High levels of structural diversity observed in microcystins from microcystis CAWBG11 and characterization of six new microcystin congeners

Marine Drugs

Volumn 12, Issue 11, 2014, Pages 5372-5395

  Puddick, Jonathan ^a   Prinsep, Michèle R ^b   Wood, Susanna A ^a,b   Kaufononga, Sangata A F ^b   Cary, Stephen Craig ^b   Hamilton, David P ^b  

^a CAWTHRON INSTITUTE   (New Zealand)

^b UNIVERSITY OF WAIKATO   (New Zealand)

Author keywords

Mass spectrometry; Microcystin diversity; Microcystins; Microcystis CAWBG11

Indexed keywords

AMINO ACID; MICROCYSTIN; MICROCYSTIN FA; MICROCYSTIN FABA; MICROCYSTIN FL; MICROCYSTIN RA; MICROCYSTIN RABA; MICROCYSTIN WA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CYANOBACTERIUM; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MICROCYSTIS; NONHUMAN; NUCLEOTIDE SEQUENCE; TANDEM MASS SPECTROMETRY; TOXIN ANALYSIS; TOXIN STRUCTURE; TOXIN SYNTHESIS; CHEMISTRY; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; PROCEDURES;

ANIMALIA; CYANOBACTERIA; MICROCYSTIS;

AMINO ACID SEQUENCE; CHROMATOGRAPHY, LIQUID; CYANOBACTERIA; MASS SPECTROMETRY; MICROCYSTINS; MICROCYSTIS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 84915750143     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12115372     Document Type: Article

References (63)

