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A decade of understanding secondary metabolism in Pseudomonas spp. for sustainable agriculture and pharmaceutical applications

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Abstract

Pseudomonas spp. have been widely studied for their plant growth promoting and antimicrobial metabolites. The genus got attention due to the production of array of secondary metabolites involved in the suppression of phytopathogens and ability to stimulate plant growth by means of nitrogen-fixation, production of hydrolytic enzymes, regulatory hormones, and solubilization of inorganic minerals. In recent years, research was focused towards identification of biosynthesis pathways and genes involved in the production of secondary metabolites that led to the discovery of novel metabolites including many new phenazine derivatives, quorum-sensing signals, rhizoxin analogues, cyclic lipopeptides, and a new class of alkyl-substituted aromatic acids. Identification of these biosynthetic pathways provided insights for their successful application in agriculture and for environmental sustainability. In addition, many genomic and metabolomic databases such as; METLIN, KEGG, GNPS, CFM-ID, MassBank, and MetaboLights, allowed exploring intricate metabolic pathways and significant genes involved in the biosynthesis of compounds. Several softwares, genome-mining tools and new techniques, such as MALDI-IMS and MALDI-FTICR MS were developed to facilitate the characterization of new metabolites. Additionally, use of MALDI-imaging techniques facilitated real-time visualization of complex microbial communities and their relationship with pathogens. Secondary metabolites of Pseudomonas spp. were also demonstrated for their apoptotic, anti-mitotic, nematocidal, herbicidal, anthelmintic, insecticidal, and phytotoxic effects. Total biosynthesis of metabolic derivatives and genetic engineering enabled to develop strains with improved yield of targeted bio-products. Availability and access to published genomic sequences and comparative bioinformatics tools helped in identification of strain-specific traits and development of multifunctional inocula. This review highlights significant advances in identification of Pseudomonas secondary metabolites for their successful agricultural and pharmaceutical applications.

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References

  • Al-Hinai AH, Al-Sadi AM, Al-Bahry SN, Mothershaw AS, Al-Said FA et al (2010) Isolation and characterization of Pseudomonas aeruginosa with antagonistic activity against Pythium aphanidermatum. J Plant Pathol 92:653–660

    CAS  Google Scholar 

  • Allen F, Pon A, Wilson M, Greiner R, Wishart D (2014) CFM-ID: a web server for annotation, spectrum prediction and metabolite identification from tandem mass spectra. Nucleic Acids Res 42:W94–W99

    Article  CAS  Google Scholar 

  • Bassarello C, Lazzaroni S, Bifulco G, Cantore P et al (2004) Tolaasins A–E, five new lipodepsipeptides produced by Pseudomonas tolaasii. J Nat Prod 67:811–816

    Article  CAS  Google Scholar 

  • Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051

    Article  CAS  Google Scholar 

  • Berti AD, Thomas MG (2009) Analysis of achromobactin biosynthesis by Pseudomonas syringae pv. syringae B728a. J Bacteriol 191:4594–4604

    Article  CAS  Google Scholar 

  • Bonnichsen L, Bygvraa Svenningsen N, Rybtke M et al (2015) Lipopeptide biosurfactant viscosin enhances dispersal of Pseudomonas fluorescens SBW25 biofilms. Microbiology 161:2289–2297. https://doi.org/10.1099/mic.0.000191

    Article  CAS  Google Scholar 

  • Burlinson P, Studholme D, Cambray-Young J, Heavens D et al (2013) Pseudomonas fluorescens NZI7 repels grazing by C. elegans, a natural predator. ISME J 7:1126–1138

    Article  CAS  Google Scholar 

  • Burr SE, Gobeli S, Kuhnert P, Goldschmidt-Clermont E, Frey J (2010) Pseudomonas chlororaphis subsp. piscium subsp. nov., isolated from freshwater fish. Int J Syst Evol Microbiol 60:2753–2757. https://doi.org/10.1099/ijs.0.011692-0

    Article  CAS  Google Scholar 

  • Calderón CE, Ramos C, de Vicente A, Cazorla FM (2015) Comparative genomic analysis of Pseudomonas chlororaphis PCL1606 reveals new insight into antifungal compounds involved in biocontrol. Mol Plant Microbe Interact 28:249–260. https://doi.org/10.1094/MPMI-10-14-0326-FI

