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Isolation and Characterization of Microcystin-Producing Microcystis aeruginosa MBDU 626 from a Freshwater Bloom Sample in Tamil Nadu, South India

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Microbiological Research In Agroecosystem Management

Abstract

Toxin-producing cyanobacteria are a worldwide threat to both human and animal health. Microcystins (MCs) are the most commonly occurring toxins produced by bloom-forming cyanobacteria, especially Microcystis sp. This study describes the occurrence of bloom-forming toxigenic Microcystis aeruginosa MBDU 626 from Manjalar Dam, Theni District, Tamil Nadu, South India. Two microcystin (MC) variants, MC-LR and [D-Asp3] MC-LR were identified from the isolated strain using high-performance liquid chromatography and gas chromatography coupled mass spectrometry (GC/MS). Four peptides such as aeruginosin, microginin, kasumigamide and anabaenopeptin were also co-produced along with these MC variants. Our results show that the presence of cyanobacterial toxins in essential water resources requires rapid remedial action and needs to develop a national program for regular monitoring of toxigenic blooms in freshwater bodies of South India, in general, Tamil Nadu, in particular.

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References

  • Agrawal MK, Bagchi D, Bagchi SN (2001) Acute inhibition of protease and suppression of growth in zooplankter, Moina macrocopa, by Microcystis blooms collected in Central India. Hydrobiologia 464:37–44

    Article  Google Scholar 

  • Agrawal MK, Ghosh SK, Bagchi D, Weckesser J, Erhard M, Bagchi SN (2006) Occurrence of microcystin-containing toxic water blooms in Central India. J Microbiol Biotechnol 16:212–218

    CAS  Google Scholar 

  • Bajpai R, Sharma NK, Lawton LA, Edwards C, Rai AK (2009) Microcystin producing cyanobacterium Nostoc sp. BHU001 from a pond in India. Toxicon 53:587–590

    Article  PubMed  CAS  Google Scholar 

  • Baldia SF, Conaco MCG, Nishijima T, Imanishi S, Harada KI (2003) Microcystin production during algal bloom occurrence in Laguna de Bay, the Philippines. Fish Sci 69:110–116

    Article  CAS  Google Scholar 

  • Beattie KA, Kaya K, Sano T, Codd GA (1998) Three dehydrobutyrine-containing microcystins from Nostoc. Phytochemistry 47:1289–1292

    Article  CAS  Google Scholar 

  • Bister B, Keller S, Baumann HI, Nicholson G, Weist S, Jung G, Sussmuth RD, Juttner F (2004) Cyanopeptolin 963A, a chymotrypsin inhibitor of Microcystis PCC 7806. J Nat Prod 67:1755–1757

    Article  PubMed  CAS  Google Scholar 

  • Botes DP, Tuinman AA, Wessel PL, Viljoen CC, Kruger H, Williams DH, Santikarn S, Smith RJ, Hammond SJ (1984) The structure of cyanoginosin-LA, a cyclic hepatopeptide toxin from the cyanobacterium Microcystis aeruginosa. J Chem Soc Perkin Trans 1:2311–2318

    Article  Google Scholar 

  • Carmichael JV (1992) The male librarian and the feminine image: a survey of stereotype, status, and gender perceptions. Libr Inform Sci Res 14:411–447

    Google Scholar 

  • Carmichael WW (1994) The toxins of cyanobacteria. Sci Amer 270:64–72

    Article  Google Scholar 

  • Carmichael WW, Azevedo SMFO, An JS (2001) Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins (Caruaru syndrome). Environ Health Persp 109:663–668

    Article  CAS  Google Scholar 

  • Codd GA (1999) Cyanobacterial toxins: their occurrence in aquatic environments and significance to health. In: Charpy P, Larkum AWD (eds) Marine Cyanobacteria. Bulletin de l’Institut Oce′anographique. Monaco, pp 483–500

    Google Scholar 

  • Codd GA, Ward CJ, Bell SG (1997) Cyanobacterial toxins: occurrence, modes of action, health effects and exposure routes. In: Seiler JP, Vilanova E (eds) Applied toxicology: approaches through basic science. In: Proceedings of the 1996 EUROTOX meeting, Spain. Archiv Toxicol Suppl 19, Berlin, Springer, pp 399–410

    Google Scholar 

  • Codd GA, Azevedo SMFO, Bagchi SN, Burch MD, Carmichael WW, Harding WR, Kaya K, Utkilen HC (2005) CYANONET A global network for cyanobacterial bloom and toxin risk management: Initial situation assessment and recommendations. Int Hydrol Progr-VI Tech Doc Hydrol 76, UNESCO, Paris

