳, 王石平, 丁金金, 等. 盐胁迫对小麦根系氧化损伤及细胞程序性死亡的影响[J]. 麦类作物学报, 2019, 39(11):1326-1332.
Li YF, Wang YS, Ding JJ, et al.Effect of salt stress on oxidative damage and programmed cell death in wheat roots[J]. Journal of Triticeae Crops, 2019, 39(11):1326-1332.
[39] 徐曼, 王茜, 王奕骁, 等. 不同盐胁迫对长穗偃麦草种子萌发及幼苗生长的影响[J]. 中国草地学报, 2020, 42(1):15-20.
Xu M, Wang Q, Wang YX, et al.Effects of different salt stress on seed germination and seedling growth of elytrigia elongate[J]. Chinese Journal of Grassland, 2020, 42(1):15-20.
[40] 纪超, 王晓辉, 刘训理. 盐胁迫环境下植物促生菌的作用机制研究进展[J]. 生物技术通报, 2020, 36(4):131-143.
Ji C, Wang XH, Liu XL.Research progress on the action mechanism of plant growth-promoting bacteria under salt stress[J]. Biotechnology Bulletin, 2020, 36(4):131-143.
[41] Woo O, Kim H, Kim JS, et al.Bacillus subtilis strain GOT9 confers enhanced tolerance to drought and salt stresses in arabidopsis thaliana and brassica campestris[J]. Plant Physiol Biochem, 2020, 148:359-367.
[42] Yasmin H, Naeem S, Bakhtawar M, et al.Halotolerant rhizobacteria pseudomonas pseudoalcaligenes and Bacillus subtilis mediate systemic tolerance in hydroponically grown soybean(Glycine max L.)against salinity stress[J]. PLoS One, 2020, 15(4):e0231348.
[43] 徐瑛, 郭晓农, 蔡德育. 解淀粉芽孢杆菌GB03对藜麦生长影响的初探[J]. 大麦与谷类科学, 2019, 36(5):10-14.
Xu Y, Guo XN, Cai DY.Preliminary study on the effects of Bacillus amyloliquefaciens GB03 on the growth of Chenopodium quinoa Willd[J]. Barley and Cereal Sciences, 2019, 36(5):10-14.
[44] Lorena RC, Erika B.Microbial volatile organic compounds produced by Bacillus amyloliquefaciens GB03 ameliorate the effects of salt stress in mentha piperita principally through acetoin emission[J]. Journal of Plant Growth Regulation, 2019.
[45] 刘环. 促进玉米耐盐碱细菌的分离筛选及其作用研究[D]. 银川:北方民族大学, 2019.
Liu H.Isolation and characterization of bacteria mitigating saline-alkine stress on zea mays[D]. Yinchuan:North Minzu University, 2019.
[46] Chauhan PS, Lata C, Tiwari S, et al.Transcriptional alterations reveal Bacillus amyloliquefaciens-rice cooperation under salt stress[J]. Scientific Reports, 2019, 9(1):11912.
[47] Chen L, Liu Y, Wu G, et al.Induced maize salt tolerance by rhizosphere inoculation of Bacillus amyloliquefaciens SQR9[J]. Physiologia Plantarum, 2016, 158(1):34-44.
[48] 袁海, 何鹏飞, 吴毅歆, 等. 盐胁迫下益生菌对玉米的促生效应研究[J]. 玉米科学, 2019, 27(1):69-74.
Yuan H, He PF, Wu YX, et al.Effects of the beneficial bacteria promoting maize growth under salt stress[J]. Journal of Maize Sciences, 2019, 27(1):69-74.
[49] 钱兰华, 钱玮, 沈雪林, 等. 耐盐促生菌的筛选鉴定及其对黄瓜的促生作用[J]. 江苏农业科学, 2019, 47(18):160-163.
Qian LH, Qian W, Shen XL, et al.Screening and identification of salt-tolerant bacteria and its promoting effect on cucumber[J]. Jiangsu Agricultural Sciences, 2019, 47(18):160-163.
[50] Xiong YW, Li XW, Wang TT, et al.Root exudates-driven rhizosphere recruitment of the plant growth-promoting rhizobacterium Bacillus flexus KLBMP 4941 and its growth-promoting effect on the coastal halophyte Limonium sinense under salt stress[J]. Ecotoxi Environ Safety, 2020, 194:110374.
