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Antimycobacterial activity in vitro of pigments isolated from Antarctic bacteria

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Abstract

In this study, we describe the antimycobacterial activity of two pigments, violacein, a purple violet pigment from Janthinobacterium sp. Ant5-2 (J-PVP), and flexirubin, a yellow-orange pigment from Flavobacterium sp. Ant342 (F-YOP). These pigments were isolated from bacterial strains found in the land-locked freshwater lakes of Schirmacher Oasis, East Antarctica. The minimum inhibitory concentrations (MICs) of these pigments for avirulent and virulent mycobacteria were determined by the microplate Alamar Blue Assay (MABA) and Nitrate Reductase Assay (NRA). Results indicated that the MICs of J-PVP and F-YOP were 8.6 and 3.6 μg/ml for avirulent Mycobacterium smegmatis mc2155; 5 and 2.6 μg/ml for avirulent Mycobacterium tuberculosis mc26230; and 34.4 and 10.8 μg/ml for virulent M. tuberculosis H37Rv, respectively. J-PVP exhibited a ~15 times lower MIC for Mycobacterium sp. than previously reported for violacein pigment from Chromobacterium violaceum, while the antimycobacterial effect of F-YOP remains undocumented. Our results indicate these pigments isolated from Antarctic bacteria might be valuable lead compounds for new antimycobacterial drugs used for chemotherapy of tuberculosis.

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References

  • Achenbach H, Kohl W, Wachter W, Reichenbach H (1978) Investigations of the pigments from Cytophaga johnsonae Cy jl. New flexirubin-type pigments. New flexirubin-type pigments. Arch Microbiol 117:253–257

    Article  CAS  PubMed  Google Scholar 

  • Agrawal DK, Saikia D, Tiwari R, Ojha S, Shanker K, Kumar JK, Gupta AK, Tandon S, Negi AS, Khanuja SP (2008) Demethoxycurcumin and its semisynthetic analogues as antitubercular agents. Planta Med 74:1828–1831

    Google Scholar 

  • Barry CE et al (1998) Mycolic acids: structure, biosynthesis and physiological functions. Prog Lipid Res 37:143–179

    Article  CAS  PubMed  Google Scholar 

  • Bernardet JF, Nakagawa Y, Holmes B (2002) Proposed minimal standards for describing new taxa of the family Flavobacteriaceae and emended description of the family. Int J Syst Evol Microbiol 52:1049–1070

    Article  CAS  PubMed  Google Scholar 

  • Brennan PJ, Nikaido H (1995) The envelope of mycobacteria. Annu Rev Biochem 64:29–63

    Article  CAS  PubMed  Google Scholar 

  • Bueno-Sanchez JG, Martinez-Morales JR, Stashenko EE, Ribon W (2009) Anti-tubercular activity of eleven aromatic and medicinal plants occurring in Colombia. Biomedica 29:51–60

    PubMed  Google Scholar 

  • Cavicchioli R, Siddiqui KS, Andrews D, Sowers KR (2002) Low-temperature extremophiles and their applications. Curr Opin Biotechnol 13:253–261

    Article  CAS  PubMed  Google Scholar 

  • Chanwong S, Maneekarn N, Makonkawkeyoon L, Makonkawkeyoon S (2007) Intracellular growth and drug susceptibility of Mycobacterium tuberculosis in macrophages. Tuberculosis (Edinb) 87:130–133

  • Duran N, Menck CF (2001) Chromobacterium violaceum: a review of pharmacological and industrial perspectives. Crit Rev Microbiol 27:201–222

    Article  CAS  PubMed  Google Scholar 

  • Fattorini L, Migliori GB, Cassone A (2007) Extensively drug-resistant (XDR) tuberculosis: an old and new threat. Ann Ist Super Sanita 43:317–319

    Google Scholar 

  • Fautz E, Reichenbach H (1980) A simple test for flexirubin-type pigments. FEMS Microbiol Lett 8:87–91