    Article  CAS  Google Scholar 

  • Cantore P, Lazzaroni S, Coraiola M, Serra MD, Cafarchia C, Evidente A, Iacobellis NS (2006) Biological characterization of white line-inducing principle (WLIP) produced by Pseudomonas reactans NCPPB1311. MPMI 19:1113–1120

    Article  Google Scholar 

  • Caspi R, Billington R, Ferrer L et al (2016) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 44:D471–D480

    Article  CAS  Google Scholar 

  • Cezairliyan B, Vinayavekhin N, Grenfell-Lee D, Yuen GJ, Saghatelian A, Ausubel FM (2013) Identification of Pseudomonas aeruginosa phenazines that kill Caenorhabditis elegans. PLoS Pathog 91:e1003101. https://doi.org/10.1371/journal.ppat.1003101

    Article  CAS  Google Scholar 

  • Chen JW, Chin S, Tee KK, Yin WF, Choo YM, Chan KG (2013) N-Acyl homoserine lactone-producing Pseudomonas putida strain T2-2 from human tongue surface. Sensors (Basel) 13:13192–13203. https://doi.org/10.3390/s131013192

    Article  CAS  Google Scholar 

  • Chen Y, Shen X, Peng H, Hu H, Wang W, Zhang X (2015) Comparative genomic analysis and phenazine production of Pseudomonas chlororaphis, a plant growth-promoting rhizobacterium. Genom Data 22:33–42. https://doi.org/10.1016/j.gdata.2015.01.006

    Article  Google Scholar 

  • Choi C, Münch R, Leupold S, Klein J, Siegel I et al (2007) SYSTOMONAS—an integrated database for systems biology analysis of Pseudomonas. Nucleic Acids Res 35:D533–D537

    Article  CAS  Google Scholar 

  • Clifford JC, Buchanan A, Vining O, Kidarsa TA, Chang JH, McPhail KL, Loper JE (2016) Phloroglucinol functions as an intracellular and intercellular chemical messenger influencing gene expression in Pseudomonas protegens. Environ Microbiol 18:3296–3308. https://doi.org/10.1111/1462-2920.13043

    Article  CAS  Google Scholar 

  • de Bruijn MJD, de Kock P, de Waard TA, van Beek Raaijmakers JM (2008) Massetolide A biosynthesis in Pseudomonas fluorescens. J Bacteriol 190:2777–2789

    Article  Google Scholar 

  • De Maeyer K, D’aes GK, Hua H, Perneel M, Vanhaecke L, Noppe H, Hofte M (2011) N-Acylhomoserine lactone quorum-sensing signaling in antagonistic phenazine-producing Pseudomonas isolates from the red cocoyam rhizosphere. Microbiology 157:459–472

    Article  Google Scholar 

  • Deng P, Wang X, Baird SM, Lu SE (2015) Complete genome of Pseudomonas chlororaphis strain UFB2, a soil bacterium with antibacterial activity against bacterial canker pathogen of tomato. Stand Genom Sci. https://doi.org/10.1186/s40793-015-0106-x

    Article  Google Scholar 

  • Deveau A, Gross H, Palin B, Mehnaz S, Schnepf M et al (2016) Role of secondary metabolites in the interaction between Pseudomonas fluorescens and soil microorganisms under iron-limited conditions. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiw107

    Article  Google Scholar 

  • Dhanasekaran AR, Pearson JL, Ganesan B, Weimer BC (2015) Metabolome searcher: a high throughput tool for metabolite identification and metabolic pathway mapping directly from mass spectrometry and metabolites. BMC Bioinform. https://doi.org/10.1186/s12859-015-0462-y

    Article  Google Scholar 

  • Dimkpa CO (2014) Can nanotechnology deliver the promised benefits without negatively impacting soil microbial life? J Basic Microbiol 54:889–904

