根瘤菌铁转运代谢及其调控机制研究进展

doi:10.13560/j.cnki.biotech.bull.1985.2019-0767

摘要/Abstract

摘要： 根瘤菌是一类可以与豆科植物高效共生固氮的兼性共生细菌,在全球氮循环及绿色可持续农业中发挥重要作用。为了适应土壤、根圈和宿主体内等多变的生活环境,根瘤菌对营养物质的感知和获取能力至关重要。铁不仅是根瘤菌在土壤中生长繁殖的限制性营养元素,更直接参与固氮酶、豆血红蛋白、电子呼吸链等与共生固氮密切相关功能蛋白的合成。因此,根瘤菌在自生和共生阶段如何获取自身所需的铁是生物固氮领域所特别关注的重要研究内容。综述了近年来有关根瘤菌中Fe²⁺、Fe³⁺-铁载体复合物、血红素吸收途径以及RirA/Irr等参与铁稳态调控方面的研究进展并进行归纳分析,以期为后续的研究工作提供借鉴。

关键词: 根瘤菌, 铁吸收, 铁载体, 血红素, 铁稳态

Abstract: Rhizobia are a collection of facultative symbiotic bacteria that possess the ability to establish symbiotic associations with legume hosts and carry out nitrogen fixation. Hence,they play important roles in the global nitrogen cycle and green sustainable agriculture. In order to adapt to the changing living environment such as soil,rhizosphere and infected host cells,it is vital for rhizobia to develop powerful strategies to sense and acquire nutrients. Iron is not only a limiting nutrient element for rhizobial growth and reproduction in the soil,but also directly involved in the synthesis of functional proteins closely related to symbiotic nitrogen fixation,such as nitrogenase,leghemoglobin and electronic respiratory chain components. Therefore,how rhizobia obtain iron under free-living and symbiotic conditions is highly concerned by scientists in the field of biological nitrogen fixation. Here we review recent researches on the uptake pathways of iron in different types such as Fe²⁺,Fe³⁺-siderophore complex,and heme and summarize regulation mechanisms of iron homeostasis mediated by RirA,Irr and other regulators in rhizobia,aiming to provide reference and insight for subsequent intensive researches.

Key words: rhizobia, iron uptake, siderophore, heme, iron homeostasis

焦健, 刘克寒, 田长富. 根瘤菌铁转运代谢及其调控机制研究进展[J]. 生物技术通报, 2019, 35(10): 7-17.

JIAO Jian, LIU Ke-han, TIAN Chang-fu. Advances in Mechanisms and Regulation of Iron Uptake and Metabolism in Rhizobia[J]. Biotechnology Bulletin, 2019, 35(10): 7-17.