    Article  CAS  Google Scholar 

  • Fs.No.104 (2008) WHO, pp 1–304

  • Gandhi NR, Nunn P, Dheda K, Schaaf HS, Zignol M, van Soolingen D, Jensen P, Bayona J (2010) Multidrug-resistant and extensively drug-resistant tuberculosis: a threat to global control of tuberculosis. Lancet 375:1830–1843

    Google Scholar 

  • Hoffmann C, Leis A, Niederweis M, Plitzko JM, Engelhardt H (2008) Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc Natl Acad Sci USA 105:3963–3967

    Article  CAS  PubMed  Google Scholar 

  • Kuete V, Ngameni B, Simo CC, Tankeu RK, Ngadjui BT, Meyer JJ, Lall N, Kuiate JR (2008) Antimicrobial activity of the crude extracts and compounds from Ficus chlamydocarpa and Ficus cordata (Moraceae). J Ethnopharmacol 120:17–24

  • Kuete V, Tangmouo JG, Meyer JJM, Lall N (2009) Diospyrone, crassiflorone and plumbagin: three antimycobacterial and antigonorrhoeal naphthoquinones from two Diospyros spp. Int J Antimicrob Agents 34:322–325

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Khan IA, Verma V, Kalyan N, Qazi GN (2005a) Rapid, inexpensive MIC determination of Mycobacterium tuberculosis isolates by using microplate nitrate reductase assay. Diagn Microbiol Infect Dis 53:121–124

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Khan IA, Verma V, Qazi GN (2005b) Microplate nitrate reductase assay versus Alamar Blue Assay for MIC determination of Mycobacterium tuberculosis. Int J Tuberc Lung Dis 9:939–941

    CAS  PubMed  Google Scholar 

  • Lall N, Meyer JJ (2001) Inhibition of drug-sensitive and drug-resistant strains of Mycobacterium tuberculosis by diospyrin, isolated from Euclea natalensis. J Ethnopharmacol 78:213–216

    Google Scholar 

  • Lechner D, Gibbons S, Bucar F (2008) Plant phenolic compounds as ethidium bromide efflux inhibitors in Mycobacterium smegmatis. J Antimicrob Chemother 62:345–348

    Google Scholar 

  • Li Y et al (2008) Bioactive asterric acid derivatives from the Antarctic ascomycete fungus Geomyces sp. J Nat Prod 71:1643–1646

    Article  CAS  PubMed  Google Scholar 

  • Lin YM, Flavin MT, Cassidy CS, Mar A, Chen FC (2001) Biflavonoids as novel antituberculosis agents. Bioorg Med Chem Lett 11:2101–2104

    Article  CAS  PubMed  Google Scholar 

  • Lo Giudice A, Brilli M, Bruni V, De Domenico M, Fani R, Michaud L (2007a) Bacterium-bacterium inhibitory interactions among psychrotrophic bacteria isolated from Antarctic seawater (Terra Nova Bay, Ross Sea). FEMS Microbiol Ecol 60:383–396

    Article  CAS  PubMed  Google Scholar 

  • Lo Giudice A, Bruni V, Michaud L (2007b) Characterization of Antarctic psychrotrophic bacteria with antibacterial activities against terrestrial microorganisms. J Basic Microbiol 47:496–505

    Article  CAS  PubMed  Google Scholar 

  • Mativandlela SP, Meyer JJ, Hussein AA, Houghton PJ, Hamilton CJ, Lall N (2008) Activity against Mycobacterium smegmatis and M. tuberculosis by extract of South African medicinal plants. Phytother Res 22:841–845

    Google Scholar 

  • Matz C et al (2008) Marine biofilm bacteria evade eukaryotic predation by targeted chemical defense. PLoS One 3:e2744

    Article  PubMed  Google Scholar 

  • McLean KJ, Marshall KR, Richmond A, Hunter IS, Fowler K, Kieser T, Gurcha SS, Besra GS, Munro AW (2002) Azole antifungals are potent inhibitors of cytochrome P450 mono-oxygenases and bacterial growth in mycobacteria and streptomycetes. Microbiology 148:2937–2949