    Article  CAS  Google Scholar 

  • Dimkpa CO, McLean JE, Britt DW, Anderson AJ (2012) CuO and ZnO nanoparticles differently affect the secretion of fluorescent siderophores in the beneficial root colonizer Pseudomonas chlororaphis O6. Nanotoxicology 6:635–642

    Article  CAS  Google Scholar 

  • Dimkpa CO, Hansen T, Stewart J, McLean JE, Britt DW, Anderson AJ (2015) ZnO nanoparticles and root colonization by a beneficial pseudomonad influence metal responses in bean (Phaseolus vulgaris). Nanotoxicology 9:271–278

    Article  CAS  Google Scholar 

  • Djavaheri M, Mercado-Blanco J, Versluis C, Meyer J-M, Loon LC, Bakker PAHM (2012) Iron-regulated metabolites produced by Pseudomonas fluorescens WCS374r are not required for eliciting induced systemic resistance against Pseudomonas syringae pv. tomato in Arabidopsis. MicrobiologyOpen 1:311–325. https://doi.org/10.1002/mbo3.32

    Article  CAS  Google Scholar 

  • Dunham SJB, Ellis JF, Li B, Sweedler JV (2017) Mass spectrometry imaging of complex microbial communities. Acc Chem Res 50:96–104. https://doi.org/10.1021/acs.accounts.6b00503

    Article  CAS  Google Scholar 

  • Elkins RB, Ingels CA, Lindow SE (2005) Control of fire blight by Pseudomonas fluorescens A506 introduced into unopened pear Flowers. Acta Hortic 671:585–594. https://doi.org/10.17660/actahortic.2005.671.82

    Article  Google Scholar 

  • Fleurbaaij F, Kraakman MEM, Claas ECJ et al (2016) Typing Pseudomonas aeruginosa isolates with ultrahigh resolution MALDI-FTICR mass spectrometry. Anal Chem 88:5996–6003. https://doi.org/10.1021/acs.analchem.6b01037

    Article  CAS  Google Scholar 

  • Fravel DR (2005) Commercialization and implementation of biocontrol. Annu Rev Phytopathol 43:337–359

    Article  CAS  Google Scholar 

  • Gao S, Hothersall J, Wu J et al (2014) Biosynthesis of mupirocin by Pseudomonas fluorescens NCIMB 10586 involves parallel pathways. J Am Chem Soc 136:5501–5507. https://doi.org/10.1021/ja501731p

    Article  CAS  Google Scholar 

  • Gao SS, Wang L, Song Z, Hothersall J, Stevens ER et al (2017) Selected mutations reveal new intermediates in the biosynthesis of mupirocin and the thiomarinol antibiotics. Angew Chem Int Ed Engl 56:3930–3934

    Article  CAS  Google Scholar 

  • Garrido-Sanz D, Arrebola E, Martínez-Granero F, García-Méndez S, Muriel C, Blanco-Romero E et al (2017) Classification of isolates from the Pseudomonas fluorescens complex into phylogenomic groups based in group-specific markers. Front Microbiol 8:413. https://doi.org/10.3389/fmicb.2017.00413

    Article  Google Scholar 

  • Gray E, Smith D (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37:395–412

    Article  CAS  Google Scholar 

  • Guttenberger N, Blankenfeldt W, Breinbauer R (2017) Recent developments in the isolation, biological function, biosynthesis, and synthesis of phenazine natural products. Bioorg Med Chem 25:6149–6166

    Article  CAS  Google Scholar 

  • Hardebeck GA, Turco RF, Latin R, Reicher ZJ (2004) Application of Pseudomonas aureofaciens Tx-1 through irrigation for control of dollar spot and brown patch on fairway-height turf. HortScience 39:1750–1753

    Google Scholar 

  • Hashimoto M, Hattori K (1966) Oxypryrrolnitrin: a metabolite of Pseudomonas. Chem Pharm Bull 14:1314–1316

    Article  CAS  Google Scholar 

  • Haug K, Salek RM, Conesa P et al (2013) MetaboLights—an open-access general-purpose repository for metabolomics studies and associated meta-data. Nucleic Acids Res. https://doi.org/10.1093/nar/gks1004