参考文献

[1] Ratledge C, Dover LG.Iron metabolism in pathogenic bacteria[J]. Annual Reviews in Microbiology, 2000, 54(1):881-941.
[2] Oldroyd GE, Murray JD, Poole PS, et al.The rules of engagement in the legume-rhizobial symbiosis[J]. Annual Review of Genetics, 2011, 45:119-144.
[3] Brear EM, Day DA, Smith PM.Iron:an essential micronutrient for the legume-rhizobium symbiosis[J]. Frontiers in Plant Science, 2013, 4:359.
[4] Dixon R, Kahn D.Genetic regulation of biological nitrogen fixation[J]. Nat Rev Microbiol, 2004, 2(8):621-631.
[5] Verma D, Nadler KD.The Rhizobium-legume symbiosis:the host’s point of view[M]. Plant gene research:genes involved in microbe-plant interactions. Berlin:Springer-Verlag, 1984.
[6] O’Hara GW, Dilworth MJ, Boonkerd N, et al. Iron-deficiency specifically limits nodule development in peanut inoculated with Bradyrhizobium sp.[J]. New Phytologist, 1988, 108(1):51-57.
[7] Tang C, Robson AD, Dilworth MJ.The role of iron in nodulation and nitrogen fixation in Lupinus angustifolius L[J]. New Phytologist, 1990, 114(2):173-182.
[8] Battistoni F, Platero R, Noya F, et al.Intracellular Fe content influences nodulation competitiveness of Sinorhizobium meliloti strains as inocula of alfalfa[J]. Soil Biology and Biochemistry, 2002, 34(5):593-597.
[9] Shamseldin A, Abdelkhalek A, Sadowsky MJ.Recent changes to the classification of symbiotic, nitrogen-fixing, legume-associating bacteria:a review[J]. Symbiosis, 2017, 71(2):91-109.
[10] Masson-Boivin C, Giraud E, Perret X, et al.Establishing nitrogen-fixing symbiosis with legumes:how many rhizobium recipes?[J]. Trends in Microbiology, 2009, 17(10):458-466.
[11] Tian CF, Zhou YJ, Zhang YM, et al.Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations[J]. Proceedings of the National Academy of Sciences, 2012, 109(22):8629-8634.
[12] Turner SL, Young JPW.The glutamine synthetases of rhizobia:phylogenetics and evolutionary implications[J]. Molecular Biology and Evolution, 2000, 17(2):309-319.
[13] Curatti L, Rubio LM.Challenges to develop nitrogen-fixing cereals by direct nif-gene transfer[J]. Plant Science, 2014, 225:130-137.
[14] Manyani H, Rey L, Palacios JM, et al.Gene products of the hupGHIJ operon are involved in maturation of the iron-sulfur subunit of the[NiFe]hydrogenase from Rhizobium leguminosarum bv. viciae[J]. J Bacteriol, 2005, 187(20):7018-7026.
[15] Cecilia B, Belén B, Juan I, et al.Diversity and evolution of hydrogenase systems in rhizobia[J]. Applied & Environmental Microbiology, 2002, 68(10):4915-4924.
[16] Ratledge C, Dover LG.Iron metabolism in pathogenic bacteria[J]. Annual Reviews in Microbiology, 2000, 54(1):881-941.
[17] Raymond KN, Dertz EA.Biochemical and physical properties of siderophores[M]. Iron Transport in Bacteria. Washington DC:ASM Press, 2004.
[18] Challis GL.A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases[J]. Chembiochem, 2005, 8(13):601-611.
[19] Donadio S, Monciardini P, Sosio M.Polyketide synthases and nonribosomal peptide synthetases:the emerging view from bacterial genomics[J]. Natural Product Reports, 2007, 24(5):1073-1109.
[20] Persmark M, Pittman P, Buyer JS, et al.Isolation and structure of rhizobactin 1021, a siderophore from the alfalfa symbiont Rhizobium meliloti 1021[J]. Cheminform, 1993, 24(39):3950-3956.
[21] Dilworth MJ, Carson KC, Giles RGF, et al.Rhizobium leguminosarum bv. viciae produces a novel cyclic trihydroxamate siderophore, vicibactin[J]. Microbiology, 1998, 144(3):781-791.
[22] Smith MJ, Shoolery JN, Schwyn B, et al.Rhizobactin, a structurally novel siderophore from Rhizobium meliloti[J]. Journal of the American Chemical Society, 1985, 107(6):1739-1743.
[23] Modi M, Shah KS, Modi VV.Isolation and characterisation of catechol-like siderophore from cowpea Rhizobium RA-1[J]. Archives of Microbiology, 1985, 141(2):156-158.
