Skip to main content

Advertisement

SpringerLink
Log in

Suboptimal growth temperatures enhance the biological activity of cultured cyanobacterium Gloeocapsa sp.

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The cytotoxic, antibacterial, and antifungal activities of cyanobacterium Gloeocapsa sp. strain Gacheva 2007/R-06/1 were investigated and the possibility for an enhancement of these activities by changing the culture conditions evaluated. Fatty acids of this cyanobacterium were found to be active against Streptococcus pyogenes. Exopolysaccharides inhibited the growth of both Gram-positive and Gram-negative bacteria and the fungus Candida albicans. Both exopolysaccharides and fatty acid mixtures also significantly decreased the viability of human cervical carcinoma cells, HeLa. Greater biological activities were exhibited by Gloeocapsa sp., cultured at suboptimal temperatures (15–26°C) than at optimal and supraoptimal ones. In comparison with higher light intensity, the low-light cultivation stimulated the cytotoxicity of the fatty acids. In general, low temperatures decreased the growth of Gloeocapsa sp., but promoted its biological activity. Prolonged cultivation also had a beneficial impact on the bioactivity. Compared to 4 days, the 17-day cultivation resulted in fourfold higher antibacterial and antifungal activities of exopolysaccharides and more than twice increases in their cytotoxicity. The study revealed that this cyanobacterial isolate is a new source of natural products with potential for pharmacological and medical applications.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aiba S, Ogawa T (1977) Assessment of growth yield of a blue-green alga Spirulina platensis in axenic and continuous culture. J Gen Microbiol 102:179–182

    Article  Google Scholar 

  • Andersen RA, Kawachi M (2005) Traditional microalgae isolation techniques. In: Andersen RA (ed) Algal culturing techniques. Elsevier, Amsterdam, pp 83–100

    Google Scholar 

  • Andrews JM (2001) Determination of minimal inhibitory concentrations. J Antimicrob Chemother 48(suppl 1):5–16

    Article  PubMed  CAS  Google Scholar 

  • Asthana RK, Srivastava A, Kayastha AM, Nath G, Singh SP (2006) Antibacterial potential of γ-linolenic acid from Fischerella sp. colonizing Neem tree bark. World J Microbiol Biotechnol 22:443–448

    Article  CAS  Google Scholar 

  • Biondi N, Tredici MR, Taton A, Wilmotte A, Hodgson DA, Losi D, Marinelli F (2008) Cyanobacteria from benthic mats of Antarctic lakes as a source of new bioactivities. J Appl Microbiol 105:105–115

    Article  PubMed  CAS  Google Scholar 

  • Borowitzka MA (1995) Microalgae as sources of pharmaceuticals and other biologically active compounds. J Appl Phycol 7:3–15

    Article  CAS  Google Scholar 

  • Bradford MA (1976) Rapid and sensitive method for the quantification of micrograms quantities of protein utilising the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Caicedo NH, Heyduck-Söller B, Fischer U, Thöming J (2011) Bioproduction of antimicrobial compounds by using marine filamentous cyanobacterium cultivation. J Appl Phycol 23:811–818

    Article  CAS  Google Scholar 

  • Chlipala G, Shunyan M, Esperanza J, de Blanco C, Ito A, Bazarek S, Orjala J (2009) Investigation of antimicrobial and protease-inhibitory activity from cultured cyanobacteria. Pharm Biol 47:53–60

    Article  PubMed  CAS  Google Scholar 

  • De Philippis R, Vincenzini M (1998) Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev 22:151–175

    Article  Google Scholar 

  • Deshmukh DV, Puranik PR (2010) Application of Plackett–Burman design to evaluate media components affecting antibacterial activity of alkaliphilic cyanobacteria isolated from Lonar Lake. Turk J Biochem 35:114–120

    CAS  Google Scholar 

  • Dilov C (1985) Mass cultivation and use of microalgae. Bulgarian Academy of Science Publishing House, Sofia, pp 16–19 (in Bulgarian)