    Article  Google Scholar 

  • Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598

    Article  Google Scholar 

  • Hennessy RC, Phippen CBW, Nielsen KF, Olsson S, Stougaard P (2017) Biosynthesis of the antimicrobial cyclic lipopeptides nunamycin and nunapeptin by Pseudomonas fluorescens strain In5 is regulated by the LuxR-type transcriptional regulator NunF. Microbiol Open 6:e516. https://doi.org/10.1002/mbo3.516

    Article  CAS  Google Scholar 

  • Henriksen A, Anthoni U, Nielsen TH, Sørensen J, Christophersen C, Gajhede M (2000) Cyclic lipoundecapeptide tensin from Pseudomonas fluorescens strain 96.578. Acta Crystallogr C 56:113–115

    Article  Google Scholar 

  • Horai H, Arita M, Kanaya S et al (2010) MassBank: a public repository for sharing mass spectral data for life sciences. J Mass Spectrom 45:703–714

    Article  CAS  Google Scholar 

  • Hummel J, Strehmel N, Metabolomics Selbig J et al (2010) Decision tree supported substructure prediction of metabolites from GC-MS profiles. Metabolomica 6:322

    Article  CAS  Google Scholar 

  • Jang JY, Yang SY, Kim YC, Lee CW, Park MS, Kim JC, Kim IS (2013) Identification of orfamide A as an insecticidal metabolite produced by Pseudomonas protegens F6. J Agric Food Chem 61:6786–6791. https://doi.org/10.1021/jf401218w

    Article  CAS  Google Scholar 

  • Jiang Q, Xiao J, Zhou C, Mu Y, Xu B, He Q, Xiao M (2014) Complete genome sequence of the plant growth-promoting rhizobacterium Pseudomonas aurantiaca strain JD37. J Biotechnol 20:85–86

    Article  Google Scholar 

  • Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 44:D353–D361. https://doi.org/10.1093/nar/gkw1092

    Article  CAS  Google Scholar 

  • Kennedy RK, Naik PR, Veena V, Lakshmi BS, Lakshmi P, Krishna R, Sakthivel N (2015) 5-Methyl phenazine-1-carboxylic acid: a novel bioactive metabolite by a rhizosphere soil bacterium that exhibits potent antimicrobial and anticancer activities. Chem Biol Interact 231:71–82. https://doi.org/10.1016/j.cbi.2015.03.002

    Article  CAS  Google Scholar 

  • Kerr JR (2000) Phenazine pigments: antibiotics and virulence factors. Rev Infect Dis 2:84–194

    Google Scholar 

  • Khan U, Rahman KM (2015) Seed treatment with bio-fungicides for management of dry root rot of Chick pea caused by Macrophomina phaseolina. Ann Plant Prot Sci 23:302–307

    Google Scholar 

  • Kidarsa TA, Goebel NC, Zabriskie TM, Loper JE (2011) Phloroglucinol mediates cross-talk between the pyoluteorin and 2,4-diacetylphloroglucinol biosynthetic pathways in Pseudomonas fluorescens Pf-5. Mol Microbiol 81:395–414. https://doi.org/10.1111/j.1365-2958.2011.07697.x

    Article  CAS  Google Scholar 

  • King ZA, Lu JS, Dräger A, Miller PC et al (2016) BiGG models: a platform for integrating, standardizing, and sharing genome-scale models. Nucleic Acids Res 44:D515–D522. https://doi.org/10.1093/nar/gkv1049

    Article  CAS  Google Scholar 

  • Lai Z, Tsugawa H, Wohlgemuth G et al (2017) Identifying metabolites by integrating metabolome databases with mass spectrometry cheminformatics. Nat Methods 15:53–56

    Article  Google Scholar 

  • Li W, Rokni-Zadeh H, De Vleeschouwer M, Ghequire MGK, Sinnaeve D et al (2013) The antimicrobial compound xantholysin defines a new group of Pseudomonas cyclic lipopeptides. PLoS ONE 8:e62946. https://doi.org/10.1371/journal.pone.0062946

    Article  CAS  Google Scholar 

  • Lim DJ, Yang SY, Noh MY, Lee CW, Kim JC, Kim IS (2017) Identification of lipopeptide xantholysins from Pseudomonas sp. DJ15 and their insecticidal activity against Myzus persicae. J Entomol Res 47:337–343