1. Holt, J.G.; Krieg, N.R.; Sneath, P.H.A.; Staley, J.T.; Williams, S.T. Oxygenic photosynthetic bacteria. In Bergey's Manual of Determinative Bacteriology, 9th ed.; Lippincott Williams and Wilkins: Philadelphia, PA, USA, 2000; pp. 377-426.
2. Whitton, B.A.; Potts, M. The Ecology of Cyanobacteria, Their Diversity in Time and Space; Kluwer Academic Publishers: Dordrecht, The Netherlands, 2000.
3. Jones, G.J.; Korth, W. In situ production of volatile odour compounds by river and reservoir phytoplankton populations in Australia. Water Sci. Technol. 1995, 31, 145-151.
4. Sivonen, K.; Jones, G. Cyanobacterial toxins. In Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management; Chorus, I., Bartram, J., Eds.; E & FN Spon: London, UK, 1999; pp. 55-124.
5. Van Apeldoorn, M.E.; van Egmond, H.P.; Speijers, G.J.A.; Bakker, G.J.I. Toxins of cyanobacteria. Mol. Nutr. Food Res. 2007, 51, 7-60.
6. Niedermeyer, T. Microcystin Congeners Described in the Literature, 2013. Available online: http://dx.doi.org/10.6084/m9.figshare.880756 (accessed on 21 October 2014).
7. Rinehart, K.; Namikoshi, M.; Choi, B. Structure and biosynthesis of toxins from blue-green algae (cyanobacteria). J. Appl. Phycol. 1994, 6, 159-176.
8. Tillett, D.; Dittmann, E.; Erhard, M.; von Döhren, H.; Börner, T.; Neilan, B.A. Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: An integrated peptide-polyketide synthetase system. Chem. Biol. 2000, 7, 753-764.
9. Moore, R.E.; Chen, J.L.; Moore, B.S.; Patterson, G.M.L.; Carmichael, W.W. Biosynthesis of microcystin-LR: Origin of the carbons in the Adda and Masp units. J. Am. Chem. Soc. 1991, 113, 5083-5084.
10. Nishizawa, T.; Asayama, M.; Fujii, K.; Harada, K.-I.; Shirai, M. Genetic analysis of the peptide synthetase genes for a cyclic heptapeptide microcystin in Microcystis spp. J. Biochem. 1999, 126, 520-529.
11. Nishizawa, T.; Ueda, A.; Asayama, M.; Fujii, K.; Harada, K.-I.; Ochi, K.; Shirai, M. Polyketide synthase gene coupled to the peptide synthetase module involved in the biosynthesis of the cyclic heptapeptide microcystin. J. Biochem. 2000, 127, 779-789.
12. Börner, T.; Dittmann, E. Molecular biology of cyanobacterial toxins. In Harmful Cyanobacteria; Huisman, J., Matthijs, H.C.P., Visser, P.M., Eds.; Springer: Dordrecht, The Netherlands, 2005; pp. 25-40.
13. Mikalsen, B.; Boison, G.; Skulberg, O.M.; Fastner, J.; Davies, W.; Gabrielsen, T.M.; Rudi, K.; Jakobsen, K.S. Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains. J. Bacteriol. 2003, 185, 2774-2785.
14. Fewer, D.; Rouhiainen, L.; Jokela, J.; Wahlsten, M.; Laakso, K.; Wang, H.; Sivonen, K. Recurrent adenylation domain replacement in the microcystin synthetase gene cluster. BMC Evol. Biol. 2007, 7, 1-11.
15. Fischer, A.; Hoeger, S.J.; Stemmer, K.; Feurstein, D.J.; Knobeloch, D.; Nussler, A.; Dietrich, D.R. The role of organic anion transporting polypeptides (OATPs/SLCOs) in the toxicity of different microcystin congeners in vitro: A comparison of primary human hepatocytes and OATP-transfected HEK293 cells. Toxicol. Appl. Pharmacol. 2010, 245, 9-20.
16. An, J.; Carmichael, W.W. Use of a colorimetric protein phosphatase inhibition assay and enzyme linked immunosorbent assay for the study of microcystins and nodularins. Toxicon 1994, 32, 1495-1507.
17. Runnegar, M.T.; Falconer, I.R.; Silver, J. Deformation of isolated rat hepatocytes by a peptide hepatotoxin from the blue-green alga Microcystis aeruginosa. Naunyn-Schmiedeberg's Arch. Pharmacol. 1981, 317, 268-272.
18. Falconer, I.R.; Yeung, D.S.K. Cytoskeletal changes in hepatocytes induced by Microcystis toxins and their relation to hyperphosphorylation of cell proteins. Chem. Biol. Interact. 1992, 81, 181-196.
19. Fujiki, H.; Suganuma, M. Tumor promotion by inhibitors of protein phosphatases 1 and 2A: The okadaic acid class of compounds. Adv. Cancer Res. 1993, 61, 143-194.
20. Sainis, I.; Fokas, D.; Vareli, K.; Tzakos, A.; Kounnis, V.; Briasoulis, E. Cyanobacterial cyclopeptides as lead compounds to novel targeted cancer drugs. Mar. Drugs 2010, 8, 629-657.
21. Niedermeyer, T.H.J.; Daily, A.; Swiatecka-Hagenbruch, M.; Moscow, J.A. Selectivity and potency of microcystin congeners against OATP1B1 and OATP1B3 expressing cancer cells. PLoS One 2014, 9, e91476.
22. Rueckert, A.; Wood, S.A.; Cary, S.C. Development and field assessment of a quantitative PCR for the detection and enumeration of the noxious bloom-former Anabaena planktonica. Limnol. Oceanogr. Methods 2007, 5, 474-483.
23. Ishida, K.; Okita, Y.; Matsuda, H.; Okino, T.; Murakami, M. Aeruginosins, protease inhibitors from the cyanobacterium Microcystis aeruginosa. Tetrahedron 1999, 55, 10971-10988.
24. Ploutno, A.; Carmeli, S. Modified peptides from a water bloom of the cyanobacterium Nostoc sp. Tetrahedron 2002, 58, 9949-9957.
