Pseudomonas fluorescens SBW25 produces furanomycin, a non-proteinogenic amino acid with selective antimicrobial properties

BMC Microbiology

Gary Banowetz³  Mark Azevedo³  Donald Armstrong¹  Kerry McPhail²  Kristin Trippe³ 

[1] Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, 97331, USA;College of Pharmacy, Oregon State University, Corvallis, OR, 97331, USA;USDA-ARS National Forage Seed Production Research Center, Corvallis, OR, 97331, USA

关键词: Furanomycin;    4-formylaminooxyvinylglycine;    Antimicrobial activity;    Non-proteinogenic amino acids;    Secondary metabolites;    Pseudomonas fluorescens WH6;    Pseudomonas fluorescens SBW25;   

Others  :  1143716
DOI  :  10.1186/1471-2180-13-111

 received in 2012-12-24, accepted in 2013-05-07,  发布年份 2013

【 摘 要 】

Background

Pseudomonas fluorescens SBW25 has been extensively studied because of its plant growth promoting properties and potential as a biocontrol agent. The genome of SBW25 has been sequenced, and among sequenced strains of pseudomonads, SBW25 appears to be most closely related to P. fluorescens WH6. In the authors’ laboratories, WH6 was previously shown to produce and secrete 4-formylaminooxyvinylglycine (FVG), a non-proteinogenic amino acid with selective herbicidal and antimicrobial activity. Although SBW25 does not have the genetic capacity to produce FVG, we were interested in determining whether this pseudomonad might produce some other type of non-proteinogenic amino acid.

Results

P. fluorescens SBW25 was found to produce and secrete a ninhydrin-reactive compound with selective antimicrobial properties. This compound was purified from SBW25 culture filtrate and identified as the non-proteinogenic amino acid L-furanomycin [2S,2′R,5′S)-2-amino-2-(5′methyl-2′,5′-dihydrofuran-2′-yl)acetic acid].

Conclusions

The identification of furanomycin as a secondary metabolite of SBW25 is the first report of the production of furanomycin by a pseudomonad. This compound was known previously only as a natural product produced by a strain of Streptomyces. This report adds furanomycin to the small list of non-proteinogenic amino acids that have been identified as secondary products of pseudomonads. This study also extends the list of bacteria that are inhibited by furanomycin to include several plant pathogenic bacteria.