[24] Patel HN, Chakraborty RN, Desai S B.Isolation and partial characterization of phenolate siderophore from Rhizobium leguminosarum IARI 102[J]. FEMS Microbiology Letters, 2010, 56(2):131-134.
[25] Carter RA, Worsley PS, Sawers G, et al.The vbs genes that direct synthesis of the siderophore vicibactin in Rhizobium leguminosarum:their expression in other genera requires ECF sigma factor RpoI[J]. Molecular Microbiology, 2002, 44(5):1153-1166.
[26] Lynch D, O’Brien J, Welch T, et al. Genetic organization of the region encoding regulation, biosynthesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti[J]. J Bacteriol, 2001, 183(8):2576.
[27] Pfleger BF, Lee JY, Somu RV, et al.Characterization and analysis of early enzymes for petrobactin biosynthesis in Bacillus anthracis[J]. Biochemistry, 2007, 46(13):4147-4157.
[28] Postle K, Larsen RA.TonB-dependent energy transduction between outer and cytoplasmic membranes[J]. Biometals, 2007, 20(3-4):453-465.
[29] Noinaj N, Guillier M, Barnard TJ, et al.TonB-dependent transporters:regulation, structure, and function[J]. Annual Review of Microbiology, 2010, 64:43-60.
[30] Chatterjee A, O’Brian MR. Rapid evolution of a bacterial iron acquisition system[J]. Molecular Microbiology, 2018, 108(1):90-100.
[31] Vojtech S, Spanning RJMV, Igor K.Ferric reductase A is essential for effective iron acquisition in Paracoccus denitrificans[J]. Microbiology, 2009, 155(4):1294-1301.
[32] Wang S, Wu Y, Outten FW.Fur and the novel regulator YqjI control transcription of the ferric reductase gene yqjH in Escherichia coli[J]. J Bacteriol, 2011, 193(2):563-574.
[33] Matzanke BF, Stefan A, Volker S, et al.FhuF, part of a siderophore-reductase system[J]. Biochemistry, 2004, 43(5):1386.
[34] Small SK, O’Brian MR. The Bradyrhizobium japonicum frcB gene encodes a diheme ferric reductase[J]. J Bacteriol, 2011, 193(16):4088-4094.
[35] Mckie A.The role of Dcytb in iron metabolism:an update[J]. Biochem Soc Trans, 2008, 36(6):1239-1241.
[36] Noya F, Arias A, Fabiano E.Heme compounds as iron sources for nonpathogenic Rhizobium bacteria[J]. J Bacteriol, 1997, 179(9):3076-3078.
[37] Nienaber A, Hennecke H, Fischer HM.Discovery of a haem uptake system in the soil bacterium Bradyrhizobium japonicum[J]. Molecular Microbiology, 2001, 41(4):787-800.
[38] Wexler M, Yeoman KH, Stevens JB, et al.The Rhizobium leguminosarum tonB gene is required for the uptake of siderophore and haem as sources of iron[J]. Molecular Microbiology, 2001, 41(4):801-816.
[39] Battistoni F, Platero R, Duran R, et al.Identification of an iron-regulated, hemin-binding outer membrane protein in Sinorhizobium meliloti[J]. Applied and Environmental Microbiology, 2002, 68(12):5877-5881.
[40] Vanesa A, O’Brian MR, Elena F. ShmR is essential for utilization of heme as a nutritional iron source in Sinorhizobium meliloti[J]. Applied & Environmental Microbiology, 2008, 74(20):6473-6475.
[41] Expert D, O’Brian MR. Molecular aspects of iron metabolism in pathogenic and symbiotic plant-microbe associations[M]. Springerbriefs in Molecular Science, 2012.
[42] Sumant P, O’Brian MR. The hmuQ and hmuD genes from Bradyrhizobium japonicum encode heme-degrading enzymes[J]. J Bacteriol, 2006, 188(18):6476.
[43] Hantke K.Is the bacterial ferrous iron transporter FeoB a living fossil?[J]. Trends in microbiology, 2003, 11(5):192-195.
[44] Sankari S, O’Brian MR. The Bradyrhizobium japonicum ferrous iron transporter FeoAB is required for ferric iron utilization in free-living aerobic cells and for symbiosis[J]. Journal of Biological Chemistry, 2016, 291(30):15653.
[45] Mourad S, Simon L, Dozois CM.A SitABCD homologue from an avian pathogenic Escherichia coli strain mediates transport of iron and manganese and resistance to hydrogen peroxide[J]. Microbiology, 2006, 152(3):745-758.