    Article  CAS  Google Scholar 

  • Liu Y, Lu SE, Baird SM, Qiao J, Du Y (2014) Draft genome sequence of Pseudomonas chlororaphis YL-1, a biocontrol strain suppressing plant microbial pathogens. Genome Announc 2:e01225-13. https://doi.org/10.1128/genomeA.01225-13

    Article  Google Scholar 

  • Liu K, Hu H, Wang W, Zhang X (2016) Genetic engineering of Pseudomonas chlororaphis GP72 for the enhanced production of 2-hydroxyphenazine. Microb Cell Fact. https://doi.org/10.1186/s12934-016-0529-0

    Article  Google Scholar 

  • Loewen PC, Villenueva J, Fernando WGD, de Kievit T (2014) Genome sequence of Pseudomonas chlororaphis strain PA23. Genome Announc 2:e00689-14. https://doi.org/10.1128/genomeA.00689-14

    Article  Google Scholar 

  • Loper JE, Henkels MD, Shaffer BT et al (2008) Isolation and identification of rhizoxin analogs from pseudomonas fluorescens Pf-5 by using a genomic mining strategy. Appl Environ Microbiol 74:3085–3093

    Article  CAS  Google Scholar 

  • Loper JE, Hassan KA, Mavrodi DV, Davis EW II, Lim CK, Shaffer BT et al (2012) Comparative genomics of plant-associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet 8:e1002784. https://doi.org/10.1371/journal.pgen.1002784

    Article  CAS  Google Scholar 

  • Loper JE, Henkels MD, Rangel LI, Olcott MH et al (2016) Rhizoxin analogs, orfamide A and chitinase production contribute to the toxicity of Pseudomonas protegens strain Pf-5 to Drosophila melanogaster. Environ Microbiol 18:3509–3521. https://doi.org/10.1111/1462-2920.13369

    Article  CAS  Google Scholar 

  • Ma Z, Geudens N, Kieu NP, Sinnaeve D, Ongena M, Martins JC, Höfte M (2016) Biosynthesis, chemical structure and structure–activity relationship of orfamide lipopeptides produced by Pseudomonas protegens and related species. Front Microbiol. https://doi.org/10.3389/fmicb.2016.00382

    Article  Google Scholar 

  • MacLean B, Tomazela DM, Shulman N, Chambers M, Finney GL, Frewen B, Kern R, Tabb DL, Liebler DC, MacCoss MJ (2010) Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26:966–968. https://doi.org/10.1093/bioinformatics/btq054

    Article  CAS  Google Scholar 

  • Matthijs S, Baysse C, Koedam N, Tehrani KA, Verheyden L, Budzikiewicz H, Schäfer M, Hoorelbeke B et al (2004) The Pseudomonas siderophore quinolobactin is synthesized from xanthurenic acid, an intermediate of the kynurenine pathway. Mol Microbiol 52:371–384. https://doi.org/10.1111/j.1365-2958.2004.03999.x

    Article  CAS  Google Scholar 

  • McCully LM, Bitzer AS, Spence CA, Bais HP, Silby MW (2014) Draft genome sequence of rice isolate Pseudomonas chlororaphis EA105. Genome Announc 2:e01342-14. https://doi.org/10.1128/genomeA.01342-14

    Article  Google Scholar 

  • Mehnaz S, Saleem RSZ, Yameen B, Pianet I, Schnakenburg G, Pietraszkiewicz H et al (2013) Lahorenoic acids A–C, ortho-dialkyl-substituted aromatic acids from the biocontrol strain Pseudomonas aurantiaca PB-St2. J Nat Prod 76:135–141

    Article  CAS  Google Scholar 

  • Mehnaz S, Bauer JS, Gross H (2014) Complete genome sequence of the sugar cane endophyte Pseudomonas aurantiaca PB-St2, a disease-suppressive bacterium with antifungal activity toward the plant pathogen Colletotrichum falcatum. Genome Announc 2:e01108–e01113. https://doi.org/10.1128/genomeA.01108-13

