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Gluconic acid-producing Pseudomonas sp. prevent γ-actinorhodin biosynthesis by Streptomyces coelicolor A3(2)

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Abstract

Streptomyces are ubiquitous soil bacteria well known for their ability to produce a wide range of secondary metabolites including antibiotics. In their natural environments, they co-exist and interact with complex microbial communities and their natural products are assumed to play a major role in mediating these interactions. Reciprocally, their secondary metabolism can be influenced by the surrounding microbial communities. Little is known about these complex interactions and the underlying molecular mechanisms. During pairwise co-culture experiments, a fluorescent Pseudomonas, Pseudomonas fluorescens BBc6R8, was shown to prevent the production of the diffusible blue pigment antibiotic γ-actinorhodin by Streptomyces coelicolor A3(2) M145 without altering the biosynthesis of the intracellular actinorhodin. A mutant of the BBc6R8 strain defective in the production of gluconic acid from glucose and consequently unable to acidify the culture medium did not show any effect on the γ-actinorhodin biosynthesis in contrast to the wild-type strain and the mutant complemented with the wild-type allele. In addition, when glucose was substituted by mannitol in the culture medium, P. fluorescens BBc6R8 was unable to acidify the medium and to prevent the biosynthesis of the antibiotic. All together, the results show that P. fluorescens BBc6R8 impairs the biosynthesis of the lactone form of actinorhodin in S. coelicolor by acidifying the medium through the production of gluconic acid. Other fluorescent Pseudomonas and the opportunistic pathogen Pseudomonas aeruginosa PAO1 also prevented the γ-actinorhodin production in a similar way. We propose some hypotheses on the ecological significance of such interaction.

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References

  • Bailey MJ, Lilley AK, Thompson IP et al (1995) Site directed chromosomal marking of a fluorescent pseudomonad isolated from the phytosphere of sugar beet; stability and potential for marker gene transfer. Mol Ecol 4:755–763

    Article  CAS  PubMed  Google Scholar 

  • Barker WW, Welch SA, Banfield JF (1997) Biogeochemical weathering of silicate minerals. Rev Mineral Geochem 35:391–428

    CAS  Google Scholar 

  • Bechet M, Blondeau R (1998) Iron deficiency-induced tetracycline production in submerged cultures by Streptomyces aureofaciens. J Appl Microbiol 84:889–894

    Article  CAS  PubMed  Google Scholar 

  • Brockmann H, Hieronymus E (1955) Über Actinomycetenfarbstoffe, V. Mitteil. 1): Zur Konstitution des Actinorhodins, III. Mitteil1). Chem Ber 88:1379–1390

    Article  CAS  Google Scholar 

  • Bystrykh LV, Fernandez-Moreno MA, Herrema JK et al (1996) Production of actinorhodin-related “blue pigments” by Streptomyces coelicolor A3(2). J Bacteriol 178:2238–2244

    CAS  PubMed Central  PubMed  Google Scholar 

  • Challis GL (2014) Exploitation of the Streptomyces coelicolor A3(2) genome sequence for discovery of new natural products and biosynthetic pathways. J Ind Microbiol Biotechnol 41:219–232

    Article  CAS  PubMed  Google Scholar 

  • Chater KF (2010) Bacterial extracellular biology. FEMS Microbiol Rev 34:87–88

    Article  CAS  PubMed  Google Scholar 

  • Coisne S, Béchet M, Blondeau R (1999) Actinorhodin production by Streptomyces coelicolor A3(2) in iron-restricted media. Lett Appl Microbiol 28:199–202

    Article  CAS  PubMed  Google Scholar 

  • Compeau G, Al-Achi BJ, Platsouka E, Levy SB (1988) Survival of rifampin-resistant mutants of Pseudomonas fluorescens and Pseudomonas putida in soil systems. Appl Environ Microbiol 54:2432–2438

    CAS  PubMed Central  PubMed  Google Scholar 

  • Davies J (2006) Are antibiotics naturally antibiotics? J Ind Microbiol Biotechnol 33:496–499

    Article  CAS  PubMed  Google Scholar 

  • Davies J (2013) Specialized microbial metabolites: functions and origins. J Antibiot Tokyo 66:361–364

    Article  CAS  PubMed  Google Scholar 

  • de Werra P, Péchy-Tarr M, Keel C, Maurhofer M (2009) Role of gluconic acid production in the regulation of biocontrol traits of Pseudomonas fluorescens CHA0. Appl Environ Microbiol 75:4162–4174