[46] Davies BW, Walker GC.Disruption of sitA compromises Sinorhi-zobium meliloti for manganese uptake required for protection aga-inst oxidative stress[J]. J Bacteriol, 2007, 189(5):2101-2109.
[47] Slatni T, Krouma A, Aydi S, et al.Growth, nitrogen fixation and ammonium assimilation in common bean(Phaseolus vulgaris L)subjected to iron deficiency[J]. Plant and Soil, 2008, 312(1-2):49-57.
[48] Moreau S, Meyer J, Puppo A.Uptake of iron by symbiosomes and bacteroids from soybean nodules[J]. FEBS Letters, 1995, 361(2-3):225-228.
[49] Levier K, Day DA, Guerinot ML.Iron uptake by symbiosomes from soybean root nodules[J]. Plant Physiology, 1996, 111(3):893-900.
[50] Kaiser BN, Moreau S, Castelli J, et al.The soybean NRAMP homologue, GmDMT1, is a symbiotic divalent metal transporter capable of ferrous iron transport[J]. The Plant Journal, 2003, 35(3):295-304.
[51] Pierre O, Engler G, Hopkins J, et al.Peribacteroid space acidification:a marker of mature bacteroid functioning in Medicago truncatula nodules[J]. Plant, Cell & Environment, 2013, 36(11):2059-2070.
[52] Gill Jr PR, Neilands JB.Cloning a genomic region required for a high-affinity iron-uptake system in Rhizobium meliloti 1021[J]. Molecular Microbiology, 1989, 3(9):1183-1189.
[53] Fabiano E, Gill PR, Noya F, et al.Siderophore-mediated iron acquisition mutants in Rhizobium meliloti 242 and its effect on the nodulation kinetic of alfalfa nodules[J]. Symbiosis, 1995, 19:197-211.
[54] Cuív PÓ, Keogh D, Clarke P, et al.The hmuUV genes of Sinorhizobium meliloti 2011 encode the permease and ATPase components of an ABC transport system for the utilization of both haem and the hydroxamate siderophores, ferrichrome and ferrioxamine B[J]. Molecular Microbiology, 2008, 70(5):1261-1273.
[55] Chao T, Becker A, Buhrmester J, et al.The Sinorhizobium meliloti fur gene regulates, with dependence on Mn(II), transcription of the sitABCD operon, encoding a metal-type transporter[J]. J Bacteriol, 2004, 186(11):3609-3620.
[56] Crespo-Rivas JC, Navarro-Gómez P, Alias-Villegas C, et al.Sinorhizobium fredii HH103 RirA is required for oxidative stress resistance and efficient symbiosis with soybean[J]. International Journal of Molecular Sciences, 2019, 20(3):787.
[57] Papanikolaou G, Pantopoulos K.Iron metabolism and toxicity[J]. Toxicology and Applied Pharmacology, 2005, 202(2):199-211.
[58] Johnston AW, Todd JD, Curson AR, et al.Living without Fur:the subtlety and complexity of iron-responsive gene regulation in the symbiotic bacterium Rhizobium and other α-proteobacteria[J]. Biometals, 2007, 20(3-4):501-511.
[59] Rodionov DA, Gelfand MS, Todd JD, et al.Computational reconstruction of iron-and manganese-responsive transcriptional networks in α-proteobacteria[J]. PLoS Comput Biol, 2006, 2(12):e163.
[60] Hamza I, Chauhan S, Hassett R, et al.The bacterial Irr protein is required for coordination of heme biosynthesis with iron availability[J]. Journal of Biological Chemistry, 1998, 273(34):21669.
[61] O’Brian MR. Perception and homeostatic control of iron in the Rhizobia and related bacteria[J]. Annual Review of Microbiology, 2015, 69:229-245.
[62] Jianhua Y, Indu S, Andrea L, et al.Bradyrhizobium japonicum senses iron through the status of haem to regulate iron homeostasis and metabolism[J]. Molecular Microbiology, 2010, 60(2):427-437.
[63] Todd JD, Sawers G, Rodionov DA, et al.The Rhizobium leguminosarum regulator IrrA affects the transcription of a wide range of genes in response to Fe availability[J]. Molecular Genetics & Genomics, 2006, 275(6):564-577.
[64] Rudolph G, Semini G, Hauser F, et al.The Iron control element, acting in positive and negative control of iron-regulated Bradyrhizobium japonicum genes, is a target for the Irr protein[J]. J Bacteriol, 2006, 188(2):733.