    Article  Google Scholar 

  • Meyer SLF, Halbrendt JM, Carta LK et al (2009) Toxicity of 2,4-diacetylphloroglucinol (DAPG) to plant-parasitic and bacterial-feeding nematodes. J Nematol 41:274–280

    CAS  Google Scholar 

  • Michelsen CF, Watrous J, Glaring MA, Kersten R, Koyama N, Dorrestein PC, Stougaard P (2015) Nonribosomal peptides, key biocontrol components for Pseudomonas fluorescens In5, isolated from a Greenlandic suppressive soil. mBio 6:00079-15. https://doi.org/10.1128/mbio.00079-15

    Article  Google Scholar 

  • Minagawa S, Inami H, Kato T, Sawada S, Yasuki T, Miyairi S et al (2012) RND type efflux pump system MexAB-OprM of Pseudomonas aeruginosa selects bacterial languages, 3-oxo-acyl-homoserine lactones, for cell-to-cell communication. BMC Microbiol. https://doi.org/10.1186/1471-2180-12-70

    Article  Google Scholar 

  • Moree WJ, Phelan VV, Wu C, Bandeira N et al (2012) Interkingdom metabolic transformations captured by microbial imaging mass spectrometry. PNAS 109:13811–13816. https://doi.org/10.1073/pnas.1206855109

    Article  Google Scholar 

  • Morohoshi T, Yamaguchi T, Xie X et al (2017) Complete genome sequence of Pseudomonas chlororaphis subsp. aurantiaca reveals a triplicate quorum-sensing mechanism for regulation of phenazine production. Microbes Environ 32:47–53

    Article  Google Scholar 

  • Nandi M, Selin C, Brassinga AKC, Belmonte MF, Fernando WGD, Loewen PC et al (2015) Pyrrolnitrin and hydrogen cyanide production by Pseudomonas chlororaphis strain PA23 exhibits nematicidal and repellent activity against Caenorhabditis elegans. PLoS ONE 10:e0123184. https://doi.org/10.1371/journal.pone.0123184

    Article  CAS  Google Scholar 

  • O’Callaghan M (2016) Microbial inoculation of seed for improved crop performance: issues and opportunities. Appl Microbiol Biotechnol 100:5729–5746. https://doi.org/10.1007/s00253-016-7590-9

    Article  CAS  Google Scholar 

  • Olorunleke FE, Kieu NP, Waele ED, Timmerman M, Ongena M, Höfte M (2017) Coregulation of the cyclic lipopeptides orfamide and sessilin in the biocontrol strain Pseudomonas sp. CMR12a. MicrobiologyOpen 6:e499. https://doi.org/10.1002/mbo3.499

    Article  CAS  Google Scholar 

  • Pathma J, Ayyadurai N, Sakthivel N (2010) Assessment of genetic and functional relationship of antagonistic fluorescent pseudomonads of rice rhizosphere by repetitive sequence, protein coding sequence and functional gene analyses. J Microbiol 48:715–727. https://doi.org/10.1007/s12275-010-0064-3

    Article  CAS  Google Scholar 

  • Peng Q, Yi L, Zhou L, Peng Q (2018) Draft genome sequence of the vanadium-leaching bacterium Pseudomonas chlororaphis strain L19. Genome Announc 6:e00966-17. https://doi.org/10.1128/genomeA.00966-17

    Article  Google Scholar 

  • Phelan VV, Fang J, Dorrestein PC (2015) Mass spectrometry analysis of Pseudomonas aeruginosa treated with azithromycin. J Am Soc Mass Spectrom 26:873–877. https://doi.org/10.1007/s13361-015-1101-6

    Article  CAS  Google Scholar 

  • Philmus B, Shaffer BT, Kidarsa TA, Yan Q et al (2015) Investigations into the biosynthesis, regulation, and self-resistance of toxoflavin in Pseudomonas protegens Pf-5. ChemBioChem 16:1782–1790. https://doi.org/10.1002/cbic.201500247

    Article  CAS  Google Scholar 

  • Pierson LS, Pierson EA (2010) Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. App Microbiol Biotechnol 86:1659–1670. https://doi.org/10.1007/s00253-010-2509-3

