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Contribution of the Siderophores Pyoverdine and Enantio-Pyochelin to Fitness in Soil of Pseudomonas protegens Pf-5

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Abstract

Pseudomonas protegens synthesizes two major iron-chelating metabolites (siderophores): pyoverdine (Pvd) and enantio-pyochelin (E-Pch). Although iron sequestration and uptake seem to be the main biological role of these siderophores, other functions including metal homeostasis and antibiotic activity have been proposed. The aim of this study was to evaluate the contribution of Pvd and E-Pch to the survival of P. protegens in soil using wild type and isogenic mutant strains unable to produce Pvd, E-Pch or both siderophores. Survival of these strains in sterile soil microcosms, in soil microcosms containing the native microflora and in sterile soil microcosms containing fusaric acid (a mycotoxin able to chelate iron and other metals), was compared by determination of colony forming units (CFU) per gram dry soil over time. In sterile soil, cell densities of Pvd-producing strains were significantly higher than that of non-producers after 21 days of permanence in the microcosms. In non-sterile soil, viability of all strains declined faster than in sterile soil and Pvd producers showed higher CFU × (g dry weight soil)−1 values than non-producers. The presence of fusaric acid negatively affected viability of strains unable to produce Pvd, while had no effect on the viability of strains able to produce Pvd. Altogether, these results show that the ability to produce Pvd increases survival of P. protegens in soil, while the ability to synthesize E-Pch does not, indicating that under the conditions which prevail in soil, iron scavenging via Pvd is more beneficial than via E-Pch.

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References

  1. Adler C, Corbalan NS, Seyedsayamdost MR, Pomares MF, de Cristobal RE, Clardy J, Kolter R, Vincent PA (2012) Catecholate siderophores protect bacteria from pyochelin toxicity. PLoS ONE 7(10):e46754

    Article  CAS  Google Scholar 

  2. Andrews SC, Robinson AK, Rodriguez-Quinones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27(2–3):215–237

    Article  CAS  Google Scholar 

  3. Bacon CW, Hinton DM, Hinton A Jr (2006) Growth-inhibiting effects of concentrations of fusaric acid on the growth of Bacillus mojavensis and other biocontrol Bacillus species. J Appl Microbiol 100(1):185–194

    Article  CAS  Google Scholar 

  4. Boyer HW, Roulland-Dussoix D (1969) A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol 41(3):459–472

    Article  CAS  Google Scholar 

  5. Brown DW, Lee SH, Kim LH, Ryu JG, Lee S, Seo Y, Kim YH, Busman M, Yun SH, Proctor RH, Lee T (2015) Identification of a 12-gene fusaric acid biosynthetic gene cluster in Fusarium species through comparative and functional genomics. Mol Plant Microbe Interact 28(3):319–332

    Article  CAS  Google Scholar 

  6. Budzikiewicz H (2004) Siderophores of the Pseudomonadaceae sensu stricto (fluorescent and non-fluorescent Pseudomonas spp.). Fortschr Chem Org Naturst 87:81–237

    CAS  PubMed  Google Scholar 

  7. Cox CD, Rinehart KL Jr, Moore ML, Cook JC Jr (1981) Pyochelin: novel structure of an iron-chelating growth promoter for Pseudomonas aeruginosa. Proc Natl Acad Sci USA 78(7):4256–4260

    Article  CAS  Google Scholar 

  8. Dumas Z, Ross-Gillespie A, Kummerli R (2013) Switching between apparently redundant iron-uptake mechanisms benefits bacteria in changeable environments. Proc Biol Sci 280(1764):20131055

    Article  Google Scholar 

  9. Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3(4):307–319

    Article  CAS  Google Scholar 

  10. Herrero M, de Lorenzo V, Timmis KN (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172(11):6557–6567

    Article  CAS  Google Scholar 

  11. Howell CR, Stipanovic RD (1979) Control of Rhizoctonia solani on cotton seedlings with Pseudomonas fluorescens and with an antibiotic produced by the bacterium. Phytopathology 69:480–482

    Article  CAS  Google Scholar 

  12. Kessler B, de Lorenzo V, Timmis KN (1992) A general system to integrate lacZ fusions into the chromosomes of gram-negative eubacteria: regulation of the Pm promoter of the TOL plasmid studied with all controlling elements in monocopy. Mol Gen Genet: MGG 233(1–2):293–301

    Article  CAS  Google Scholar 

  13. King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44(2):301–307

    CAS  PubMed  Google Scholar 

  14. Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428

    Article  CAS  Google Scholar 

  15. Loper JE, Kobayashi DY, Paulsen IT (2007) The genomic sequence of Pseudomonas fluorescens Pf-5: insights into biological control. Phytopathology 97(2):233–238

    Article  CAS  Google Scholar 

  16. López NI, Ruiz JA, Méndez BS (1998) Survival of poly-3-hydroxybutyrate-producing bacteria in soil microcosms. World J Microbiol Biotechnol 14:681–684