    Google Scholar 

  • Dai R, Liu H, Qu J, Ru J, Hou Y (2008) Cyanobacteria and their toxins in Guanting Reservoir of Beijing, China. J Hazard Mater 153:470–477

    Article  PubMed  CAS  Google Scholar 

  • Del campo FF, Ouahid Y (2010) Identification of Microcystis from three collection strains of Microcystis aeruginosa. Environ poll 158:2906–2914

    Article  CAS  Google Scholar 

  • Diehnelt CW, Peterman SM, Budde WL (2005) Liquid chromatography-tandem mass spectrometry and accurate m/z measurements of cyclic peptide cyanobacteria toxins. TrAC Trends Anal Chem 24:622–634

    Article  CAS  Google Scholar 

  • Dittmann E, Neilan BA, Erhard M, von Dohren H, Borner T (1997) Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Mol Microbiol 26:779–787

    Article  PubMed  CAS  Google Scholar 

  • Erhard M (1999) Ph.D. thesis. Technische Universitat Berlin, Germany

    Google Scholar 

  • Falconer IR (1996) Potential impact on human health of toxic cyanobacteria. Phycologia 35:6–11

    Article  Google Scholar 

  • Falconer IR (1997) Blue-green algae in lakes and rivers: their harmful effects on human health. Austr Biologist 10:107–110

    Google Scholar 

  • Falconer IR, Bartram J, Chorus I, Kuiper-Goodman T, Utkilen H, Burch M, Codd GA (1999) Safe levels and safe practice. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water, a guide of their public health consequences, monitoring and management. E&FN Spon WHO, London, pp 155–176

    Google Scholar 

  • Fastner J, Erhard M, von Dohren H (2001) Determination of oligopeptide diversity within a natural population of Microcystis spp. (Cyanobacteria) by typing single colonies by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Appl Environ Microbiol 67:5069–5076

    Article  PubMed  CAS  Google Scholar 

  • Frias HV, Mendes MA, Cardozo KHM, Carvalho VM, Tomazela D, Colepicolo P, Pinto E (2006) Use of electrospray tandem mass spectrometry for identification of microcystins during a cyanobacterial bloom event. Biochem Biophys Res Commun 344:741–746

    Article  PubMed  CAS  Google Scholar 

  • Fukuta Y, Ohshima T, Gnanadesikan V, Shibuguchi T, Nemoto T, Kisugi T, Okino T, Shibasaki M (2004) Enantioselective syntheses and biological studies of aeruginosin 298-A and its analogs: application of catalytic asymmetric phase-transfer reaction. Proc Natl Acad Sci 101:5433–5438

    Article  PubMed  CAS  Google Scholar 

  • Gkelis S, Harjunpaa V, Lanaras T, Sivonen K (2005) Diversity of hepatotoxic microcystins and bioactive anabaenopeptins in cyanobacterial blooms from Greek freshwaters. Environ Toxicol 20:249–256

    Article  PubMed  CAS  Google Scholar 

  • Grach-Pogrebinsky O, Sedmak B, Carmeli S (2003) Protease inhibitors from a Slovenian lake Bled toxic water bloom of the cyanobacterium Planktothrix rubescens. Tetrahed 59:8329–8336

    Article  CAS  Google Scholar 

  • Grosse Y, Baan R, Straif K, Secretan B, Ghissassi FE, Cogliano V (2006) Carcinogenicity of nitrate, nitrite, and cyanobacterial peptide toxins. Lancet Oncol 7:628–629

    Article  PubMed  Google Scholar 

  • Gulledge BM, Aggen JB, Huang HB, Nairn AC, Chamberlin AR (2002) The microcystins and nodularins: cyclic polypeptide inhibitors of PP1 and PP2A. Curr Med Chem 9:1991–2003

    Article  CAS  Google Scholar 

  • Haande S, Ballot A, Rohrlack T, Fastner J, Wiedner C, Edvardsen B (2007) Diversity of Microcystis aeruginosa isolates (Chroococcales, Cyanobacteria) from East-African water bodies. Arch Microbiol 188:15–25

    Article  PubMed  CAS  Google Scholar 

  • Harada KI (1995) Chemistry and detection of microcystins. In: Watanabe MF, Harada KI, Carmichael WW, Fujiki H (eds) Toxic microcystis. CRC Press, Boca Raton, pp 103–148

    Google Scholar 

  • Harada KI (2004) Production of secondary metabolites by freshwater cyanobacteria. Chem Pharm Bull 52:889–899