    Article  PubMed Central  PubMed  Google Scholar 

  • Deveau A, Brulé C, Palin B et al (2010) Role of fungal trehalose and bacterial thiamine in the improved survival and growth of the ectomycorrhizal fungus Laccaria bicolor S238 N and the helper bacterium Pseudomonas fluorescens BBc6R8: role of trehalose and thiamine in mutualistic interaction. Environ Microbiol Rep 2:560–568

    Article  CAS  PubMed  Google Scholar 

  • Ditta G, Stanfield S, Corbin D, Helinski DR (1980) Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci 77:7347–7351

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Duine JA (1991) Quinoproteins: enzymes containing the quinonoid cofactor pyrroloquinoline quinone, topaquinone or tryptophan–tryptophan quinone. Eur J Biochem FEBS 200:271–284

    Article  CAS  Google Scholar 

  • Eisenberg RC, Butters SJ, Quay SC, Friedman SB (1974) Glucose uptake and phosphorylation in Pseudomonas fluorescens. J Bacteriol 120:147–153

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fender JE, Bender CM, Stella NA et al (2012) Serratia marcescens quinoprotein glucose dehydrogenase activity mediates medium acidification and inhibition of prodigiosin production by glucose. Appl Environ Microbiol 78:6225–6235

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Floriano B, Bibb M (1996) afsR is a pleiotropic but conditionally required regulatory gene for antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 21:385–396

    Article  CAS  PubMed  Google Scholar 

  • Frey-Klett P, Pierrat JC, Garbaye J (1997) Location and survival of mycorrhiza helper Pseudomonas fluorescens during establishment of ectomycorrhizal symbiosis between Laccaria bicolor and Douglas fir. Appl Environ Microbiol 63:139–144

    CAS  PubMed Central  PubMed  Google Scholar 

  • Frey-Klett P, Chavatte M, Clausse M-L et al (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol 165:317–328

    Article  PubMed  Google Scholar 

  • Geng J, Yu S-B, Wan X et al (2008) Protective action of bacterial melanin against DNA damage in full UV spectrums by a sensitive plasmid-based noncellular system. J Biochem Biophys Methods 70:1151–1155

    Article  CAS  PubMed  Google Scholar 

  • Gliese N, Khodaverdi V, Görisch H (2010) The PQQ biosynthetic operons and their transcriptional regulation in Pseudomonas aeruginosa. Arch Microbiol 192:1–14

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580

    Article  CAS  PubMed  Google Scholar 

  • Holloway BW (1955) Genetic recombination in Pseudomonas aeruginosa. J Gen Microbiol 13:572–581

    Article  CAS  PubMed  Google Scholar 

  • Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kamilova F, Kravchenko LV, Shaposhnikov AI et al (2006) Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant Microbe Interact MPMI 19:250–256

    CAS  Google Scholar 

  • Kaur R, Macleod J, Foley W, Nayudu M (2006) Gluconic acid: an antifungal agent produced by Pseudomonas species in biological control of take-all. Phytochemistry 67:595–604

    Article  CAS  PubMed  Google Scholar 

  • Kieser T, Bibb MJ, Buttner MJ et al (2000) Practical streptomyces genetics. John Innes Fundation, Norwich, UK

    Google Scholar 

  • Kim Y, Bae B, Choung Y (2005) Optimization of biological phosphorus removal from contaminated sediments with phosphate-solubilizing microorganisms. J Biosci Bioeng 99:23–29

    Article  CAS  PubMed  Google Scholar 

  • Kovach ME, Elzer PH, Steven Hill D et al (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175–176

    Article  CAS  PubMed  Google Scholar 

  • Kraemer SM (2004) Iron oxide dissolution and solubility in the presence of siderophores. Aquat Sci Res Bound 66:3–18

    Article  CAS  Google Scholar 

  • Loper JE, Henkels MD (1999) Utilization of heterologous siderophores enhances levels of iron available to Pseudomonas putida in the rhizosphere. Appl Environ Microbiol 65:5357–5363

    CAS  PubMed Central  PubMed  Google Scholar 

  • McCarthy AJ, Williams ST (1992) Actinomycetes as agents of biodegradation in the environment—a review. Gene 115:189–192

    Article  CAS  PubMed  Google Scholar 

  • Miller SH, Browne P, Prigent-Combaret C et al (2010) Biochemical and genomic comparison of inorganic phosphate solubilization in Pseudomonas species. Environ Microbiol Rep 2:403–411

    Article  CAS  PubMed  Google Scholar 

  • Mueller KE, Eissenstat DM, Hobbie SE et al (2012) Tree species effects on coupled cycles of carbon, nitrogen, and acidity in mineral soils at a common garden experiment. Biogeochemistry 111:601–614

