Skip to main content
SpringerLink
Log in

Overproduction and biological activity of prodigiosin-like pigments from recombinant fusant of endophytic marine Streptomyces species

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Thirty-four endophytic marine Actinomycetes isolates were recovered from the Egyptian marine sponge Latrunculia corticata, out of them 5 isolates (14.7 %) showed red single colonies on yeast-CzAPEK plates. Isolates under the isolation code NRC50 and NRC51 were observed with the strongest red biomass. After application of protoplast fusion between NRC50 and NRC51 isolates, 26 fusants were selected and produced widely different amounts of prodigiosin-like pigments (PLPs) on different fermentation media. Among them fusant NRCF69 produced 79 and 160.4 % PLPs more than parental strains NRC50 and NRC51, respectively. According to the analysis of 16S rDNA sequence (amplified, sequenced, and submitted to GenBank under Accession no. JN232405 and JN232406, respectively), together with their morphological and biochemical characteristics, parental strains NRC50 (P1) and NRC51 (P2) were identified as Streptomyces sp. and designated as Streptomyces sp. NRC50 and Streptomyces sp. NRC51. This study describes a low cost, effective production media by using peanut seed broth, sunflower oil broth or dairy processing wastewater broth alone, or supplemented with 0.5 % mannitol that supports the production of PLPs by the Streptomyces fusant NRCF69 under study (42.03, 40.11, 36.7 and 47 g L−1, respectively). PLPs compounds exhibited significant cytotoxic activities against three human cancer cell lines: colon cancer cell line (HCT-116), liver cancer cell line (HEPG-2) and breast cancer cell line (MCF-7) and antimycotic activity against clinical dermatophyte isolates of Trichophyton, Microsporum and Epidermophyton.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alihosseini F, Ju KS, Lango J, Hammock BD, Sun G (2008) Antibacterial colorants: characterization of prodiginines and their applications on textile materials. Biotechnol Prog 24:742–747

    Article  PubMed  CAS  Google Scholar 

  • Anne J, Van Melleart L, Eyssen H (1990) Optimal condition for efficient transformation of S. venezuelae protoplasts. Appl Microbiol Biotechnol 32:431–435

    Article  PubMed  CAS  Google Scholar 

  • Baltz RH (1978) Genetic recombination in S. fradiae by protoplast fusion and cell regeneration. J Gen Microbiol 107:93–102

    Article  PubMed  CAS  Google Scholar 

  • Baltz RH (2001) Genetic methods and strategies for secondary metabolite yield improvement in actinomycetes. Antonie Van Leeuwenhoek 79:251–259

    Article  PubMed  CAS  Google Scholar 

  • Baltz RH, Matsushima P (1981) Protoplast fusion in Streptomyces: conditions for efficient genetic recombination and cell regeneration. J Gen Microbiol 127:137–146

    PubMed  CAS  Google Scholar 

  • Butte W (1983) Rapid method for the determination of fatty acid profiles from fats and oils using trimethylsulphonium hydroxide for transesterification. J Chromatogr 261:142–145

    Article  CAS  Google Scholar 

  • Cappuccino JG, Sherman N (1999) Microbiology: a laboratory manual, 4th edn. Addison Wesley Longman Inc., Harlow, pp 199–204

  • Casullo de Araújo HW, Fukushima K, Takaki GMC (2010) Prodigiosin production by Serratia marcescens UCP 1549 using renewable-resources as a low cost substrate. Molecules 15:6931–6940

    Article  Google Scholar 

  • Cerdeño AM, Bibb MJ, Challis GL (2001) Analysis of the prodiginine biosynthesis gene cluster of Streptomyces coelicolor A3: new mechanisms for chain initiation and termination in modular multienzymes. Chem Biol 8:817–829

    Article  PubMed  Google Scholar 

  • Demain AL (1995) Why do microorganisms produce antimicrobials. In : Hunter PA, Darby GK, Russell NJ (eds) In fifty years of antimicrobials: past perspectives and future trends. Society for General Microbiology, Cambridge, pp 205–228

  • El-Bondkly AM, El-Gendy MMA (2010) Keratinolytic activity from new recombinant fusant AYA2000, an endophytic Micromonospora sp. Can J Microbiol 56:748–760

    Article  PubMed  CAS  Google Scholar 

  • El-Gendy MMA (2010a) Optimization of process parameters for keratinase produced by endophytic Penicillium sp. Morsy1 under solid state fermentation. Appl Biochem Biotechnol 162:780–794

    Article  PubMed  CAS  Google Scholar 

  • El-Gendy MMA (2010b) In vitro, evaluation of medicinal activity of Egyptian honey from different floral sources as anticancer and antimycotic infective agents. J Microbial Biochem Technol 2(5):118–123

