Abstract
The control of pyrimidine nucleotide formation in the bacterium Pseudomonas aurantiaca ATCC 33663 by pyrimidines was studied. The activities of the pyrimidine biosynthetic pathway enzymes were investigated in P. aurantiaca ATCC 33663 cells and from cells of an auxotroph lacking orotate phosphoribosyltransferase activity under selected culture conditions. All activities of the pyrimidine biosynthetic pathway enzymes in ATCC 33663 cells were depressed by uracil addition to the minimal medium when succinate served as the carbon source. In contrast, all pyrimidine biosynthetic pathway enzyme activities in ATCC 33663 cells were depressed by orotic acid supplementation to the minimal medium when glucose served as the carbon source. The orotidine 5′-monophosphate decarboxylase activity in the phosphoribosyltransferase mutant strain increased by more than sixfold in succinate-grown cells and by more than 16-fold in glucose-grown cells after pyrimidine limitation showing possible repression of the decarboxylase by a pyrimidine-related compound. Inhibition by ATP, GTP, UTP and pyrophosphate of the in vitro activity of aspartate transcarbamoylase in ATCC 33663 was observed. The findings demonstrated control at the level of pyrimidine biosynthetic enzyme synthesis and activity for the P. aurantiaca transcarbamoylase. The control of pyrimidine synthesis in P. aurantiaca seemed to differ from what has been observed previously for the regulation of pyrimidine biosynthesis in related Pseudomonas species. This investigation could prove helpful to future work studying pseudomonad taxonomic analysis as well as to those exploring antifungal and antimicrobial agents produced by P. aurantiaca.
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References
Anzai Y, Kim H, Park J-Y, Wakabayashi H, Oyaizu H (2000) Phytogenetic affiliation of the pseudomonads based on 16S rRNA sequence. Int J Syst Evol Microbiol 50:1563–1589. https://doi.org/10.1099/00207713-50-4-1563
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of dye-binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Carlier E, Rovera M, Jaume AR, Rosas SB (2008) Improvement of growth, under field conditions, of wheat inoculated with Pseudomonas chlororaphis subsp. aurantiaca SR1. World J Microbiol Biotechnol 24:2653–2658. https://doi.org/10.1007/s11274-008-9791-6
Chin AWTF, van den Broek D, Lugtenberg BJ, Bloemberg GV (2005) The Pseudomonas chlororaphis PCL1391 sigma regulator psrA represses the production of the antifungal metabolite phenazine-1-carboxamide. Mol Plant Microbe Interact 18:244–253. https://doi.org/10.1094/MPMI.2001.14.8.969
Chunduru J, West TP (2018) Pyrimidine nucleotide synthesis in the emerging pathogen Pseudomonas monteilii. Can J Microbiol 64:432–438. https://doi.org/10.1139/cjm-2018-0015
Esipov SE, Adanin VM, Baskunov BP, Kiprianova EA, Garagulia AD (1975) New antibiotically active fluoroglucide from Pseudomonas aurantiaca. Antibiotiki 20:1077–1081 (PMID: 1225181)
Fang R, Jia L, Yao SS, Wang YJ, Wang J, Zhou CH, Wang HJ, Xiao M (2013) Promotion of plant growth, biological control and induced systemic resistance in maize by Pseudomonas aurantiaca JD37. Ann Microbiol 63:1177–1185. https://doi.org/10.1007/s13213-012-0576-7
Feklistova IN, Maksimova NP (2008) Obtaining Pseudomonas aurantiaca strains capable of overproduction of phenazine antibiotics. Microbiology 77:176–180. https://doi.org/10.1134/S0026261708020094
Felker P, Medina D, Soulier C, Velicce G, Velarde M, Gonzalez C (2005) A survey of environmental and biological factors (Azospirillum spp, Agrobacterium rhizogenes, Pseudomonas aurantiaca) for their influence in rooting cuttings of Prosopis alba clones. J Arid Environ 61:227–247. https://doi.org/10.1016/j.jaridenv.2004.09.010
Haas D, Keel C (2003) Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu Rev Phytopathol 41:117–153. https://doi.org/10.1146/annurev.phyto.41.052002.095656
Jiao Z, Wu N, Hale L, Wu W, Wu D, Guo Y (2013) Characterisation of Pseudomonas chlororaphis subsp. aurantiaca strain Pa40 with the ability to control wheat sharp eyespot disease. Ann Appl Biol 163:444–453. https://doi.org/10.1111/aab.12068
Mandryk MN, Kolomiets EI, Dey ES (2007) Characterization of antimicrobial compounds produced by Pseudomonas aurantiaca S-1. Polish J Microbiol 56:245–250