    Article  Google Scholar 

  17. Lowbury EJ (1951) Improved culture methods for the detection of Ps. pyocyanea. J Clin Pathol 4(1):66–72

    Article  CAS  Google Scholar 

  18. Malini S (1966) Heavy metal chelates of fusaric acid: in vitro spectrophotometry. J Phytopathol 57(3):221–231

    Article  CAS  Google Scholar 

  19. Martinez-Garcia E, Aparicio T, de Lorenzo V, Nikel PI (2014) New transposon tools tailored for metabolic engineering of gram-negative microbial cell factories. Front Bioeng Biotechnol 2:46

    PubMed  PubMed Central  Google Scholar 

  20. Meyer JM, Abdallah MA (1978) The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. J Gen Microbiol 107:319–328

    Article  CAS  Google Scholar 

  21. Michavila G, Adler C, De Gregorio PR, Lami MJ, Caram Di Santo MC, Zenoff AM, de Cristobal RE, Vincent PA (2017) Pseudomonas protegens CS1 from the lemon phyllosphere as a candidate for citrus canker biocontrol agent. Plant Biol (Stuttg) 19(4):608–617

    Article  CAS  Google Scholar 

  22. Mirleau P, Delorme S, Philippot L, Meyer J, Mazurier S, Lemanceau P (2000) Fitness in soil and rhizosphere of Pseudomonas fluorescens C7R12 compared with a C7R12 mutant affected in pyoverdine synthesis and uptake. FEMS Microbiol Ecol 34(1):35–44

    Article  CAS  Google Scholar 

  23. Nelson DW, Sommers E (1982) Total carbon, organic carbon and organic matter. In: Page AL (ed) Methods of soil analysis, part 2, 2nd edn, vol 9. American Society of Agronomy, Madison, pp 534–579

    Google Scholar 

  24. Phoebe CH Jr, Combie J, Albert FG, Van Tran K, Cabrera J, Correira HJ, Guo Y, Lindermuth J, Rauert N, Galbraith W, Selitrennikoff CP (2001) Extremophilic organisms as and unexplored source fo antifungal compounds. J Antibiot (Tokyo) 54(1):56–65

    Article  CAS  Google Scholar 

  25. Ruiz JA, Bernar EM, Jung K (2015) Production of siderophores increases resistance to fusaric acid in Pseudomonas protegens Pf-5. PLoS ONE 10(1):e0117040

    Article  Google Scholar 

  26. Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13(11):2844–2854

    Article  CAS  Google Scholar 

  27. . Sun GX, Zhou WQ, Zhong JJ (2006) Organotin decomposition by pyochelin, secreted by Pseudomonas aeruginosa even in an iron-sufficient environment. Appl Environ Microbiol 72(9):6411–6413

    Article  CAS  Google Scholar 

  28. Vasil ML, Ochsner UA (1999) The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol Microbiol 34(3):399–413

    Article  CAS  Google Scholar 

  29. Verhagen BW, Trotel-Aziz P, Couderchet M, Hofte M, Aziz A (2010) Pseudomonas spp.-induced systemic resistance to Botrytis cinerea is associated with induction and priming of defence responses in grapevine. J Exp Bot 61(1):249–260

    Article  CAS  Google Scholar 

  30. Wendenbaum S, Demange P, Dell A, Meyer JM, Abdallah MA (1983) The structure of pyoverdine Pa, the siderophore of Pseudomonas aeruginosa. Tetrahedron Lett 24(44):4877–4880

    Article  CAS  Google Scholar 

  31. Youard ZA, Mislin GL, Majcherczyk PA, Schalk IJ, Reimmann C (2007) Pseudomonas fluorescens CHA0 produces enantio-pyochelin, the optical antipode of the Pseudomonas aeruginosa siderophore pyochelin. J Biol Chem 282(49):35546–35553

    Article  CAS  Google Scholar 

  32. Youard ZA, Wenner N, Reimmann C (2011) Iron acquisition with the natural siderophore enantiomers pyochelin and enantio-pyochelin in Pseudomonas species. Biometals 24(3):513–522

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by Grants from Buenos Aires University, Argentina (UBACyT 20020130200117BA) and the Alexander von Humboldt Foundation, Germany (Grant equipment to JAR).

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  1. Ignacio Drehe and Ester Simonetti have contributed equally to this work.

Authors and Affiliations

  1. Instituto de Investigaciones en Biociencias Agrícolas y Ambientales, Universidad de Buenos Aires, CONICET, Facultad de Agronomía, Avenida San Martín 4453, C1417DSE, Buenos Aires, Argentina

    Ignacio Drehe, Ester Simonetti & Jimena A. Ruiz

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  1. Ignacio Drehe
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  2. Ester Simonetti
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  3. Jimena A. Ruiz
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Correspondence to Jimena A. Ruiz.

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Drehe, I., Simonetti, E. & Ruiz, J.A. Contribution of the Siderophores Pyoverdine and Enantio-Pyochelin to Fitness in Soil of Pseudomonas protegens Pf-5. Curr Microbiol 75, 1560–1565 (2018). https://doi.org/10.1007/s00284-018-1560-7

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  • DOI: https://doi.org/10.1007/s00284-018-1560-7

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