    Google Scholar 

  • Dobretsov S, Abed RMM, Al Maskari SMS, Al Sabahi JN, Victor R (2011) Cyanobacterial mats from hot springs produce antimicrobial compounds and quorum-sensing inhibitors under natural conditions. J Appl Phycol 23:983–993

    Article  CAS  Google Scholar 

  • DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugar and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Garbacki N, Gloaguen V, Damas J, Hoffmann L, Tits M, Angenot L (2000) Inhibition of croton oil-induced oedema in mice ear skin by capsular polysaccharides from cyanobacteria. Naunyn-Schmiedeberg’s Arch Pharmacol 361:460–464

    Article  CAS  Google Scholar 

  • Griffiths DJ, Saker ML (2003) The Palm Island mystery disease 20 years on: a review of research on cyanotoxin cylindrospermopsin. Inc Environ Toxicol 18:78–93

    Article  CAS  Google Scholar 

  • Hirata K, Yoshitomi S, Dwi S, Iwabe O, Mahakhant A, Polchai J, Miyamoto K (2003) Bioactivities of nostocine A produced by a freshwater cyanobacterium Nostoc spongiaforme TISTR 8169. J Biosci Bioeng 95:512–517

    PubMed  CAS  Google Scholar 

  • Hu C, Liu Y, Paulsen BS, Petersen D, Klaveness D (2003) Extracellular carbohydrate polymers from five desert soil algae with different cohesion in the stabilization of fine sand grain. Carbohydr Polym 54:33–42

    Article  CAS  Google Scholar 

  • Ikawa M (2004) Algal polyunsaturated fatty acids and effects on plankton ecology and other organisms. UNH Center Freshwater Biol Res 6(2):17–44

    Google Scholar 

  • Iliev I, Petkov G (2006) Growth, lipids and fatty acids of the desert tolerant blue-green alga Arthronema africanum. Compt Rend Acad Bulg Sci 59:1079–1082

    CAS  Google Scholar 

  • Issa AA (1999) Antibiotic production by the cyanobacteria Oscillatoria angustissima and Calothrix parietina. Environ Toxicol Pharmacol 8:33–37

    Article  PubMed  CAS  Google Scholar 

  • Kajiyama ST, Kanzaki H, Kawazu K, Kobayashi A (1998) Nostofungicidine, a antifungal lipopeptide from the field grown terrestrial blue green algae Nostoc commune. Tetrahedron Lett 39:3737–3740

    Article  CAS  Google Scholar 

  • Kumar SG, Das UN (1997) Cytotoxic action of alpha-linolenic and eicosapentaenoic acids on myeloma cells in vitro. Prostaglandins Leukot Essent Fatty Acids 56:285–293

    Article  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Levasseur M, Thompson PA, Harrison PJ (1993) Physiological acclimation of marine phytoplankton to different nitrogen sources. J Phycol 29:587–595

    Article  CAS  Google Scholar 

  • Li H, Li Z, Xiong S, Zhang H, Li N, Zhou S, Liu Y, Huang Z (2011) Pilot-scale isolation of bioactive extracellular polymeric substances from cell-free media of mass microalgal cultures using tangential-flow ultrafiltration. Process Biochem 46:1104–1109

    Article  CAS  Google Scholar 

  • Linington RG, González J, Ureña L-D, Romero LI, Ortega-Barría E, Gerwick WH (2007) Venturamides A and B: antimalarial constituents of the Panamanian marine cyanobacterium Oscillatoria sp. J Nat Prod 70:397–401

    Article  PubMed  CAS  Google Scholar 

  • Lodemel JB, Maehre HK, Winberg J-O, Olsen RL (2004) Tissue distribution, inhibition and activation of gelatinolytic activities in Atlantic cod (Gadus morhua). Comp Biochem Physiol B 137:363–371