【 授权许可】

   
2013 Trippe et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Bossis E, Lemanceau P, Latour X, Gardan L: The taxonomy of Pseudomonas fluorescens and Pseudomonas putida: current status and need for revision. Agronomie 2000, 20:51-63.
• [2]Yamamoto S, Kasai H, Arnold DL, Jackson RW, Vivian A, Harayama S: Phylogeny of the genus Pseudomonas: intrageneric structure reconstructed from the nucleotide sequences of gyrB and rpoD genes. Microbiol 2000, 146:2385-2394.
• [3]Silby MW, Winstanley C, Godfrey SAC, Levy SB, Jackson RW: Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev 2011, 35:652-680.
• [4]Silby MW, Cerdñeo-Tárraga AM, Vernikos GS, Giddens SR, Jackson RW, Preston GM, Zhang X-X, Moon CD, Gehrig SM, Godfrey SAC, Knight CG, Malone JG, Robinson Z, Spiers AJ, Harris S, Challis GL, Yaxley AM, Harris D, Seeger K, Murphy L, Rutter S, Squares R, Quail MA, Saunders E, Mavromatis K, Brettin TS, Bentley SD, Hothersall J, Stephens E, Thomas CM, Parkhill J, Levy SB, Rainey PB, Thomson NR: Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol 2009, 10:R51. BioMed Central Full Text
• [5]Loper JE, Hassan KA, Mavrodi DV, Davis EW II, Lim CK, Shaffer BT, Elbourne LD, Stockwell VO, Hartney SL, Breakwell K, Henkels MD, Tetu SG, Rangel LI, Kidarsa TA, Wilson NL, van de Mortel JE, Song C, Blumhagen R, Radune D, Hostetler JB, Brinkac LM, Durkin AS, Kluepfel DA, Wechter WP, Anderson AJ, Kim YC, Pierson LS III, Pierson EA, Lindow SE, Kobayashi DY, Raaijmakers JM, Weller DM, Thomashow LS, Allen AE, Paulsen IT: Comparative genomics of plant-associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet 2012, 8(7):e1002784.
• [6]Gross H, Loper JE: Genomics of secondary metabolite production by Pseudomonas spp. Nat Prod Rep 2009, 26:1408-1446.
• [7]Lesinger T, Margraff R: Secondary metabolites of fluorescent pseudomonads. Microbiol Rev 1979, 43:422-442.
• [8]Elliott LF, Lynch JM: Plant growth-inhibitory pseudomonads colonizing winter wheat (Triticum aestivum L.) roots. Plant Soil 1985, 84:57-65.
• [9]Elliott LF, Azevedo MD, Mueller-Warrant GW, Horwath WR: Weed control with rhizobacteria. Soil Sci Agrochem Ecol 1998, 33:3-7.
• [10]Banowetz GM, Azevedo MD, Armstrong DJ, Halgren AB, Mills DI: Germination-Arrest Factor (GAF): biological properties of a novel, naturally-occurring herbicide produced by selected isolates of rhizosphere bacteria. Biol Control 2008, 46:380-390.
• [11]Armstrong D, Azevedo M, Mills D, Bailey B, Russell B, Groenig A, Halgren A, Banowetz G, McPhail K: Germination-Arrest Factor (GAF): 3. Determination that the herbicidal activity of GAF is associated with a ninhydrin-reactive compound and counteracted by selected amino acids. Biol Control 2009, 51:181-190.
• [12]McPhail KL, Armstrong DJ, Azevedo MD, Banowetz GM, Mills DI: 4-Formylaminooxyvinylglycine, an herbicidal germination-arrest factor from Pseudomonas rhizosphere bacteria. J Nat Prod 2010, 73:1853-1857.
• [13]Kimbrel JA, Givan SA, Halgren AB, Creason AL, Mills DI, Banowetz GM, Armstrong DJ, Chang JH: An improved, high-quality draft genome sequence of the Germination-Arrest Factor-producing Pseudomonas fluorescens WH6. BMC Genomics 2010, 11:522. BioMed Central Full Text
• [14]Halgren A, Maselko M, Azevedo M, Mills D, Armstrong D, Banowetz G: Genetics of germination-arrest factor (GAF) production by Pseudomonas fluorescens WH6: Identification of a gene cluster essential for GAF biosynthesis. Microbiol 2013, 159:36-45.
• [15]De Leij F, Sutton EJ, Whipps JM, Fenlon JS, Lynch JM: Impact of field release of genetically modified Pseudomonas fluorescens on indigenous microbial populations of wheat. Appl Environ Microbiol 1995, 61:3443-3453.
• [16]Rainey PB, Bailey MJ: Physical and genetic map of the Pseudomonas fluorescens SBW25 chromosome. Mol Microbiol 1996, 19:521-533.
• [17]Kassen R, Llewellyn M, Rainey PB: Ecological constraints on diversification in a model adaptive radiation. Nature 2004, 431:984-988.
• [18]Rainey PB, Rainey K: Evolution of cooperation and conflict in experimental bacterial populations. Nature 2003, 425:72-74.
• [19]Zhang X-X, Rainey PB: The role of a P1-type ATPase from Pseudomonas fluorescens SBW25 in copper homeostasis and plant colonization. Mol Plant Microbe Interact 2007, 20:581-588.
• [20]Giddens SR, Jackson RW, Moon CD, Jacobs MA, Zhang X-X, Gehrig SM, Rainey PB: Mutational activation of niche-specific genes provides insight into regulatory networks and bacterial function in a complex environment. Proc Nat Acad Sci 2007, 104:18247-18252.
• [21]Naseby DC, Way JA, Bainton NJ, Lynch JM: Biocontrol of Pythium in the pea rhizosphere by antifungal metabolite producing and non-producing Pseudomonas strains. J Appl Microbiol 2001, 90:421-429.