[65] Small SK, Puri SI, O’Brian MR. Positive control of ferric siderophore receptor gene expression by the Irr protein in Bradyrhizobium japonicum[J]. J Bacteriol, 2009, 191(5):1361-1368.
[66] Gesine R, Geo S, Felix H, et al.The Iron control element, acting in positive and negative control of iron-regulated Bradyrhizobium japonicum genes, is a target for the Irr protein[J]. J Bacteriol, 2006, 188(2):733.
[67] Qi Z, Hamza I, O’Brian MR. Heme is an effector molecule for iron-dependent degradation of the bacterial iron response regulator(Irr)protein[J]. Proceedings of the National Academy of Sciences of the United States of America, 1999, 96(23):13056-13061.
[68] Jianhua Y, Koichiro I, O’Brian MR. Two heme binding sites are involved in the regulated degradation of the bacterial iron response regulator(Irr)protein[J]. Journal of Biological Chemistry, 2005, 280(9):7671-7676.
[69] Ishikawa H, Nakagaki M, Ai B, et al.Unusual heme binding in the bacterial iron response regulator protein(Irr):spectral characterization of heme binding to heme regulatory motif[J]. Biochemistry, 2011, 50(6):1016-1022.
[70] Chloe S, White GF, Todd JD, et al.Heme-responsive DNA binding by the global iron regulator Irr from Rhizobium leguminosarum[J]. Journal of Biological Chemistry, 2010, 285(21):16023-16031.
[71] Todd JD, Wexler M, Sawers G, et al.RirA, an iron-responsive reg-ulator in the symbiotic bacterium Rhizobium leguminosarum[J]. Microbiology, 2002, 148(12):4059-4071.
[72] Yeoman KH, Curson AR, Todd JD, et al.Evidence that the Rhizobium regulatory protein RirA binds to cis-acting iron-responsive operators(IROs)at promoters of some Fe-regulated genes[J]. Microbiology, 2004, 150(12):4065-4074.
[73] Chao T, Buhrmester J, Hansmeier N, et al.Role of the regulatory gene rirA in the transcriptional response of Sinorhizobium meliloti to iron limitation[J]. Applied and Environmental Microbiology, 2005, 71(10):5969-5982.
[74] Battisti JM, Smitherman LS, Sappington KN, et al.Transcriptional regulation of the heme binding protein gene family of Bartonella quintana is accomplished by a novel promoter element and iron response regulator[J]. Infection & Immunity, 2007, 75(9):4373-4385.
[75] Ngok-Ngam P, Ruangkiattikul N, Mahavihakanont A, et al.Roles of Agrobacterium tumefaciens RirA in iron regulation, oxidative stress response, and virulence[J]. J Bacteriol, 2009, 191(7):2083-2090.
[76] Viguier C, Cuív PÓ, Clarke P, et al.RirA is the iron response regulator of the rhizobactin 1021 biosynthesis and transport genes in Sinorhizobium meliloti 2011[J]. FEMS Microbiology Letters, 2005, 246(2):235-242.
[77] Martinez MTP, Martinez AB, Crack JC, et al.Sensing iron availa- bility via the fragile[4Fe-4S]cluster of the bacterial transcrip-tional repressor RirA[J]. Chemical Science, 2017, 8(12):8451-8463.
[78] Costa D, Amarelle V, Valverde C, et al.The Irr and RirA proteins participate in a complex regulatory circuit and act in concert to modulate bacterioferritin expression in Ensifer meliloti 1021[J]. Applied & Environmental Microbiology, 2017, 83(16):817-895.
[79] Amarelle V, Koziol U, Rosconi F, et al.A new small regulatory protein, HmuP, modulates haemin acquisition in Sinorhizobium meliloti[J]. Microbiology, 2010, 156(6):1873-1882.
[80] Rosalba EH, O’Brian MR. HmuP is a coactivator of Irr-dependent expression of heme utilization genes in Bradyrhizobium japonicum[J]. J Bacteriol, 2012, 194(12):3137-3143.
[81] ó Cuív P, Clarke P, Lynch D, et al. Identification of rhtX and fptX, novel genes encoding proteins that show homology and function in the utilization of the siderophores rhizobactin 1021 by Sinorhizobium meliloti and pyochelin by Pseudomonas aeruginosa, Respectively[J]. J Bacteriol, 2004, 186(10):2996.