    Google Scholar 

  • Melo PS, Justo GZ, de Azevedo MB, Duran N, Haun M (2003) Violacein and its beta-cyclodextrin complexes induce apoptosis and differentiation in HL60 cells. Toxicology 186:217–225

    Article  CAS  PubMed  Google Scholar 

  • Migliori GB, De Iaco G, Besozzi G, Centis R, Cirillo DM (2007) First tuberculosis cases in Italy resistant to all tested drugs. Eurosurveillance 12(20):3194

    Google Scholar 

  • Migliori GB, Sotgiu G (2010) XDR tuberculosis in South Africa: old questions, new answers. Lancet 375:1760–1761

    Google Scholar 

  • Mitscher LA, Baker W (1998) Tuberculosis: a search for novel therapy starting with natural products. Med Res Rev 18:363–374

    Article  CAS  PubMed  Google Scholar 

  • Momen AZ, Hoshino T (2000) Biosynthesis of violacein: intact incorporation of the tryptophan molecule on the oxindole side, with intramolecular rearrangement of the indole ring on the 5-hydroxyindole side. Biosci Biotechnol Biochem 64:539–549

    Article  CAS  PubMed  Google Scholar 

  • Murthy PS, Ratnakar P, Gadre DV, Talwar V, Gupta HC, Gupta RL (2008) Trifluoperazine and CEF-allicin from garlic (Allium sativum) as potential new antitubercular drugs active against drug resistant Mycobacterium tuberculosis. Ind J Clin Biochem 12:72–75

    Google Scholar 

  • Paudel B, Bhattarai HD, Lee JS, Hong SG, Shin HW, Yim JH (2008) Antibacterial potential of Antarctic lichens against human pathogenic Gram-positive bacteria. Phytother Res 22:1269–1271

    Article  CAS  PubMed  Google Scholar 

  • Raviglione MC, Smith IM (2007) XDR tuberculosis—implications for global public health. N Engl J Med 356:656–659

    Article  CAS  PubMed  Google Scholar 

  • Reichenbach H, Kleinig H (1974) The pigments of Flexibacter elegans: novel and chemosystematically useful compounds. Arch Microbiol 101:131–144

    Article  CAS  Google Scholar 

  • Rettori D, Duran N (1998) Production, extraction and purification of violacein: an antibiotic produced by Chromobacterium violaceum. World J Microbiol Biotechnol 14:685–688

    Article  CAS  Google Scholar 

  • Sajilata MG, Singhal RS, Kamat MY (2008) The carotenoid pigment zeaxanthin—a review. Compr Rev Food Sci Food Saf 7:29–49

    Article  CAS  Google Scholar 

  • Samad A, Sultana Y, Akhter MS, Aqil M (2008) Treatment of tuberculosis: use of active pharmaceuticals. Recent Pat Antiinfect Drug Discov 3:34–44

    Article  CAS  PubMed  Google Scholar 

  • Shandil RK, Jayaram R, Kaur P, Gaonkar S, Suresh BL, Mahesh BN, Jayashree R, Nandi V, Bharath S, Balasubramanian V (2007) Moxifloxacin, ofloxacin, sparfloxacin, and ciprofloxacin against Mycobacterium tuberculosis: evaluation of in vitro and pharmacodynamic indices that best predict in vivo efficacy. Antimicrob Agents Chemother 51:576-582

    Google Scholar 

  • Shiloh MU, Champion PAD (2010) To catch a killer. What can mycobacterial models teach us about Mycobacterium tuberculosis pathogenesis? Curr Opin Microbiol 13:86–92

    Article  CAS  PubMed  Google Scholar 

  • Singh JA, Upshur R, Padayatchi N (2007) XDR-TB in South Africa: no time for denial or complacency. PLoS Med 4:e50