• [22]Moon CD, Zhang X-X, Matthijs S, Schäfer M, Budzikiewicz H, Rainey PB: Genomic, genetic and structural analysis of pyoverdine-mediated iron acquisition in the plant growth-promoting bacterium Pseudomonas fluorescens SBW25. BMC Microbiol 2008, 8:7. BioMed Central Full Text
• [23]De Bruijn I, De Kock MJD, Yang M, De Waard P, Van Beek TA, Raaijmakers JM: Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Mol Microbiol 2007, 63:417-428.
• [24]Haapalainen M, Mosorin H, Dorati F, Wu R-F, Roine E, Taira S, Nissinen R, Mattinen L, Jackson R, Pirhonen M, Lin N-C: Hcp2, a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000, is required for fitness for competition against bacteria and yeasts. J Bacteriol 2012, 194:4810-4822.
• [25]Halgren A, Azevedo M, Mills D, Armstrong D, Thimmaiah M, McPhail K, Banowetz G: Selective inhibition of Erwinia amylovora by the herbicidally active germination-arrest factor (GAF) produced by Pseudomonas bacteria. J Appl Microbiol 2011, 111:949-959.
• [26]Katagiri K, Tori K, Kimura Y, Yoshida T, Nagasaki T, Minato H: A new antibiotic. Furanomycin, an isoleucine antagonist. J Med Chem 1967, 10:1149-1154.
• [27]Joullié MM, Wang PC, Semple JE: Total synthesis and revised structural assignment of (+)-furanomycin. J Am Chem Soc 1980, 102:887-889.
• [28]Semple JE, Wang PC, Lysenko Z, Joullié MM: Total synthesis of (+)-furanomycin and stereoisomers. J Am Chem Soc 1980, 102:7505-7510.
• [29]Zimmermann PJ, Lee JY, Hlobilova I, Endermann R, Häbich D, Jäger V: Synthesis of L-furanomycin and its analogues via furoisoxazolines. Eur J Org Chem 2005, 2005:3450-3460.
• [30]Parry RJ, Buu HP: Investigations of the biosynthesis of furanomycin. Unexpected derivation from acetate and propionate. J Am Chem Soc 1983, 105:7446-7447.
• [31]Parry RJ, Turakhia R, Buu HP: The biosynthesis of furanomycin: on the mechanism of formation of the ether linkage. J Am Chem Soc 1988, 110:4035-4036.
• [32]Parry RJ, Yang N: Isolation and characterization of furanomycin nonproducing Streptomyces threomyceticus mutants. J Antibiot (Tokyo) 1992, 45:1161-1166.
• [33]Mitchell RE, Frey EJ, Benn MH: Rhizobitoxine and L-threo-hydroxythreonine production by the plant pathogen Pseudomonas andropogonis. Phytochemistry 1986, 25:2711-2715.
• [34]Sahm U, Knobloch G, Wagner F: Isolation and characterization of the methionine antagonist L-2-amino-4-methoxy-trans-3-butenoic acid from Pseudomonas aeruginosa grown on n-paraffin. J Antibiot (Tokyo) 1973, 26:389-390.
• [35]Scannell JP, Pruess DL, Demny TC, Sello LH, Williams T, Stempel A: Antimetabolites produced by microorganisms. V. L-2-Amino-4-methoxy-trans-3-butenoic acid. J Antibiot (Tokyo) 1972, 25:122-127.
• [36]Braun SD, Völksch B, Nüske J, Spiteller D: 3-Methylarginine from Pseudomonas syringae pv. syringae 22d/93 suppresses the bacterial blight caused by its close relative Pseudomonas syringae pv. glycinea. ChemBioChem 2008, 9:1913-1920.
• [37]Lee X, Azevedo MD, Armstrong DJ, Banowetz GM, Reimmann C: The Pseudomonas aeruginosa antimetabolite L-2-amino-4-methoxy-trans-3-butenoic acid inhibits growth of Erwinia amylovora and acts as a seed germination arrest factor. Environ Microbiol Rep 2013, 5:83-89.
• [38]Lee X, Reimmann C, Greub G, Sufrin J, Croxatto A: The Pseudomonas aeruginosa toxin L-2-amino-4-methoxy-trans-3-butenoic acid inhibits growth and induces encystment in Acanthamoeba castellanii. Microbes Infect 2012, 14:268-272.
• [39]Kohno T, Kohda D, Haruki M, Yokoyama S, Miyazawa T: Nonprotein amino acid furanomycin, unlike isoleucine in chemical structure, is charged to isoleucine tRNA by isoleucyl-tRNA synthetase and incorporated into protein. J Biol Chem 1990, 265:6931-6935.
• [40]Sugawara M, Okazaki S, Nukui N, Ezura H, Mitsui H, Minamisawa K: Rhizobitoxine modulates plant-microbe interactions by ethylene inhibition. Biotechnol Adv 2006, 24:382-388.
• [41]Mazzola M, Cook RJ, Thomashow LS, Weller DM, Pierson LS 3rd: Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl Environ Microbiol 1992, 58:2616-2624.
• [42]Sambrook JF, Russell DW: Molecular cloning: A laboratory manual. 3rd edition. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2001.
• [43]Langley RA, Kado CI: Studies on Agrobacterium tumefaciens. Conditions for mutagenesis by N-methyl-N’-nitro-N-nitrosoguanidine and relationships of A. tumefaciens to crown-gall tumor induction. Mutat Res 1972, 14:277-286.
• [44]Shenker M, Chen Y, Hadar Y: Rapid method for accurate determination of colorless siderophores and synthetic chelates. Soil Sci Soc Am J 1995, 59:1612-1618.