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Elicitation of Streptomyces coelicolor with dead cells of Bacillus subtilis and Staphylococcus aureus in a bioreactor increases production of undecylprodigiosin

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Abstract

Since microorganisms normally co-exist with other species in nature, they have developed complex metabolic and physiological responses as a result of such interspecies interactions. We utilized some of these interactions by introducing heat-killed cells of Bacillus subtilis and Staphylococcus aureus to Streptomyces coelicolor cultures and, as a result, stimulated undecylprodigiosin production. Undecylprodigiosin is not only an antibiotic; it has also been attributed with antitumor activities, but, in a defined medium, pure cultures of S. coelicolor produced only low concentrations. Elicitation with B. subtilis increased the maximum undecylprodigiosin concentration by threefold and S. aureus by fivefold compared with the pure culture of S. coelicolor. Growth and glucose consumption of elicited S. coelicolor, however, remained similar to those observed in the pure culture. Furthermore, another positive outcome of the elicitation with both B. subtilis and S. aureus was the earlier onset of undecylprodigiosin production by 24 h compared with the pure culture of S. coelicolor. This is the first time that such a phenomenon has been seen in 2L bioreactors. Our work supports the use of biotic elicitation in order to enhance the production of secondary metabolites for industrial-scale applications.

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References

  • Ariyo TA, Bucke C, Keshavarz T (1997) Alginate oligosaccharides as enhancers of penicillin production in cultures of Penicillium chrysogenum. Biotech Bioeng 53:17–20

    Article  CAS  Google Scholar 

  • Asilonu E, Bucke C, Keshavarz T (2000) Enhancement of chrysogenin production in cultures of Penicillium chrysogenum by uronic acid oligosaccharides. Biotechnol Lett 22:931–936

    Article  CAS  Google Scholar 

  • Bibb M (1996) The regulation of antibiotic production in Streptomyces coelicolor A3(2). Microbiology-UK 142:1335–1344

    Article  CAS  Google Scholar 

  • Chio SU, Lee CK, Hwang YI, Kinoshita HT (2004) Inter generic conjugal transfer of plasmid DNA from Escherichia coli to Kitasatospora setae, a bafilomycin B-1 producer. Arch Microbiol 181(4):294–298

    Article  Google Scholar 

  • Elibol M, Ulgen K, Kamaruddin K, Mavituna F (1995) Effect of inoculum type on actinorhodin production by Streptomyces coelicolor A3(2). Biotechnol Lett 17(6):579–582

    Article  CAS  Google Scholar 

  • Feng JS, Qian H, Tsang JC (1982) Separation and detection of monopyrrole and bipyrrole precursors of prodigiosin from Serratia marcescence by a combined method of high performance liquid chromatography and syntrophic pigment synthesis. J Liq Chrom 5:1329–1340

    Article  CAS  Google Scholar 

  • Genigeorgis CA (1989) Present state of knowledge on staphylococcal intoxication. Int J Food Microbiol 9:327–360

    Article  CAS  Google Scholar 

  • Gundogan N, Citak S, Yucel N, Devren A (2005) A note on the incidence and antibiotic resistance of Staphylococcus aureus isolated from meat and chicken samples. Meat Science 69:807–810

    Article  CAS  Google Scholar 

  • Ho TF, Ma CJ, Lu CH, Tsai YT, Wei YH, Chang JS, Lai JK, Cheuh PJ, Yeh CT, Tang PC, Chang JT, Ko JL, Liu FS, Yen HE, Chang CC (2007) Undecylprodigiosin selectively induces apoptosis in human breast carcinoma cells independent of p53. Toxicol Appl Pharmacol 225(3):318–328

    Article  CAS  Google Scholar 

  • Hobbs G, Frazer CM, Gardner DCJ, Cullum JA, Oliver SG (1989) Dispersed growth of Streptomyces in liquid culture. Appl Microbiol Biotechnol 31(3):272–277

    Article  CAS  Google Scholar 

  • Jung HY, Kang SM, Kang YM, Kang MJ, Yun DJ, Bahk JD, Yang JK, Choi MS (2003) Enhanced production of scopolamine by bacterial elicitors in adventitious hairy root cultures of Scopolia parviflora. Enzym Microb Tech 33(7):987–990

    Article  CAS  Google Scholar 

  • Kang SG, Jin W, Bibb M, Lee KJ (1998) Actinorhodin and undecylprodigiosin production in wild-type and relA mutant strains of Streptomyces coelicolor A3(2) grown in continuous culture. FEMS Microbiol Lett 168:221–226

    Article  CAS  Google Scholar 

  • Kim HB, Smith CP, Micklefield J, Mavituna F (2004) Metabolic flux analysis for calcium-dependent antibiotic (CDA) production in Streptomyces coelicolor. Metab Eng 6:313–325

    Article  CAS  Google Scholar 

  • Luti KJK, Mavituna F (2010) Streptomyces coelicolor increases the production of undecylprodigiosin when interacted with Bacillus subtilis. Biotechnol Lett. doi:10.1007/s10529-010-0401-y

