Research Progress in Chemical Structure, Biosynthesis, Regulation and Applications of Pseudomonas Metabolite Pyoluteorin

doi:10.16409/j.cnki.2095-039x.2021.01.028

Abstract

Abstract: Pyoluteorin (Plt) is one of the secondary metabolites produced by Pseudomonas spp. and has a broad spectrum of antibiotic activity. In this review, Plt producing strains, chemical structure, biosynthesis and regulatory mechanisms were introduced. The strategies and achievements in constructing high Plt yield strains were then summarized. Finally, the potential of Plt as a new metabolite biopesticide and future work in this field were discussed and prospected.

Key words: Pseudomonas, pyoluteorin, biosynthesis, regulatory network, metabolite biopesticide

CLC Number:

S476

CUI Ying, SONG Kai, HE Yawen. Research Progress in Chemical Structure, Biosynthesis, Regulation and Applications of Pseudomonas Metabolite Pyoluteorin[J]. Chinese Journal of Biological Control, 2021, 37(1): 52-59.

References

[1] Silby M W, Winstanley C, Godfrey S A, et al. Pseudomonas genomes:diverse and adaptable[J]. FEMS Microbiology Reviews, 2011, 35(4):652-680.
[2] Ramette A, Frapolli M, Saux M F, et al. Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2,4-diacetylphloroglucinol and pyoluteorin.[J]. Systematic and Applied Microbiology, 2011, 34(3):180-188.
[3] 蒋海霞, 周莲, 何亚文. 铜绿假单胞菌生防菌株抑菌代谢产物及其生防应用研究进展[J]. 微生物学通报, 2015(7):145-156.
[4] Gross H, Loper J E. Genomics of secondary metabolite production by Pseudomonas spp.[J]. Natural Products Report, 2009, 26(11):1408-1446.
[5] Keswani C, Singh H B, Hermosa R, et al. Antimicrobial secondary metabolites from agriculturally important fungi as next biocontrol agents[J]. Applied Microbiology and Biotechnology, 2019, 103:1-10.
[6] Takeda R. Pseudomonas pigments:I. Pyoluterin, a new chlorinecontaining pigment produced by Pseudomonas aeruginosa[J]. Hako Kogaku Zasshi, 1958, 36:281-90.
[7] Vinay J U, Naik M K, Rangeshwaran R, et al. Detection of antimicrobial traits in fluorescent pseudomonads and molecular characterization of an antibiotic pyoluteorin[J]. Biotechonoly, 2016, 6(2):227.
[8] Cascioferro S, Raimondi M V, Cusimano M G, et al. Pharmaceutical potential of synthetic and natural pyrrolomycins[J]. Molecules, 2015, 20(12):21658-21658.
[9] Lacerna N M, Miller B W, Lim A L, et al. Mindapyrroles A-C, pyoluteorin analogues from a shipworm-associated bacterium[J]. Journal of Natural Products, 2019, 82(4):1024-1028.
[10] Ohmori T, Hagiwara S I, Minoda Y, et al. Production of pyoluteorinand its derivatives from n-paraffin by Pseudomonas aeruginosa S10B2[J]. Agricultural Biology Chemistry, 1978, 42:2031-2036.
[11] Bakthavatchalu S, Shivakumar S, Sullia S B, et al. Molecular detection of antibiotic related genes from Pseudomonas aeruginosa FP6, an antagonist towards Rhizoctonia solani and Colletotrichum gloeosporioides[J]. Turkish Journal of Biology, 2013, 37(3):289-295.
[12] Hu H B, Xu Y Q, Zhang X H, et al. Isolation and characterization of a new fluorescent Pseudomonas strain that produces both phenazine 1-carboxylic acid and pyoluteorin[J]. Journal of Microbiology and Biotechnology, 2005,15(1):86-90.
[13] 崔莹, 金子靖, 何亚文. 碳源影响水稻根际假单胞菌PA1201藤黄绿菌素的生物合成[J]. 微生物学通报, 2020, 47(8):2399-2408.
[14] Howell C R, Stipanovic R D. Suppression of Pythium ultimum-induced damping-off of cotton seedlings by Pseudomonas fluorescens and its antibiotic, pyoluteorin[J]. Phytopathology, 1980, 70:712-715.