    Article  Google Scholar 

  • El-Gendy MMA, El-Bondkly AM (2011) Genome shuffling of marine derived bacterium Nocardia sp. ALAA 2000 for improved ayamycin production. Antonie Van Leeuwenhoek 99:773–780

    Article  PubMed  CAS  Google Scholar 

  • Feitelson JS, Malpartida F, Hopwood DA (1985) Genetic and biochemical characterization of the red gene cluster of Streptomyces coelicolor A3. J Gen Microbiol 131:2431–2441

    PubMed  CAS  Google Scholar 

  • Gerber NN (1975) Prodigiosin like pigments. CRC Crit Rev Microbiol 3:469–485

    Article  PubMed  CAS  Google Scholar 

  • Gerber N, McInnes A, Smith D, Walter J, Wright J, Vining L (1978) Biosynthesis of prodiginines. 13C assignments and enrichment patterns in nonyl-, cyclononyl-, methylcyclodecyl and butylcycloheptylprodiginine produced by actinomycete cultures supplemented with 13C labeled acetate and 15N-labeled nitrate. Can J Chem 56:1155–1163

    Article  CAS  Google Scholar 

  • Giri AV, Anandkumar N, Muthukumaran G, Pennathur G (2004) A novel medium for the enhanced cell growth and production of prodigiosin from Serratia marcescens isolated from soil. BMC Microbiol 4:1–10

    Article  Google Scholar 

  • Hasegawa T, Takizawa M, Tanida S (1983) A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 29:319–322

    Article  CAS  Google Scholar 

  • Hayakawa Y, Kawakami K, Seto H, Furihata K (1992) Structure of a new antibiotic, roseophilin. Tetrahedron Lett 33:2701–2704

    Article  Google Scholar 

  • Hewitt W, Vincent S (1989) The agar diffusion assay. In: Theory and application of microbiological assay. Academic press, New York, pp 38–79

  • Hopwood DA, Bibb MJ, Chater KF, Kieser T, Bruton CJ, Kieser THM, Lydiate DJ, Smith CP, Ward JM, Schrempf H (1985) Genetic manipulation of Streptomyces: a laboratory manual. The John Innes Foundation, Norwich

    Google Scholar 

  • Jiang Y, Tang SK, Wiese J, Xu LH, Imhoff JF, Jiang CL (2007) Streptomyces hainanensis sp. nov., a novel member of the genus Streptomyces. Int J Syst Evol Microbiol 57:2694–2698

    Article  PubMed  CAS  Google Scholar 

  • Kojiri K, Nakajima S, Suzuki H, Okura A, Suda H (1993) A new antitumor substance, Be-18591, produced by a streptomycete. 1. Fermentation, isolation, physicochemical and biological properties. J Antibiot 46:1799–1803

    Article  PubMed  CAS  Google Scholar 

  • Lane DL (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175

    Google Scholar 

  • Lavermicocca P, Valerio F, Visconti A (2003) Antifungal activity of phenyl lactic acid against molds isolated from bakery products. Appl Environ Microbiol 69:634–640

    Article  PubMed  CAS  Google Scholar 

  • Lechevalier MP, De Bie`vre C, Lechevalier HA (1977) Chemotaxonomy of aerobic actinomycetes: phospholipid composition. Biochem Syst Ecol 5:249–260

    Article  CAS  Google Scholar 

  • Liu R, Cui CB, Duan L, Gu QQ, Zhu WM (2005) Potent in vitro anticancer activity of metacycloprodigiosin and undecylprodigiosin from a sponge-derived actinomycete Saccharopolyspora sp. nov. Arch Pharm Res 28(12):1341–1344

    Article  PubMed  CAS  Google Scholar 

  • Llagostera E, Soto-Cerrato V, Montaner B, Pérez-Tomás R (2003) Prodigiosin induces apoptosis by acting on mitochondria in human lung cancer cells. Ann NY Acad Sci 1010:178–181

    Article  PubMed  CAS  Google Scholar 

  • Mandel M, Marmur J (1968) Use of ultraviolet absorbance–temperature profile for determining the guanine plus cytosine content of DNA. Methods Enzymol 12B:195–206

    Article  Google Scholar 

  • Manfio GP, Zakrzewska-Czerwinska J, Atalan E, Goodfellow M (1995) Towards minimal standards for the description of Streptomyces species. Bioteknologia 7–8:242–253

    Google Scholar 

  • Minnikin DE, Patel PV, Alshamaony L, Goodfellow M (1977) Polar lipid composition in the classification of Streptomyces and related bacteria. Int J Syst Bacteriol 27:104–117

    Article  CAS  Google Scholar 

  • Morrison DA (1966) Prodigiosin synthesis in mutants of Serratia marcesens. J Bacteriol 91:1599–1604