Mehnaz S, Baig DN, Jamil F, Weselowski B, Lazarovits G (2009) Characterization of a phenazine and hexanoyl homoserine lactone producing Pseudomonas aurantiaca strain PB-St2, isolated from sugarcane stem. J Microbiol Biotechnol 19:1688–1694. https://doi.org/10.4014/jmb.0904.04022
Mehnaz S, Baig DN, Lazarovits G (2010) Genetic and phenotypic diversity of plant growth promoting rhizobacteria isolated from sugarcane plants growing in Pakistan. J Microbiol Biotechnol 20:1614–1623. https://doi.org/10.4014/jmb.1005.05014
Mehnaz S, Saleem RS, Yameen B, Pianet I, Schnakenburg G, Pietraszkiewicz H, Valeriote F, Josten M, Sahl HG, Franzblau SG, Gross H (2013) Lahorenoic acids A-C, ortho-dialkyl-substituted aromatic acids from the biocontrol strain Pseudomonas aurantiaca PB-St2. J Nat Prod 76:135–141. https://doi.org/10.1021/np3005166
Morohoshi T, Wang WZ, Suto T, Saito Y, Ito S, Someya N, Ikeda T (2013) Phenazine antibiotic production and antifungal activity are regulated by multiple quorum-sensing systems in Pseudomonas chlororaphis subsp. aurantiaca StFRB508. J Biosci Bioeng 116:580–584. https://doi.org/10.1016/j.jbiosc.2013.04.022
O’Donovan GA, Neuhard J (1970) Pyrimidine metabolism in microorganisms. Bacteriol Rev 34:278–343 (PMID: 4919542)
Park JY, Oh SA, Anderson AJ, Neiswender J, Kim JC, Kim YC (2011) Production of the antifungal compounds phenazine and pyrrolnitrin from Pseudomonas chlororaphis O6 is differentially regulated by glucose. Lett Appl Microbiol 52:532–537. https://doi.org/10.1111/j.1472-765X.2011.03036.x
Peix A, Valverde A, Rivas R, Igual JM, Ramírez-Bahena M-H, Mateos PF, Santa-Regina I, Rodríguez-Barrueco C, Martínez-Molina E, Velázquez E (2007) Reclassification of Pseudomonas aurantiaca as a synonym of Pseudomonas chlororaphis and proposal of three subspecies, P. chlororaphis subsp. chlororaphis subsp. nov., P. chlororaphis subsp. aureofaciens subsp. nov., comb. nov. and P. chlororaphis subsp. aurantiaca subsp. nov., comb. nov. Int J Syst Evol Microbiol 57:1286–1290. https://doi.org/10.1099/ijs.0.64621-0
Price-Whelan A, Dietrich LE, Newman DK (2006) Rethinking 'secondary' metabolism: physiological roles for phenazine antibiotics. Nat Chem Biol 2:71–78. https://doi.org/10.1038/nchembio764
Rosas SB, Avanzini G, Carlier E, Pasluosta C, Pastor N, Rovera M (2009) Root colonization and growth promotion of wheat and maize by Pseudomonas aurantiaca SR1. Soil Biol Biochem 41:1802–1806. https://doi.org/10.1016/j.soilbio.2008.10.009
Rovera M, Pastor N, Niederhauser M, Rosas SB (2014) Evaluation of Pseudomonas chlororaphis subsp. aurantiaca SR1 for growth promotion of soybean and for control of Macrophomina phaseolina. Biocontrol Sci Technol 24:1012–1025. https://doi.org/10.1080/09583157.2014.910293
Santiago MF, West TP (2002) Regulation of pyrimidine synthesis in Pseudomonas mendocina. J Basic Microbiol 42:75–79. https://doi.org/10.1002/1521-4028(200203)42:1%3c75:AID-JOBM75%3e3.0.CO;2-W
Watson JM, Holloway BW (1976) Suppressor mutations in Pseudomonas aeruginosa. J Bacteriol 125:780–786 (PMID: 815247)
West TP (2002) Control of pyrimidine synthesis in Pseudomonas fragi. Lett Appl Microbiol 35:380–384. https://doi.org/10.1046/j.1472-765x.2002.01203.x
West TP (2004) Regulation of pyrimidine nucleotide formation in Pseudomonas taetrolens ATCC 4683. Microbiol Res 159:29–33. https://doi.org/10.1016/j.micres.2004.01.007
West TP (2009) Regulation of pyrimidine formation in Pseudomonas lundensis. Can J Microbiol 55:261–268. https://doi.org/10.1139/w08-137
West TP, Herlick SA, O'Donovan GA (1983) Inverse relationship between thymidylate synthetase and cytidine triphosphate synthetase activities during pyrimidine limitation in Salmonella typhimurium. FEMS Microbiol Lett 18:275–278. https://doi.org/10.1111/j.1574-6968.1983.tb00491.x
Acknowledgements
This work was funded by the Robert A. Welch Foundation Departmental Grant T-0014. Thanks to Layne C. Stanush for his technical assistance during his National Science Foundation REU 2016 Summer Fellowship and his funding by NSF REU Grant CHE-1263094.
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Domakonda, A., West, T.P. Control of pyrimidine nucleotide formation in Pseudomonas aurantiaca. Arch Microbiol 202, 1551–1557 (2020). https://doi.org/10.1007/s00203-020-01842-x
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DOI: https://doi.org/10.1007/s00203-020-01842-x