[15] Maurhofer M, Keel C, Défago G, et al. Pyoluteorin production by Pseudomonas fluorescens strain CHA0 is involved in the suppression of Pythium damping-off of cress but not cucumber[J]. European Journal of Plant Pathology, 1994, 100:221-232.
[16] Yuan Z, Cang S, Matsufuji M, et al. High production of pyoluteorin and 2,4-diacetylphloroglucinol by Pseudomonas fluorescens S272 grown on ethanol as a sole carbon source[J]. Journal of Fermentation and Bioengineering, 1998, 86(6):559-563.
[17] de La Fuente L, Thomashow L, Weller D, et al. Pseudomonas Fluorescens UP61 isolated from birdsfoot trefoil rhizosphere produces multiple antibiotics and exerts a broad spectrum of biocontrol activity[J]. European Journal of Plant Pathology, 2004, 110(7):671-681.
[18] Matano I, Tsunekawa M, Shimizu S, et al. The chloride ion is an environmental factor affecting the biosynthesis of pyoluteorin and 2,4-Diacetylphloroglucinol in Pseudomonas sp. YGJ3[J]. Bioscience, Biotechnology and Biochemistry, 2010, 74(2):427-429.
[19] Zhang Q, Xiao Q, Xu J, et al. Effect of retS gene on antibiotics production in Pseudomonas fluorescens FD6[J]. Microbiological Research, 2015, 1:23-29.
[20] Saikia R, Sarma R K, Yadav A, et al. Genetic and functional diversity among the antagonistic potential fluorescent Pseudomonads isolated from tea rhizosphere[J]. Current Microbiology, 2011, 62(2):434-444.
[21] Salman M. Determination of antibiotic activity on plasmids from fluorescent Pseudomonads isolates CW2, WB15 and WB52 against pre-emergence damping-off caused by Pythium ultimum and Rhizoctonia solani in cucumber[J]. Biological Control, 2010, 53(2):161-167.
[22] Andreolli M, Zapparoli G, Angelini E, et al. Pseudomonas protegens MP12:A plant growth-promoting endophytic bacterium with broad-spectrum antifungal activity against grapevine phytopathogens[J]. Microbiological research, 2019, 219:123-131.
[23] Wang X, Mavrodi D V, Ke L, et al. Biocontrol and plant growth-promoting activity of rhizobacteria from Chinese fields with contaminated soils[J]. Microbial biotechnology, 2015, 8(3):404-418.
[24] Rai R, Srinivasamurthy R, Dash P K, et al. Isolation, characterization and evaluation of the biocontrol potential of Pseudomonas protegens RS-9 against Ralstonia solanacearum in Tomato[J]. Indian Journal of Experimental Biology, 2017, 55(9):595-603.
[25] Polano C, Martini M, Savian F, et al. Genome sequence and antifungal activity of two niche-sharing Pseudomonas protegens related strains isolated from hydroponics[J]. Microbial Ecology, 2019, 77(4):1025-1035.
[26] Huang X, Wang Z, Liu Y, et al. Complete genome sequence of Pseudomonas protegens H78, a plant growth-promoting rhizobacterium[J]. Genome Announcements, 2017, 5(16):e00233-17.
[27] Hassan M N, Afghan S, Hafeez F Y. Biological control of red rot in sugarcane by native pyoluteorin-producing Pseudomonas putida strain NH-50 under field conditions and its potential modes of action[J]. Pest Management Science, 2011, 67(9):1147-1154.
[28] Lu J, Huang X, Li K, et al. LysR family transcriptional regulator PqsR as repressor of pyoluteorin biosynthesis and activator of phenazine-1-carboxylic acid biosynthesis in Pseudomonas sp. M18[J]. Journal of BioTechnology, 2009, 143(1):1-9.
[29] Yan A, Wang X, Zhang X, et al. LysR family factor PltR positively regulates Pyoluteorin production in a pathway-specific manner in Pseudomonas sp. M18[J]. Science China-life Sciences, 2007, 50(4):518-524.