    Article  PubMed  CAS  Google Scholar 

  • Harada KI, Murata H, Qiang Z, Suzuki M, Kondo F (1996) Mass spectrometric screening method for microcystins in cyanobacteria. Toxicon 34:701–710

    Article  PubMed  CAS  Google Scholar 

  • Ishida K, Murakami M (2000) Kasumigamide an antialgal peptide from the cyanobacterium Microcystis aeruginosa. J Org Chem 65:5898–5900

    Article  PubMed  CAS  Google Scholar 

  • Ishida K, Okita Y, Matsuda H, Okino T, Murakami M (1999) Aeruginosins, protease inhibitors from the cyanobacterium Microcystis aeruginosa. Tetrahed 55:10971–10988

    Article  CAS  Google Scholar 

  • Jacobi C, Rinehart KL, Codd GA, Carmienke I, Weckesser J (1996) Occurrence of toxic water blooms containing microcystins in a German lake over a three year period. J Syst Appl Microbiol 19:249–254

    Article  Google Scholar 

  • Jayatissa LP, Silva EIL, McElhiney J, Lawton LA (2006) Occurrence of toxigenic cyanobacterial blooms in freshwaters of Sri Lanka. Syst Appl Microbiol 29:156–164

    Article  PubMed  CAS  Google Scholar 

  • Jungblut AD, Hoeger SJ, Mountfort D, Hitzfeld BC, Dietrich DR, Neilan BA (2006) Characterization of microcystin production in Antarctic cyanobacterial mat community. Toxicon 47:271–278

    Article  PubMed  CAS  Google Scholar 

  • Kaebernick M, Neilan BA, Borner T, Dittmann E (2000) Light and the transcriptional response of the microcystin biosynthesis gene cluster. Appl Environ Microbiol 66:3387–3392

    Article  PubMed  CAS  Google Scholar 

  • Karas M, Gluckmann M, Schafer J (2000) Ionization in matrix-assisted laser desorption/ionization: singly charged molecular ions are the lucky survivors. J Mass Spectrom 35:1–12

    Article  PubMed  CAS  Google Scholar 

  • Kaya K, Sano T (1999) Total microcystin determination using erythro-2-methyl-3-[methoxy-(3)]-4-phenylbutyric acid [MMPB-(3)] as the internal standard. Anal Chim Acta 386:107–112

    Article  CAS  Google Scholar 

  • Kim B, Kim HS, Park HD, Choi K, Park JG (1999) Microcystin content of cyanobacterial cells in Korean reservoirs and their toxicity. Korean J Limnol 32:288–294

    Google Scholar 

  • Kodani S, Suzuki S, Ishida K, Murakami M (1999) Five new cyanobacterial peptides from water bloom materials of lake Teganuma (Japan). FEMS Microbiol Lett 178:343–348

    Article  CAS  Google Scholar 

  • Kondo F, Harada K (1996) Mass-spectrometric analysis of cyanobacterial toxins. J Mass Spectrom Soc Jpn 44:355–376

    Article  CAS  Google Scholar 

  • Lehman PW, Boyer G, Hall C, Waller S, Gehrts K (2005) Distribution and toxicity of a new colonial Microcystis aeruginosa bloom in the San Francisco Bay Estuary, California. Hydrobiologia 541:87–99

    Article  CAS  Google Scholar 

  • Li S, Xie P, Xu J, Zhang X, Qin J, Zheng L, Liang G (2007) Factors shaping the pattern of seasonal variations of microcystins in Lake Xingyun, a subtropical plateau lake in China. Bull Environ Contam Toxicol 78:226–230

    Article  PubMed  CAS  Google Scholar 

  • Luukkainen R, Namikoshi M, Sivonen K, Rinehart KL, Niemela SI (1994) Isolation and identification of 12 microcystins from four strains and two bloom samples of Microcystis spp: structure of a new hepatotoxin. Toxicon 32:133–139

    Article  PubMed  CAS  Google Scholar 

  • Matsuda H, Okino T, Murakami M, Yamaguchi K (1997) Aeruginosins 102-A and B, new thrombin inhibitors from the cyanobacterium Microcystis viridis (NIES-102). Tetrahed 52:14501–14506

    Article  Google Scholar 

  • Meriluoto J, Lawton L, Harada K (2000) Isolation and detection of microcystins and nodularins, cyanobacterial peptide hepatotoxins. Methods Mol Biol 145:65–87

    PubMed  CAS  Google Scholar 

  • Murakami M, Ishida K, Okino T, Okita Y, Matsuda H, Yamaguchi K (1995) Aeruginosin 98-A and-B, trypsin inhibitors from the blue-green alga Microcystis aeruginosa (NIES-98). Tetrahed Lett 36:2758–2788