[51] Zhang Z, Yin L, Li X, et al.Analyses of the complete genome sequence of the strain Bacillus pumilus ZB201701 isolated from rhizosphere soil of maize under drought and salt stress[J]. Microbes Environ, 2019, 34(3):310-315.
[52] Singh RP, Jha PN.A halotolerant bacterium Bacillus licheniformis HSW-16 augments induced systemic tolerance to salt stress in wheat plant(Triticum aestivum)[J]. Frontiers in Plant Science, 2016, 7(1252):1890.
[53] Misra S, Chauhan PS.ACC deaminase-producing rhizosphere competent Bacillus sp. mitigate salt stress and promote zea mays growth by modulating ethylene metabolism[J]. 3 Biotech, 2020, 10(3):119.
[54] Wang W, Wu Z, He Y, et al.Plant growth promotion and alleviation of salinity stress in capsicum annuum L. by Bacillus isolated from saline soil in Xinjiang[J]. Ecotoxicology & Environmental Safety, 2018, 164:520-529.
[55] El-Esawi MA, Alaraidh IA, Alsahli AA, et al.Bacillus firmus(SW5)augments salt tolerance in soybean(Glycine max L.)by modulating root system architecture, antioxidant defense systems and stress-responsive genes expression[J]. Plant Physiology & Biochemistry, 2018, 132:375-384.
[56] Rafiq K, Sohail Akram M, Shahid M, et al.Enhancement of salt tolerance in maize(Zea mays L.)using locally isolated Bacillus sp. SR-2-1/1[J]. Biologia, 2020, 75:1425-1436.
[57] Baek D, Rokibuzzaman M, Khan A, et al.Plant-growth promoting Bacillus oryzicola YC7007 modulates stress-response gene expression and provides protection from salt stress[J]. Frontiers in Plant Science, 2020, 10:1646.
[58] Orozco-Mosqueda MDC, Glick BR, Santoyo G.ACC deaminase in plant growth-promoting bacteria(PGPB):an efficient mechanism to counter salt stress in crops[J]. Microb Res, 2020, 235:126439.
[59] 刘珂. 转蜡样芽孢杆菌acdS基因改善烟草耐盐性研究[D]. 郑州:郑州大学, 2017.
Liu K.The research of cloning the acdS gene of Bacillus cereus into tobacco to improve its salt tolerance[D]. Zhengzhou:Zhengzhou University, 2017.
[60] 姚强, 董晓霞, 宫志远, 等. 滨海盐碱地产ACC脱氨酶细菌的筛选及根际促生研究[J]. 山东农业科学, 2020, 52(2):54-58.
Yao Q, Dong XX, Gong ZY, et al.Screening and rhizosphere promotion of bacteria producing ACC deaminase in coastal saline-alkali land[J]. Shandong Agricultural Sciences, 2020, 52(2):54-58.
[61] Amna, Ud Din B, Sarfraz S, et al. Mechanistic elucidation of germination potential and growth of wheat inoculated with exopolysaccharide and ACC- deaminase producing Bacillus strains under induced salinity stress[J]. Ecotoxi Environ Safety, 2019, 183:109466.
[62] Bokhari A, Essack M, Lafi FF, et al.Bioprospecting desert plant Bacillus endophytic strains for their potential to enhance plant stress tolerance[J]. Scientific Reports, 2019, 9(1):18154.
[63] Bokhari A, Essack M, Lafi FF, et al.Mitigation of salt stress in wheat seedlings by halotolerant bacteria isolated from saline habitats[J]. Springerplus, 2013, 2(1):6.
[64] Khan N, Bano A, Ali S, et al.Crosstalk amongst phytohormones from planta and PGPR under biotic and abiotic stresses[J]. Plant Growth Regulation, 2020, 90:189-203.
[65] 李海洋, 李爱学, 王成, 等. 盐胁迫对苗期向日葵内源激素含量的影响[J]. 干旱地区农业研究, 2018, 36(6):92-97.
Li HY, Li AX, Wang C, et al.Effects of salt stress on endogenous hormone contents in sunflower seedlings[J]. Agricultural Research in Arid Areas, 2018, 36(6):92-97.
[66] 涂文文. NaCl处理对酸枣幼苗内源激素含量的影响及转录组测序分析[D]. 石河子:石河子大学, 2019.