    Article  PubMed  Google Scholar 

  • Martins RF, Ramos MF, Herfindal L, Sousa JA, Skarven K, Vasconcelos VT (2008) Antimicrobial and cytotoxic assessment of marine cyanobacteria Synechocystis and Synechococcus. Mar Drugs 6:1–11

    Article  PubMed  CAS  Google Scholar 

  • Moore RE, Patterson GML, Carmichael WW (1988) New pharmaceuticals from cultured blue-green algae. Mem Calif Acad Sci 13:143–150

    Google Scholar 

  • Mossmann T (1983) Rapid colorimetric assay of cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63

    Article  Google Scholar 

  • Mundt S, Kreitlow S, Nowotny A, Effmert U (2001) Biochemical and pharmacological investigation of selected cyanobacteria. Int J Hyg Environ Health 203:327–334

    Article  PubMed  CAS  Google Scholar 

  • Mundt S, Kreitlow S, Rolf J (2003) Fatty acids with antibacterial activity from the cyanobacterium Oscillatoria redekei HBU 051. J Appl Phycol 15:263–267

    Article  CAS  Google Scholar 

  • Noaman NH, Fattah A, Khaleafa M, Zaky SH (2004) Factors affecting antimicrobial activity of Synechococcus leopoliensis. Microbiol Res 159:395–402

    Article  PubMed  CAS  Google Scholar 

  • Noda K, Ohno N, Tanaka K, Okuda M, Yadomae T, Nomoto K, Shoyama Y (1998) A new type of biological response modifier from Chlorella vulgaris which needs protein moiety to show an antitumour activity. Phytother Res 12:309–319

    Article  CAS  Google Scholar 

  • Ohta S, Shiomo Y, Kawashima A, Aozasa O, Teruyuki N (1995) Antibiotic effect of linolenic acid from the Chlorococcum strain HS-101 and Dunaliella primolecta on methicillin-resistant Staphylococcus aureus. J Appl Phycol 7:121–127

    Article  CAS  Google Scholar 

  • Patterson GML, Baker KK, Baldwin CL, Bolis ChM, Caplan FR, Larsen LK, Levine IA, Moore RE, Nelson CS, Tschappat KD, Tuang GD, Boyd MR, Cardellina JH, Collins RP, Gustafson KR, Snader KM, Weislow OS, Lewin RA (1993) Antiviral activity of cultured blue-green algae (Cyanophyta). J Phycol 29:125–130

    Article  Google Scholar 

  • Prasanna R, Nain L, Tripathi R, Gupta V, Chaudhary V, Middha S, Joshi M, Ancha R, Kaushik BD (2008) Evaluation of fungicidal activity of extracellular filtrates of cyanobacteria—possible role of hydrolytic enzymes. J Basic Microbiol 48:186–194

    Article  PubMed  CAS  Google Scholar 

  • Preubel K, Wessel G, Fastner J, Chorus I (2009) Response of cylindrospermopsin production and release in Aphanizomenon flos-aquae (Cyanobacteria) to varying light and temperature conditions. Harmful Algae 8:645–650

    Article  Google Scholar 

  • Pugh N, Ross SA, ElSohly HN, ElSohly MA, Pasco DS (2001) Isolation of three high molecular weight polysaccharide preparations with potent immunostimulatory activity from Spirulina platensis, Aphanizomenon flos-aquae and Chlorella pyrenoidosa. Plant Med 67:737–742

    Article  CAS  Google Scholar 

  • Radhakrishnan B, Prasanna R, Jaiswal P, Nayak S, Dureja P (2009) Modulation of biocidal activity of Calothrix sp. and Anabaena sp. by environmental factors. Biologia 64:881–889

    Article  Google Scholar 

  • Raungsomboon S, Chidthaisong A, Bunnag B, Inthorn D, Harvey NW (2006) Production, composition and Pb2+ adsorption characteristics of capsular polysaccharides extracted from a cyanobacterium Gloeocapsa gelatinosa. Water Res 40:3759–3766

    Article  PubMed  CAS  Google Scholar 

  • Schaeffer DJ, Krylov VS (2000) Anti-HIV activity of extracts and compounds from algae and cyanobacteria. Ecotoxicol Environ Saf 45:208–227