    Google Scholar 

  • Mearns-Spragg A, Bregu M, Boyd KG, Burgess JG (1998) Cross-species induction and enhancement of antimicrobial activity produced by epibiotic bacteria from marine algae and invertebrates after exposure to terrestrial bacteria. Lett Appl Microbiol 27:142–146

    Article  CAS  Google Scholar 

  • Murphy T, Parra P, Radman R, Roy I, Harrop A, Dixon K, Keshavarz T (2007) Novel application of oligosaccharides as elicitors for the enhancement of bacitracin A production in cultures of Bacillus licheniformis. Enzym Microb Tech 40:1518–1523

    Article  CAS  Google Scholar 

  • Oh DC, Jensen PR, Kauffman CA, Fenical W (2005) Libertellenones A-D: induction of cytotoxic ditrerpenoid biosynthesis by marine competition. Bioorg Med Chem 13(17):5267–5273

    Article  CAS  Google Scholar 

  • Peterson SB, Dunn AK, Klimowicz AK, Handelsman J (2006) Peptidoglycan from Bacillus cereus mediates commensalism with rhizosphere bacteria from the Cytophaga–Flavobacterium group. Appl Environ Microbiol 72:5421

    Article  CAS  Google Scholar 

  • Radman R, Saez T, Bucke C, Keshavarz T (2003) Elicitation of plants and microbial cell systems. Biotechnol Appl Biochem 37:91–102

    Article  CAS  Google Scholar 

  • Rasool KA, Wimpenny JWT (1982) Mixed continuous culture experiments with an antibiotic-producing streptomycete and Escherichia coli. Microb Ecol 8:267–277

    Article  Google Scholar 

  • Rigali S, Titgemeyer F, Barends S (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Reports 9:670–675

    Article  CAS  Google Scholar 

  • Rjazantseva IN, Andreeva IN, Ogorodnikova TI (1994) Effect of various growth—conditions on pigmentation of Serratia. Microbios 79:155–161

    CAS  Google Scholar 

  • Sevcikova B, Kormanec J (2004) Differential production of two antibiotics of Streptomyces coelicolor A3(2), actinorhodin and undecylprodigiosin, upon salt stress conditions. Arch Microbiol 181(5):384–389

    Article  CAS  Google Scholar 

  • Straight PD, Willy JM, Kotler R (2006) Inetractions between Streptomyces coelicolor and Bacillus subtilis: role of surfactants in rising aerial structurees. J Bact 188(13):4918–4925

    Article  CAS  Google Scholar 

  • Suvarnalatha G, Rajendran L, Ravishankar GA, Venkataraman LV (1994) Elicitation of anthocyanin production in cell cultures of carrot (Daucus carota L.) by using elicitors and abiotic stress. Biotechnol Lett 16:1275–1280

    CAS  Google Scholar 

  • Takano E, Gramajo HC, Strauch E, Andres N, White J, Bibb MJ (1992) Transcriptional regulation of the redD transcriptional activator gene accounts for growth-phase-dependent production of the antibiotic undecylprodigiosin in Streptomyces coelicolor A3(2). Mol Microbiol 6(19):2797–2804

    Article  CAS  Google Scholar 

  • Val G, Marín S, Mellado RP (2009) A sensitive method to monitor Bacillus subtilis and Streptomyces coelicor-related bacteria in maize rhizobacterial communities: the use of genome-wide microarrays. Microb Ecol 58:108–115

    Article  Google Scholar 

  • Wei YH, Chen WC (2005) Enhanced production of prodigiosin-like pigment from Serratia marcescens SM Delta R by medium improvement and oil-supplementation strategies. J Biosci Bioeng 99:616–622

    Article  CAS  Google Scholar 

  • Wei YH, Yu WJ, Chen WC (2005) Enhanced undecylprodigiosin production from Serratia marcescens SS-1 by medium formulation and amino-acid supplementation. J Biosci Bioeng 100:466–471

    Article  CAS  Google Scholar 

  • White J, Bibb M (1997) bldA dependence of undecylprodigiosin production in Streptomyces coelicolor A3(2) involves a pathway-specific regulatory cascade. J Bact 197(3):627–633

    Google Scholar 

  • Williamson NR, Fineran PC, Leeper FJ, Salmond GPC (2006) The biosynthesis and regulation of bacterial prodiginines. Nat Rev Microbiol 4(12):887–899

    Article  CAS  Google Scholar 

  • Zhao JL, Zhou LG, Wu JY (2010) Effect of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl Microbiol Biotechnol 87:137–144

    Article  CAS  Google Scholar 

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Acknowledgments

We would like to acknowledge the financial support from the Ministry of Higher Education and Scientific Research of Iraq for Khalid Jaber Kadhum Luti.

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Correspondence to Ferda Mavituna.

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Luti, K.J.K., Mavituna, F. Elicitation of Streptomyces coelicolor with dead cells of Bacillus subtilis and Staphylococcus aureus in a bioreactor increases production of undecylprodigiosin. Appl Microbiol Biotechnol 90, 461–466 (2011). https://doi.org/10.1007/s00253-010-3032-2

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  • DOI: https://doi.org/10.1007/s00253-010-3032-2

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