    Article  CAS  Google Scholar 

  • Rokni-Zadeh H, Li W, Yilma E, Sanchez-Rodriguez A, De Mot R (2013) Distinct lipopeptide production systems for WLIP (white line-inducing principle) in Pseudomonas fluorescens and Pseudomonas putida. Environ Microbiol Rep 5:160–169. https://doi.org/10.1111/1758-2229.12015

    Article  CAS  Google Scholar 

  • Ruffner B, Péchy-Tarr M, Höfte M et al (2015) Evolutionary patchwork of an insecticidal toxin shared between plant-associated pseudomonads and the insect pathogens Photorhabdus and Xenorhabdus. BMC Genom 16:609. https://doi.org/10.1186/s12864-015-1763-2

    Article  CAS  Google Scholar 

  • Samina G, Pavlovab M, Arifa MI et al (2014) A Pseudomonas putida strain genetically engineered for 1,2,3-trichloropropane bioremediation. Appl Environ Microbiol 80:5467–5476

    Article  Google Scholar 

  • Sams T, Baker Y, Hodgkinson J, Gross J, Spring D, Welch M (2016) The Pseudomonas quinolone signal (PQS). Isr J Chem 56:282–294. https://doi.org/10.1002/ijch.201400128

    Article  CAS  Google Scholar 

  • Shahid I, Rizwan M, Baig DN, Saleem RS, Malik KA, Mehnaz S (2017) Secondary metabolites production and plant growth promotion by Pseudomonas chlororaphis subsp. aurantiaca strains isolated from cotton, cactus and para grass. J Microbiol Biotechnol 27:480–491

    Article  Google Scholar 

  • Shanmugaiah V, Mathivanan N, Varghese B (2010) Purification, crystal structure and antimicrobial activity of phenazine-1-carboxamide produced by a growth-promoting biocontrol bacterium, Pseudomonas aeruginosa MML2212. J Appl Microbiol 108:703–711. https://doi.org/10.1111/j.1365-2672.2009.04466.x

    Article  CAS  Google Scholar 

  • Shen X, Chen M, Hu H et al (2012) Genome sequence of Pseudomonas chlororaphis GP72, a root-colonizing biocontrol strain. J Bacteriol 194:1269–1270. https://doi.org/10.1128/JB.06713-11

    Article  CAS  Google Scholar 

  • Shen X, Wang Z, Huang X, Hu H, Wang W, Zhang X (2017) Developing genome-reduced Pseudomonas chlororaphis strains for the production of secondary metabolites. BMC Genom 18:715. https://doi.org/10.1186/s12864-017-4127-2

    Article  Google Scholar 

  • Slininger PJ, Burkhead KD, Schisler DA, Bothast RJ (2000) Isolation, identification, and accumulation of 2-acetamidophenol in liquid cultures of the wheat take all biocontrol agent Pseudomonas fluorescens 2–79. App Microbiol Biotechnol 54:376–381

    Article  CAS  Google Scholar 

  • Smith CA, O’Maille G, Want EJ, Qin C, Trauger SA, Brandon TR et al (2005) METLIN: a metabolite mass spectral database. Ther Drug Monit 27:747–751

    Article  CAS  Google Scholar 

  • Sørensen D, Nielsen TH, Christophersen C, Sørensen J, Gajhede M (2001) Cyclic lipoundecapeptide amphisin from Pseudomonas sp. strain DSS73. Acta Crystallogr C 57:1123–1124

    Article  Google Scholar 

  • Sutherland R, Boon RJ, Griffin KE, Masters PJ, Slocombe B, White AR (1985) Antibacterial activity of mupirocin (pseudomonic acid), a new antibiotic for topical use. Antimicrob Agents Chemother 27:495–498

    Article  CAS  Google Scholar 

  • Tashiro Y, Yawata Y, Toyofuku M, Uchiyama H, Nomura N (2013) Interspecies interaction between Pseudomonas aeruginosa and other microorganisms. Microbes Environ 28:13–24