    Article  PubMed  Google Scholar 

  • Snapper SB, Melton RE, Mustafa S, Kieser T, Jacobs WR (1990) Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol Microbiol 4:1911–1919

    Article  CAS  PubMed  Google Scholar 

  • Souza AO, Aily DCG, Sato DN, Duran N (1999) In vitro activity of violacein against Mycobacterium tuberculosis H37Ra. Rev Inst Adolfo Lutz 58:59–62

    Google Scholar 

  • Suksamrarn A, Poomsing P, Aroonrerk N, Punjanon T, Suksamrarn S, Kongkun S (2003) Antimycobacterial and antioxidant flavones from Limnophila geoffrayi. Arch Pharm Res 26:816–820

    Google Scholar 

  • Thompson BN, Hammer PE, Hill DS, Stafford J, Torkewitz N, Gaffney TD, Lam ST, Molnár I, Ligon JM (2003) 2,5-Dialkylresorcinol biosynthesis in Pseudomonas aurantiaca: novel head-to-head condensation of two fatty acid-derived precursors. J Bacteriol 185:860–869

    Article  Google Scholar 

  • Tomioka H, Namba K (2006) Development of antituberculous drugs: current status and future prospects. Kekkaku 81:753–774

    PubMed  Google Scholar 

  • Uplekar M, Lonnroth K (2007) MDR and XDR—the price of delaying engagement with all care providers for control of TB and TB/HIV. Trop Med Int Health 12:473–474

    Article  PubMed  Google Scholar 

  • Wallace RJ Jr, Bedsole G, Sumter G, Sanders CV, Steele LC, Brown BA, Smith J, Graham DR (1990) Activities of ciprofloxacin and ofloxacin against rapidly growing mycobacteria with demonstration of acquired resistance following single-drug therapy. Antimicrob Agents Chemother 34:65–70

    Google Scholar 

  • Zeng Y, Chen B, Zou Y, Zheng T (2008) Polar microorganisms, a potential source for new natural medicines—a review. Wei Sheng Wu Xue Bao 48:695–700

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Richard B. Hoover of NASA for helping with the sample collection for the Janthinobacterium strain; Dr. Venkatram R. Attigada of UAB Chemistry department for the chemical analysis of the bacterial pigments. We thank Tawani Foundation of Chicago for supporting the Tawani 2008 International Antarctic Scientific Expedition; we are grateful to Colonel (IL) J. N. Pritzker IL ARNG (Retired) for supporting the expedition. Logistical support was provided by the Arctic and Antarctic Research Institute/Russian Antarctic Expedition (AARI/RAE); Antarctic Logistics Centre International (ALCI), Cape Town, SA; Marty Kress of Von Braun Center for Science Innovation, Inc., NASA (VCSI, Inc.); Rasik Ravindra (Director) of National Center for Antarctic and Ocean Research (NCAOR); 2008–2009 Maitri staff and Cdr. Arun Chaturvedi, Cdr. Pradip Malhotra and geologist Ashit Swain; and personnel at Novolazarevskaya Station, Russia. We also thank Ed Tracy and Lisa Lanz of Tawani Foundation, and Dr. Robert Fischer of Biology, UAB for support. We also thank Dr. Daniel D. Jones for critically reviewing this manuscript and the helpful suggestions.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Biology, University of Alabama at Birmingham, 1300 University Blvd., CH251, Birmingham, AL, 35294-1170, USA

    Nazia Mojib, Rachel Philpott, Jonathan P. Huang & Asim K. Bej

  2. Department of Microbiology, University of Alabama at Birmingham School of Medicine, Birmingham, AL, 35294-1170, USA

    Rachel Philpott & Michael Niederweis

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  1. Nazia Mojib
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Correspondence to Asim K. Bej.

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Mojib, N., Philpott, R., Huang, J.P. et al. Antimycobacterial activity in vitro of pigments isolated from Antarctic bacteria. Antonie van Leeuwenhoek 98, 531–540 (2010). https://doi.org/10.1007/s10482-010-9470-0

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