Tu WW.Effect of NaCl treatment on the content of endogenous hormones in jujube seedings and the analysis of transcription group sequencing[D]. Shihezi:Shihezi University, 2019.
[67] 魏士平, 刘贝贝. 产生生长素的类短短芽孢杆菌及其应用:中国, CN201910507692. 1[P].2019-11-01.
Wei SP, Liu BB. Application of a Bacillus brevis strain producing auxin:China, CN201910507692. 1[P].2019-11-01.
[68] 汪钱龙, 张德智, 王菊芬, 等. 不同植物促生细菌对玉米生长的影响及其生长素分泌能力研究[J]. 云南农业大学学报:自然科学, 2015, 30(4):494-498.
Wang QL, Zhang DZ, Wang JF, et al.Effects of plant growth-promoting bacterial on the growth of maize and the IAA secrete ability detection[J]. Journal of Yunnan Agricultural University:Natural Science, 2015, 30(4):494-498.
[69] Khan AM, Asaf S, Khan AL, et al.Halotolerant rhizobacterial strains mitigate the adverse effects of NaCl stress in soybean seedlings[J]. Biomed Research International, 2019, 2019:9530963.
[70] 王磊, 冯二梅, 宿红艳. 烟台海域一株中度嗜盐芽孢杆菌YTM-5的鉴定及其耐盐机制研究[J]. 新乡学院学报:自然科学版, 2010, 27(3):50-55.
Wang L, Feng EM, Su HY.Identification of a moderately halophilic Bacillus Strain YTM-5 in Yantai sea area and the preliminary study of its salt-tolerant mechanism[J]. Journal of Xinxiang University:Natural Science Edition, 2010, 27(3):50-55.
[71] Xu Y, Zhang D, Dai L, et al.Influence of salt stress on growth of spermosphere bacterial communities in different peanut(Arachis hypogaea L.)cultivar[J]. International Journal of Molecular Sciences, 2020, 21(6):2131.
[72] 郭英, 刘栋, 赵蕾. 生防枯草芽孢杆菌胞外植酸酶对小麦耐盐性的影响[J]. 应用与环境生物学报, 2009, 15(1):39-43.
Guo Y, Liu D, Zhao L.Effect of extracellular phytase produced by Bacillus subtilis T2 on salt tolerance of wheat seedlings[J]. Chinese Journal of Applied & Environmental Biology, 2009, 15(1):39-43.
[73] Boukhris I, Farhat-Khemakhem A, Blibech M, et al.Characteriza-tion of an extremely salt-tolerant and thermostable phytase from Bacillus amyloliquefaciens US573[J]. International Journal of Biological Macromolecules, 2015, 80:581-587.
[74] Lee S, Trinh CS, Lee WJ, et al. Bacillus subtilis strain L1 promotes nitrate reductase activity in arabidopsis and elicits enhanced growth performance in arabidopsis, lettuce, and wheat[J]. Journal of Plant Research, 2020, 133(2):231-244.
[75] Liang W, Ma X, Wan P, et al.Plant salt-tolerance mechanism:a review[J]. Biochemical and Biophysical Research Communications, 2018, 495(1):286-291.
[76] Nautiyal CS, Srivastava S, Chauhan PS, et al.Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress[J]. Plant Physiol Biochem, 2013, 66:1-9.
[77] Chen L, Liu Y, Wu G, et al.Beneficial rhizobacterium Bacillus amyloliquefaciens SQR9 induces plant salt tolerance through spermidine production[J]. Molecular Plant Microbe Interactions, 2017, 30(5):423-432.
[78] 蒲强. 多功能芽孢杆菌筛选及其促生长和吸附镉效果与机理研究[D]. 广州:华南农业大学, 2017.
Pu Q.Study on screening of multifunctional Bacillus and its effect and mechanism on plant growth and biosorption of cadmium[D]. Guangzhou:South China Agricultural University, 2017.
[79] 谢庆东, 何琳燕, 王琪, 等. 一株高效溶解钾长石芽孢杆菌的分离鉴定与生物学特性研究[J]. 土壤, 2017, 49(2):302-307.
Xie QD, He LY, Wang Q, et al.Isolation and identification of a feldspar-dissolving Bacillus strain and its biological characteristics[J]. Soil, 2017, 49(2):302-307.