    Article  Google Scholar 

  • Thongsri Y, Aromdee C, Yenjai C, Kanokmedhakul S, Chaiprasert A, Hamal Prariyachatigul C (2014) Detection of diketopiperazine and pyrrolnitrin, compounds with anti-Pythium insidiosum activity, in a Pseudomonas stutzeri environmental strain. Biomed Pap 158:378–383

    Article  Google Scholar 

  • Town J, Audy P, Boyetchko SM, Dumonceaux TJ (2016a) Genome sequence of Pseudomonas chlororaphis strain 189. Genome Announc 4:e00581-16. https://doi.org/10.1128/genomeA.00581-16

    Article  Google Scholar 

  • Town J, Cui N, Audy P, Boyetchko S, Dumonceaux TJ (2016b) Improved high-quality draft genome sequence of Pseudomonas fluorescens KENGFT3. Genome Announc 3:e00428-16. https://doi.org/10.1128/genomeA.00428-16

    Article  Google Scholar 

  • Vázquez-Rivera D, González O, Guzmán-Rodríguez J et al (2015) Cytotoxicity of cyclodipeptides from Pseudomonas aeruginosa PAO1 leads to apoptosis in human cancer cell lines. BioMed Res Intern. https://doi.org/10.1155/2015/197608

    Article  Google Scholar 

  • Vleeschouwer M, Martins JC, Madder A (2016) First total synthesis of WLIP: on the importance of correct protecting group choice. J Pept Sci 22:149–155. https://doi.org/10.1002/psc.2852

    Article  CAS  Google Scholar 

  • Wang D, Yu JM, Dorosky RJ, Pierson LS III, Pierson EA (2016a) The Phenazine 2-hydroxy-phenazine-1-carboxylic acid promotes extracellular DNA release and has broad transcriptomic consequences in Pseudomonas chlororaphis 30–84. PLoS ONE 11:e0148003. https://doi.org/10.1371/journal.pone.0148003

    Article  CAS  Google Scholar 

  • Wang M et al (2016b) Sharing and community curation of mass spectrometry data with global natural products social molecular networking. Nat Biotechnol 34:828–837

    Article  CAS  Google Scholar 

  • Weber T, Blin K, Duddela S et al (2015) antiSMASH 3.0-a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43:W237–W243

    Article  CAS  Google Scholar 

  • Welbaum GE, Sturz AV, Dong Z, Nowak J (2004) Managing soil microorganisms to improve productivity of agroecosystems. Crit Rev Plant Sci 23:175–193

    Article  CAS  Google Scholar 

  • Wells G, Palethorpe S, Pesci EC (2017) PsrA controls the synthesis of the Pseudomonas aeruginosa quinolone signal via repression of the FadE homolog, PA0506. PLoS ONE 12:e0189331. https://doi.org/10.1371/journal.pone.0189331

    Article  CAS  Google Scholar 

  • Yadav G, Gokhale RS, Mohanty D (2003) SEARCHPKS: a program for detection and analysis of polyketide synthase domains. Nucleic Acids Res 31:3654–3658

    Article  CAS  Google Scholar 

  • Yang JY, Phelan VV, Simkovsky R et al (2012) Primer on agar-based microbial imaging mass spectrometry. J Bacteriol 194:6023–6028

    Article  CAS  Google Scholar 

  • Zhang XX, Rainey PB (2013) Exploring the sociobiology of pyoverdin-producing Pseudomonas. Evolution 67:3161–3174. https://doi.org/10.1111/evo.12183

    Article  Google Scholar 

  • Zhang R, Xu X, Chen W, Huang Q (2016) Genetically engineered Pseudomonas putida X3 strain and its potential ability to bioremediate soil microcosms contaminated with methyl parathion and cadmium. Appl Microbiol Biotechnol 100:1987–1997. https://doi.org/10.1007/s00253-015-7099-7

    Article  CAS  Google Scholar 

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Correspondence to Samina Mehnaz.

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Shahid, I., Malik, K.A. & Mehnaz, S. A decade of understanding secondary metabolism in Pseudomonas spp. for sustainable agriculture and pharmaceutical applications. Environmental Sustainability 1, 3–17 (2018). https://doi.org/10.1007/s42398-018-0006-2

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