    Article  Google Scholar 

  • Muthukumar C, Vijayakumar R, Muralitharan G, Panneerselvam A, Thajuddin N (2007) Cyanobacterial biodiversity from different freshwater ponds of Thanjavur, Tamil Nadu (India). Acta Bot Malacitana 32:17–25

    Google Scholar 

  • Namikoshi M, Rinehart KL (1996) Bioactive compounds produced by cyanobacteria. J Ind Microbiol 17:373–384

    Article  CAS  Google Scholar 

  • Namikoshi M, Rinehart KL, Sakai R, Stotts RR, Dahlem AM, Beasley VR, Carmichael WW, Evans WR (1992a) Identification of 12 hepatotoxins from a homer lake bloom of the cyanobacteria Microcystis aeruginosa, Microcystis viridis, and Microcystis wesenbergii: nine new microcystins. J Org Chem 57:866–872

    Article  CAS  Google Scholar 

  • Namikoshi M, Sivonen K, Evans WR, Sun F, Carmichael WW, Rinehart KL (1992b) Isolation and structures of microcystins from a cyanobacterial water bloom (Finland). Toxicon 30:1473–1479

    Article  PubMed  CAS  Google Scholar 

  • Namikoshi MF, Sun B, Choi BW, Rinehart KL, Carmichael WW, Evans WR, Beasley VR (1995) Seven more microcystins from Homer Lake cells: application of the general method for structure assignment of peptides containing α,β-dehydroamino acid unit(s). J Org Chem 60:3671–3679

    Article  CAS  Google Scholar 

  • Neilan BA (1995) Identification and phylogenetic analysis of toxigenic cyanobacteria by multiplex randomly amplified polymorphic DNA PCR. Appl Environ Microbiol 61:2286–2291

    PubMed  CAS  Google Scholar 

  • Nelissen B, Wilmotte A, Neefs JM, De Wachter R (1994) Phylogenetic relationships among filamentous helical bacteria investigated on the basis of 16S ribosomal RNA gene sequence analysis. System Appl Microbiol 17:206–210

    Article  CAS  Google Scholar 

  • Neumann U, Forchert A, Flury T, Weckesser J (1997) Microginin FR1, a linear peptide from a water bloom of Microcystis species. FEMS Microbiol Lett 153:475–478

    Article  CAS  Google Scholar 

  • Neumann U, Campos V, Cantarero S, Urrutia H, Heinze R, Weckesser J, Erhard M (2000) Co-occurrence of non-toxic (cyanopeptolin and toxic microcystin) peptides in a bloom of Microcystis sp from a Chilean lake. Syst Appl Microbiol 23:191–197

    Article  PubMed  CAS  Google Scholar 

  • Oh HM, Lee SJ, Kim JH, Kim HS, Yoon BD (2001) Seasonal variation and indirect monitoring of microcystin concentrations in Daechung reservoir, Korea. Appl Environ Microbiol 67:1484–1489

    Article  PubMed  CAS  Google Scholar 

  • Ortea PM, Allis O, Healy BM, Lehane M, Ni Shuilleabhain A, Furey A, James KJ (2004) Determination of toxic cyclic heptapeptides by liquid chromatography with detection using ultra-violet, protein phosphatase assay and tandem mass spectrometry. Chemosphere 55:1395–1402

    Article  PubMed  CAS  Google Scholar 

  • Oudra B, Loudikia M, Sbiyyaa B, Martins R, Vasconcelos V, Namikoshi N (2001) Isolation, characterization and quantification of microcystins (heptapeptides hepatotoxins) in Microcystis aeruginosa dominated bloom of Lalla Takerkoust lake-reservoir (Morocco). Toxicon 39:1375–1381

    Article  PubMed  CAS  Google Scholar 

  • Parker DL, Kumar HD, Rai LC, Singh JB (1997) Potassium salts inhibit growth of the cyanobacteria Microcystis spp. in pond water and defined media: implications for control of microcystin-producing aquatic blooms. Appl Environ Biol 63:2324–2329

    CAS  Google Scholar 

  • Prakash S, Lawton LA, Edwards C (2009) Stability of toxigenic Microcystis blooms. Harmful Algae 8:376–384

    Article  Google Scholar 

  • Rippka R, Dereuelles J, Waterbury J, Herdman M, Stanier R (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Sangolkar LN, Maske SS, Muthal PL, Kashyap SM, Chakrabarti T (2009) Isolation and characterization of microcystin producing Microcystis from a Central Indian water bloom. Harmful Algae 8:674–684