[30] Jaremko M J, Lee D J, Opella S J, et al. Structure and substrate sequestration in the pyoluteorin type Ⅱ peptidyl carrier protein PltL[J]. Journal of the American Chemical Society, 2015, 137(36):11546-11549.
[31] Dorrestein P C, Yeh E, Garneautsodikova S, et al. Dichlorination of a pyrrolyl-S-carrier protein by FADH₂-dependent halogenase PltA during pyoluteorin biosynthesis[J]. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(39):13843-13848.
[32] Pang A H, Garneautsodikova S, Tsodikov O V, et al. Crystal structure of halogenase PltA from the pyoluteorin biosynthetic pathway[J]. Journal of Structural Biology, 2015, 192(3):349-357.
[33] Li S, Huang X, Wang G, et al. Transcriptional activation of pyoluteorin operon mediated by the LysR-type regulator PltR bound at a 22 bp lys box in Pseudomonas aeruginosa M18[J]. PloS ONE, 2012, 7(6):e39538.
[34] Huang X, Zhu D, Ge Y, et al. Identification and characterization of pltZ, a gene involved in the repression of pyoluteorin biosynthesis in Pseudomonas sp. M18[J]. Fems Microbiology Letters, 2004, 232(2):197-202.
[35] 黄显清, 葛宜和, 张雪洪, 等. 假单胞菌M18株pltZ基因转录阻抑藤黄绿菌素ABC转运系统[J]. 微生物学报, 2005(3):344-348.
[36] Kidarsa T A, Goebel N C, Zabriskie T M, et al. Phloroglucinol mediates cross-talk between the pyoluteorin and 2,4-diacetylphloroglucinol biosynthetic pathways in Pseudomonas fluorescens Pf-5[J]. Molecular Microbiology, 2011, 81(2):395-414.
[37] Yan Q, Philmus B, Chang J H, et al. Novel mechanism of metabolic co-regulation coordinates the biosynthesis of secondary metabolites in Pseudomonas protegens[J]. eLife, 2017, 6:e22835.
[38] Mori S, Pang A H, Chandrika N T, et al. Unusual substrate and halide versatility of phenolic halogenase PltM[J]. Nature Communications, 2019, 10(1):1255-1255.
[39] Sun S, Zhou L, Jin K, et al. Quorum sensing systems differentially regulate the production of phenazine-1-carboxylic acid in the rhizobacterium Pseudomonas aeruginosa PA1201[J]. Scientific Reports, 2016, 6(1):30352-30352.
[40] Huang X, Zhang X, Xu Y, et al. PltR expression modulated by the global regulators GacA, RsmA, LasI and RhlI in Pseudomonas sp. M18[J]. Research in Microbiology, 2008, 159(2):128-136.
[41] 唐璐璐. 假单胞菌株M18中pqsA突变株的构建及其对plt的调控[J]. 微生物学通报, 2014, 41(10):2094-2099.
[42] Huang X, Zhang X, Xu Y, et al. Positive regulation of pyoluteorin biosynthesis in Pseudomonas sp. M18 by quorum-sensing regulator VqsR[J]. Journal of Microbiology and Biotechnology, 2008, 18(5):828-836.
[43] Kay E, Dubuis C, Haas D. Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0[J]. Proceedings of the National Academy of Sciences, 2005, 102(47):17136-17141.
[44] Humair B, Wackwitz B, Haas D, et al. GacA-Controlled activation of promoters for small RNA genes in Pseudomonas fluorescens[J]. Applied and Environmental Microbiology, 2010, 76(5):1497-1506.
[45] Wang Z, Huang X, Liu Y, et al. GacS/GacA activates pyoluteorin biosynthesis through Gac/Rsm-RsmE cascade and RsmA/RsmE-driven feedback loop in Pseudomonas protegens H78[J]. Molecular Microbiology, 2017, 105(6):968-985.
[46] 关业俊, 王正, 向涛, 等. 防御假单胞菌双突变体H78ΔrsmA/E中hmgA基因对藤黄绿菌素生物合成的抑制[J]. 微生物学通报, 2020, 47(8):2331-2337.
[47] Ge Y, Yang S, Fang Y, et al. RpoS as an intermediate in RsmA-dependent regulation of secondary antifungal metabolites biosynthesis in Pseudomonas sp. M18[J]. FEMS Microbiology Letters, 2007, 268(1):81-87.
[48] 朱栋华, 徐汪节, 耿海峰, 等. 荧光假单胞菌M18 rpoD克隆及其对抗生素合成的影响[J]. 微生物学报, 2003(3):315-323.