    Article  PubMed  CAS  Google Scholar 

  • Scorzoni L, Benaducci T, Almeida AMF, Silva DHS, Bolzani VS, Mendes-Giannini MJS (2007) Comparative study of disk diffusion and microdilution methods for evaluation of antifungal activity of natural compounds against medical yeasts Candida spp and Cryptococcus sp. J Basic Appl Pharm Sci 28:25–34

    CAS  Google Scholar 

  • Soltani N, Zarrini G, Ghasemi Y, Shokravi Sh, Baftchechi L (2007) Characterization of a soil cyanobacterium Fischerella sp. FS 18 under NaCl stress. J Biol Sci 7:931–936

    Article  CAS  Google Scholar 

  • Song L, Sano T, Li R, Watanabe MM, Liu Y, Kaya K (1998) Microcystin production of Microcystis viridis (cyanobacteria) under different culture conditions. Phycol Res 46(Suppl):19–23

    CAS  Google Scholar 

  • Spooner FD, Sykes G (1972) Laboratory assessment of antibacterial activity. In: Norris JR, Ribbons DW (eds) Methods in microbiology 7B. Academic Press, London, pp 216–217

    Google Scholar 

  • Svircev Z, Cetojevic-Simin D, Simeunovic J, Karaman M, Stojanovic D (2008) Antibacterial, antifungal and cytotoxic activity of terrestrial cyanobacterial strains from Serbia. Sci China Ser C-Life Sci 51(10):941–947

    Article  Google Scholar 

  • Volk R-B, Furkert FH (2006) Antialgal, antibacterial and antifungal activity of two metabolites produced and excreted by cyanobacteria during growth. Microbiol Res 161:180–186

    Article  PubMed  CAS  Google Scholar 

  • Wall RS, Gyi TJ (1988) Alcian blue staining of proteoglycans in polyacrylamide gels using the “critical electrolyte concentration” approach. Anal Biochem 175:298–299

    Article  PubMed  CAS  Google Scholar 

  • Wase NV, Wright PC (2008) Systems biology of cyanobacterial secondary metabolite production and its role in drug discovery. Expert Opin Drug Discov 3:903–929

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by research grants D002-299/2008 and DMU-02/2 from the National Science Fund, Ministry of Education, Youth and Science, Bulgaria. The authors are grateful to Mrs. Iva Tsvetkova for her excellent technical assistance during antibacterial and antifungal screening.

Author information

Authors and Affiliations

  1. Department of Experimental Algology, Bulgarian Academy of Sciences, Institute of Plant Physiology and Genetics, Acad. G. Bonchev Str., Bldg 21, 1113, Sofia, Bulgaria

    Gergana Gacheva, Liliana Gigova, Natalia Ivanova & Ivan Iliev

  2. Department of Pathology, Bulgarian Academy of Sciences, Institute of Experimental Morphology, Pathology and Anthropology with a Museum, Acad. G. Bonchev Str., Bldg 25, 1113, Sofia, Bulgaria

    Reneta Toshkova & Elena Gardeva

  3. Department of Infectious Microbiology, Bulgarian Academy of Sciences, The Stephan Angeloff Institute of Microbiology, Acad. G. Bonchev Str., Bldg 26, 1113, Sofia, Bulgaria

    Vesselin Kussovski & Hristo Najdenski

Authors
  1. Gergana Gacheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liliana Gigova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalia Ivanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ivan Iliev
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Reneta Toshkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Elena Gardeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vesselin Kussovski
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hristo Najdenski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Liliana Gigova.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gacheva, G., Gigova, L., Ivanova, N. et al. Suboptimal growth temperatures enhance the biological activity of cultured cyanobacterium Gloeocapsa sp.. J Appl Phycol 25, 183–194 (2013). https://doi.org/10.1007/s10811-012-9852-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-012-9852-y

Keywords

Search

Navigation