    Article  CAS  Google Scholar 

  • O’Brien J, Wright GD (2011) An ecological perspective of microbial secondary metabolism. Curr Opin Biotechnol 22:552–558

    Article  PubMed  Google Scholar 

  • Ochi K, Hosaka T (2013) New strategies for drug discovery: activation of silent or weakly expressed microbial gene clusters. Appl Microbiol Biotechnol 97:87–98

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Onaka H, Mori Y, Igarashi Y, Furumai T (2011) Mycolic acid-containing bacteria induce natural-product biosynthesis in Streptomyces Species. Appl Environ Microbiol 77:400–406

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Perez J, Munoz-Dorado J, Brana AF et al (2011) Myxococcus xanthus induces actinorhodin overproduction and aerial mycelium formation by Streptomyces coelicolor. Microb Biotechnol 4:175–183

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ponraj P, Shankar M, Ilakkiam D et al (2013) Influence of periplasmic oxidation of glucose on pyoverdine synthesis in Pseudomonas putida S11. Appl Microbiol Biotechnol 97:5027–5041

    Article  CAS  PubMed  Google Scholar 

  • Ramette A, Frapolli M, Saux MFL et al (2011) Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2,4-diacetylphloroglucinol and pyoluteorin. Syst Appl Microbiol 34:180–188

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    Article  CAS  PubMed  Google Scholar 

  • Seipke RF, Kaltenpoth M, Hutchings MI (2012) Streptomyces as symbionts: an emerging and widespread theme? Fems Microbiol Rev 36:862–876

    Article  CAS  PubMed  Google Scholar 

  • Sverdrup H, Warfvinge P (1995) Estimating field weathering rates using laboratory kinetics. Rev Mineral Geochem 31:485–541

    CAS  Google Scholar 

  • Traxler MF, Watrous JD, Alexandrov T et al (2013) Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. mBio 4:e00459–13

    Article  PubMed Central  PubMed  Google Scholar 

  • Uroz S, Calvaruso C, Turpault MP et al (2007) Effect of the mycorrhizosphere on the genotypic and metabolic diversity of the bacterial communities involved in mineral weathering in a forest soil. Appl Environ Microbiol 73:3019–3027

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Uroz S, Calvaruso C, Turpault MP et al (2009a) Efficient mineral weathering is a distinctive functional trait of the bacterial genus Collimonas. Soil Biol Biochem 41:2178–2186

    Article  CAS  Google Scholar 

  • Uroz S, Calvaruso C, Turpault M-P, Frey-Klett P (2009b) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–387

    Article  CAS  PubMed  Google Scholar 

  • Uroz S, Oger P, Lepleux C et al (2011) Bacterial weathering and its contribution to nutrient cycling in temperate forest ecosystems. Res Microbiol 162:820–831

    Article  CAS  PubMed  Google Scholar 

  • Watrous J, Roach P, Alexandrov T et al (2012) Mass spectral molecular networking of living microbial colonies. Proc Natl Acad Sci 109:E1743–E1752

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Welch SA, Taunton AE, Banfield JF (2002) Effect of microorganisms and microbial metabolites on apatite dissolution. Geomicrobiol J 19:343–367

    Article  CAS  Google Scholar 

  • Wright LF, Hopwood DA (1976) Actinorhodin is a chromosomally-determined antibiotic in Streptomyces coelicolor A3(2). J Gen Microbiol 96:289–297

    Article  CAS  PubMed  Google Scholar 

  • Yang Y-L, Xu Y, Straight P, Dorrestein PC (2009) Translating metabolic exchange with imaging mass spectrometry. Nat Chem Biol 5:885–887

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yim G, Wang HH, Davies J (2007) Antibiotics as signalling molecules. Philos Trans R Soc Lond B Biol Sci 362:1195–1200

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu H, Sandiford SK, van Wezel GP (2014) Triggers and cues that activate antibiotic production by actinomycetes. J Ind Microbiol Biotechnol 41:371–386

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was founded by the French National Research Agency through the Laboratory of Excellence ARBRE (ANR-11-LABX-0002-01), by the French National Institute for Agricultural Research (INRA) and Région Lorraine. JG was supported by a CJS (Contrat Jeune Scientifique) Grant from INRA. We thank Jean-Selim Medot for his help in this work.

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Correspondence to Bertrand Aigle.

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Communicated by Matthias Boll.

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Galet, J., Deveau, A., Hôtel, L. et al. Gluconic acid-producing Pseudomonas sp. prevent γ-actinorhodin biosynthesis by Streptomyces coelicolor A3(2). Arch Microbiol 196, 619–627 (2014). https://doi.org/10.1007/s00203-014-1000-4

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