[49] Liu Y J, Shi H M, Wang Z, et al. Pleiotropic control of antibiotic biosynthesis, flagellar operon expression, biofilm formation, and carbon source utilization by RpoN in Pseudomonas protegens H78[J]. Applied Microbiology and Biotechnology, 2018, 102(22):9719-9730.
[50] Xie Y, Liu Z, Zhang G, et al. A rifampicin-resistant (rpoB) mutation in Pseudomonas protegens Pf-5 strain leads to improved antifungal activity and elevated production of secondary metabolites[J]. Research in Microbiology, 2016, 167(8):625-629.
[51] 王国昊. 假单胞菌株M18psrA突变株的构建及其对吩嗪-1-羧酸和藤黄绿菌素合成的调控[J]. 微生物学通报, 2012, 39(3):291-299.
[52] Zhang Q, Ji Y, Xiao Q, et al. Role of Vfr in the regulation of antifungal compound production by Pseudomonas fluorescens FD6[J]. Microbiological Research, 2016, (188-189):106-112.
[53] Wang G, Huang X, Li S, et al. The RNA chaperone Hfq regulates antibiotic biosynthesis in the rhizobacterium Pseudomonas aeruginosa M18[J]. Journal of Bacteriology, 2012, 194(10):2443-2457.
[54] Whistler C A, Stockwell V O, Loper J E. Lon protease influences antibiotic production and UV tolerance of Pseudomonas fluorescens Pf-5[J]. Applied and Environmental Microbiology, 2000, 66(7):2718-2725.
[55] 王正, 吴玲玉, 刘玉洁, 等. 假单胞菌H78中PhoR/B系统对磷元素吸收及其藤黄绿菌素合成的调控[J]. 微生物学通报, 2016, 43(9):1881-1886.
[56] Wu L, Wang Z, Guan Y, et al. The (p)ppGpp-mediated stringent response regulatory system globally inhibits primary metabolism and activates secondary metabolism in Pseudomonas protegens H78[J]. Applied Microbiology and Biotechnology, 2020, 104(7):3061-3079.
[57] Wu D, Ye J, Ou H, et al. Genomic analysis and temperature-dependent transcriptome profiles of the rhizosphere originating strain Pseudomonas aeruginosa M18[J]. BMC Genomics, 2011, 12(1):438-438.
[58] Duffy B K, Geneviève D. Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains[J]. Applied and Environmental Microbiology, 1999, 65(6):2429-2438.
[59] Brodhagen M, Henkels M D, Loper J E. Regulation of pyoluteorin production in Pseudomonas fluorescens Pf-5 includes positive autoregulation and repression by 2,4-diacetylphloroglucinol and pyrrolnitrin[J]. Phytopathology, 2003, 93:11.
[60] Brodhagen M, Henkels M D, Loper J E. Positive autoregulation and signaling properties of pyoluteorin, an antibiotic produced by the biological control organism Pseudomonas fluorescens Pf-5[J]. Applied and Environmental Microbiology, 2004, 70(3):1758-1766.
[61] 许煜泉. 制备基因工程菌株的方法及生产藤黄绿菌素的方法[P]. 中国发明专利, 2011, CN201010282431.3.
[62] Yan Q, Benjamin P, Cedar H, et al. The rare codon AGA is involved in regulation of pyoluteorin biosynthesis in Pseudomonas protegens Pf-5[J]. Frontiers in Microbiology, 2016, 7:497.
[63] Shi H, Huang X, Wang Z, et al. Improvement of pyoluteorin production in Pseudomonas protegens H78 through engineering its biosynthetic and regulatory pathways[J]. Applied Microbiology and Biotechnology, 2019, 103(8):3465-3476.
[64] Ding T, Yang L J, Zhang W D, et al. Pyoluteorin induces cell cycle arrest and apoptosis in human triple-negative breast cancer cells MDA-MB-231:Pyoluteorin induces cycle arrest and apoptosis[J]. Journal of Pharmacy and Pharmacology, 2020, 72(7):969-978.
[65] Zhang J, Wang W, Lu X, et al. The stability and degradation of a new biological pesticide, pyoluteorin[J]. Pest Management Science, 2010, 66(3):248-252.
[66] 董卉. 假单胞菌抗生素:吩嗪类化合物的检测与藤黄绿菌素的土壤残留分析[D]. 上海:上海交通大学, 2011.
[67] Chen J, Wang W, Xu Y, et al. Slow-release formulation of a new biological pesticide, pyoluteorin, with mesoporous silica[J]. Journal of Agricultural and Food Chemistry, 2011, 59(1):307-311.