    PubMed  CAS  Google Scholar 

  • Nobutaka S, Masami N, Kazuyuki H, Tadaaki H, Katsumi A (2001) Synergistic antifungal activity of chitinolytic enzymes and prodigiosin produced by biocontrol bacterium, Serratia marcescens strain B2 against gray mold pathogen, Botrytis cinerea. J Gen Plant Pathol 67:312–319

    Article  Google Scholar 

  • Omar S, Khaled H, Gaafar R, Zekry AR, Eissa S, El-Khatib O (2003) Breast cancer in Egypt: a review of disease presentation and detection strategies. East Mediterr Health J 9(3):448–463

    PubMed  CAS  Google Scholar 

  • Pérez-Tomás R, Montaner B, Llagostera E, Soto-Cerrato V (2003) The prodigiosins, proapoptotic drugs with anticancer properties. Biochem Pharmacol 66:1447–1452

    Article  PubMed  Google Scholar 

  • Saleh MA, Mahmood UF (2004) Anaerobic digestion technology for industrial wastewater treatment. In: Eighth international water technology conference, IWTC8, Alexandria, Egypt, p 817

  • Seif H, Moursy A (2001) Treatment of slaughterhouse wastes. In: Sixth international water technology conference, IWTC, Alexandria, Egypt

  • Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

    Article  Google Scholar 

  • Sikyta B (1995) Genetics and selection of industrial microorganisms. In: Progress in industrial microbiology: technique in applied microbiology, vol 31. Elsevier, Amsterdam, pp 286–288

  • Solé M, Francia A, Rius N, Lorén JG (1997) The role of pH in the glucose effect on prodigiosin production by non-proliferating cells of Serratia marcescens. Lett Appl Microbiol 25:81–84

    Article  Google Scholar 

  • Soliman AS, Bondy ML, Raouf AA, Makram MA, Johnston DA, Levin B (1999) Cancer mortality in Menofeia, Egypt: comparison with US mortality rates. Cancer Causes Control 10(5):349–354

    Article  PubMed  CAS  Google Scholar 

  • Szabo IM, Marton M, Buti I, Fermandez C (1975) A diagnostic key for the identification of species of Streptomyces and Streptoverticillium included in the International Streptomyces Project. Acta Bot Acad Sci Hung 21:387–418

    Google Scholar 

  • Taechowisan T, Peberdy JF, Lumyong S (2003) Isolation of endophytic actinomycetes from selected plants and their antifungal activity. World J Microbiol Biotechnol 19(4):381–385

    Article  CAS  Google Scholar 

  • Tsao S-W, Rudd BAM, Het X-G, Chang C-J, Floss HG (2005) Identification of red pigment from Streptomyces coelicolor A3 (2) as a mixture of prodigiosin derivatives. Arch Pharm Res 28(12):1341–1344

    Article  Google Scholar 

  • Venil CK, Lakshmanaperumalsamy P, Thayalakumaran N, Bhamidimarri R, Bickers PO (2009) An insightful overview on microbial pigment, prodigiosin. Electron J Biol 5(3):49–61

    Google Scholar 

  • Williams ST, Goodfellow M, Alderson G (1989) Genus Streptomyces Waksman and Henrici 1943, 339AL. In: Williams ST, Sharpe ME and Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 4. Williams & Wilkins, Baltimore, pp 2452–2504

  • Yang SS, Kao CY (1991) Oxytetracycline production in solid state and submerged fermentation by protoplast fusants of S. rimosus. Proc Natl Sci Counc Part 1 Repub China 15:20–27

    CAS  Google Scholar 

  • Zhang J, Shen Y, Liu J, Wei D (2005) Antimetastatic effect of prodigiosin through inhibition of tumor invasion. Biochem Pharmacol 69:407–414

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Genetics and Cytology, National Research Centre, Dokki, Giza, Egypt

    Ahmed M. A. El-Bondkly

  2. Department of Chemistry of Natural and Microbial Products, National Research Centre, Dokki, Giza, Egypt

    Mervat M. A. El-Gendy

  3. Department of Medical Microbiology and Immunology, Faculty of Medicine, Fayoum University, Fayoum, Egypt

    Rasha H. Bassyouni

Authors
  1. Ahmed M. A. El-Bondkly
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mervat M. A. El-Gendy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rasha H. Bassyouni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rasha H. Bassyouni.

Rights and permissions

Reprints and permissions

About this article

Cite this article

El-Bondkly, A.M.A., El-Gendy, M.M.A. & Bassyouni, R.H. Overproduction and biological activity of prodigiosin-like pigments from recombinant fusant of endophytic marine Streptomyces species. Antonie van Leeuwenhoek 102, 719–734 (2012). https://doi.org/10.1007/s10482-012-9772-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-012-9772-5

Keywords

Search

Navigation