    Article  CAS  Google Scholar 

  • Sano T, Kaya K (1995) Oscillamide Y, a chymotrypsin inhibitor from toxic Oscillatoria agardhii. Tetrahed Lett 36:5933–5936

    CAS  Google Scholar 

  • Sano T, Kaya K (1998) Two new (E)-2-Amino-2-Butenoic Acid (Dhb)-containing microcystins isolated from Oscillatoria agardhii. Tetrahed 54:463–470

    Article  CAS  Google Scholar 

  • Sivonen K (1996) Cyanobacterial toxins and toxin production. Phycologia 35:12–24

    Article  Google Scholar 

  • Sivonen K, Jones G (1999) Cyanobacterial toxins. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. E&FN Spon, London, pp 41–111

    Google Scholar 

  • Sivonen K, Niemela SI, Niemi RM, Lepisto L, Luoma TH, Rasinen LA (1990) Toxic cyanobacteria (bluegreen algae) in Finnish fresh and coastal waters. Hydrobiologia 190:267–275

    Article  Google Scholar 

  • Tsuji K, Masui H, Uemura H, Mori Y, Harada KI (2001) Analysis of microcystins in sediments using MMPB method. Toxicon 39:687–692

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Parkpian P, Fujimoto N, Ruchirawat KM, DeLaune RD, Jugsujinda A (2002) Environmental conditions associating microcystins production to Microcystis aeruginosa in a reservoir of Thailand. J Environ Sci Health Part A-Toxic/Hazard Subst Environ Eng 37:1181–1207

    Article  Google Scholar 

  • Welker M, Brunke M, Preussel K, Lippert I, von Dohren H (2004a) Diversity and distribution of Microcystis (Cyanobacteria) oligopeptide chemotypes from natural communities studied by single-colony mass spectrometry. Microbiology 150:1785–1796

    Article  PubMed  CAS  Google Scholar 

  • Welker M, Christiansen G, von Dohren H (2004b) Diversity of co existing Planktothrix (Cyanobacteria) chemotypes deduced by mass spectral analysis of microcystins and other oligopeptides. Arch Microbiol 182:288–289

    Article  PubMed  CAS  Google Scholar 

  • Welker M, Khan S, Haque MM, Islam S, Khan NH, Chorus I, Fastner J (2005) Microcystins (cyanobacterial toxins) in surface waters of rural Bangladesh: pilot study. J Water Health 3:325–337

    PubMed  CAS  Google Scholar 

  • Welker M, Marsalek B, Sejnohova L, von Dohren H (2006) Detection and identification of oligopeptides in Microcystis (Cyanobacteria) colonies: toward an understanding of metabolic diversity. Peptides 27:2090–2103

    Article  PubMed  CAS  Google Scholar 

  • Wilmotte A, Van de Peer Y, Goris A, Chapelle S, De Baere R, Nelissen B, Neefs JM, Hennebert GL, De Wachter R (1993) Evolutionary relationships among higher fungi inferred form small ribosomal subunit RNA sequence analysis. System Appl Microbiol 16:436–444

    Article  CAS  Google Scholar 

  • Wood SA, Mountfort D, Selwood AI, Holland PT, Puddick J, Cary SC (2008) Widespread distribution and identification of eight novel microcystins in Antarctic cyanobacterial mats. Appl Environ Microbiol 74:7243–7251

    Article  PubMed  CAS  Google Scholar 

  • World Health Organization (1998). Guidelines for drinking water quality. Addendum to Volume 2. Health Criteria and Other supporting information, 2nd edn. World Health Organization, Geneva, pp 95–110

    Google Scholar 

  • Xu Y, Wu Z, Yu B, Peng X, Yu G, Wei Z, Wang G, Li R (2008) Non-microcystin producing Microcystis wesenbergii (Komárek) Komárek (Cyanobacteria) representing a main water bloom-forming species in Chinese waters. Environ Poll 156:162–167

    Article  CAS  Google Scholar 

  • Zurawell RW, Chen H, Burke JM, Prepas EE (2005) Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. J Toxicol Environ Health 8:1–37

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to the University Grants Commission (UGC), Government of India, for the financial support. AMP Anahas acknowledges the Maulana Azad National Fellowship Scheme (MANF) for the fellowship.

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Anahas, A.M.P., Gayathri, M., Muralitharan, G. (2013). Isolation and Characterization of Microcystin-Producing Microcystis aeruginosa MBDU 626 from a Freshwater Bloom Sample in Tamil Nadu, South India. In: Velu, R. (eds) Microbiological Research In Agroecosystem Management. Springer, India. https://doi.org/10.1007/978-81-322-1087-0_16

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