25. Welker, M.; Marsálek, B.; Sejnohová, L.; von Döhren, H. Detection and identification of oligopeptides in Microcystis (cyanobacteria) colonies: Toward an understanding of metabolic diversity. Peptides 2006, 27, 2090-2103.
26. Murakami, M.; Okita, Y.; Matsuda, H.; Okino, T.; Yamaguchi, K. Aeruginosin 298-A, a thrombin and trypsin inhibitor from the blue-green alga Microcystis aeruginosa (NIES-298). Tetrahedron Lett. 1994, 35, 3129-3132.
27. Howard, K.L.; Boyer, G.L. Quantitative analysis of cyanobacterial toxins by matrix-assisted laser desorption ionization mass spectrometry. Anal. Chem. 2007, 79, 5980-5986.
28. Puddick, J.; Prinsep, M.R.; Wood, S.A.; Miles, C.O.; Rise, F.; Cary, S.C.; Hamilton, D.P.; Wilkins, A.L. Structural characterization of new microcystins containing tryptophan and oxidized tryptophan residues. Mar. Drugs 2013, 11, 3025-3045.
29. Meriluoto, J.A.O.; Sandström, A.; Eriksson, J.E.; Remaud, G.; Grey Graig, A.; Chattopadhyaya, J. Structure and toxicity of a peptide hepatotoxin from the cyanobacterium Oscillatoria agardhii. Toxicon 1989, 27, 1021-1034.
30. Kusumi, T.; Ooi, T.; Watanabe, M.M.; Takahashi, H.; Kakisawa, H. Cyanoviridin RR, a toxin from the cyanobacterium (blue-green alga) Microcystis viridis. Tetrahedron Lett. 1987, 28, 4695-4698.
31. Painuly, P.; Perez, R.; Fukai, T.; Shimizu, Y. The structure of a cyclic peptide toxin, cyanogenosin-RR from Microcystis aeruginosa. Tetrahedron Lett. 1988, 29, 11-14.
32. Watanabe, M.F.; Oishi, S.; Harada, K.-I.; Matsuura, K.; Kawai, H.; Suzuki, M. Toxins contained in Microcystis species of cyanobacteria (blue-green algae). Toxicon 1988, 26, 1017-1025.
33. Botes, D.P.; Wessels, P.L.; Kruger, H.; Runnegar, M.T.C.; Santikarn, S.; Smith, R.J.; Barna, J.C.J.; Williams, D.H. Structural studies on cyanoginosins-LR,-YR,-YA, and-YM, peptide toxins from Microcystis aeruginosa. Org. Bioorg. Chem. 1985, 12, 2747-2748.
34. Krishnamurthy, T.; Szafraniec, L.; Hunt, D.F.; Shabanowitz, J.; Yates, J.R.; Hauer, C.R.; Carmichael, W.W.; Skulberg, O.; Codd, G.A.; Missler, S. Structural characterization of toxic cyclic peptides from blue-green algae by tandem mass spectrometry. Proc. Natl. Acad. Sci. USA 1989, 86, 770-774.
35. Harada, K.-I.; Ogawa, K.; Kimura, Y.; Murata, H.; Suzuki, M.; Thorn, P.M.; Evans, W.R.; Carmichael, W.W. Microcystins from Anabaena flos-aquae NRC 525-17. Chem. Res. Toxicol. 1991, 4, 535-540.
36. Lee, T.-H.; Chou, H.-N. Isolation and identification of seven microcystins from a cultured M.TN-2 strain of Microcystis aeruginosa. Bot. Bull. Academ. Sinica 2000, 41, 197-202.
37. Namikoshi, M.; Rinehart, K.L.; Sakai, R.; Stotts, R.R.; Dahlem, A.M.; Beasley, V.R.; Carmichael, W.W.; Evans, W.R. 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. 1992, 57, 866-872.
38. Lee, T.-H.; Chen, Y.-M.; Chou, H.-N. First report of microcystins in Taiwan. Toxicon 1998, 36, 247-255.
39. Miles, C.O.; Sandvik, M.; Nonga, H.E.; Rundberget, T.; Wilkins, A.L.; Rise, F.; Ballot, A. Thiol derivatization for LC-MS identification of microcystins in complex matrices. Environ. Toxicol. 2012, 46, 8937-8944.
40. Diehnelt, C.W.; Dugan, N.R.; Peterman, S.M.; Budde, W.L. Identification of microcystin toxins from a strain of Microcystis aeruginosa by liquid chromatography introduction into a hybrid linear ion trap-fourier transform ion cyclotron resonance mass spectrometer. Anal. Chem. 2006, 78, 501-512.
41. Botes, D.P.; Tuinman, A.A.; Wessels, P.L.; Viljoen, C.C.; Kruger, H.; Williams, D.H.; Santikarn, S.; Smith, R.J.; Hammond, S.J. The structure of cyanoginosin-LA, a cyclic heptapeptide toxin from the cyanobacterium Microcystis aeruginosa. Org. Bioorg. Chem. 1984, 10, 2311-2318.
42. Puddick, J.; Prinsep, M.R.; Wood, S.A.; Cary, S.C.; Hamilton, D.P.; Wilkins, A.L. Isolation and structure determination of two new hydrophobic microcystins from Microcystis sp. (CAWBG11). Phytochem. Lett. 2013, 6, 575-581.
43. Del Campo, F.F.; Ouahid, Y. Identification of microcystins from three collection strains of Microcystis aeruginosa. Environ. Pollut. 2010, 158, 2906-2914.
44. Gathercole, P.S.; Thiel, P.G. Liquid chromatographic determination of the cyanoginosins, toxins produced by the cyanobacterium Microcystis aeruginosa. J. Chromatogr. A 1987, 408, 435-440.
45. Craig, M.; McCready, T.L.; Luu, H.A.; Smillie, M.A.; Dubord, P.; Holmes, C.F.B. Identification and characterization of hydrophobic microcystins in Canadian freshwater cyanobacteria. Toxicon 1993, 31, 1541-1549.
46. Beattie, K.A.; Kaya, K.; Sano, T.; Codd, G.A. Three dehydrobutyrine-containing microcystins from Nostoc. Phytochemistry 1998, 47, 1289-1292.
47. Sano, T.; Beattie, K.A.; Codd, G.A.; Kaya, K. Two (Z)-dehydrobutyrine-containing microcystins from a hepatotoxic bloom of Oscillatoria agardhii from Soulseat Loch, Scotland. J. Nat. Prod. 1998, 61, 851-853.
48. Sano, T.; Kaya, K. Two new (E)-2-amino-2-butenoic acid (Dhb)-containing microcystins isolated from Oscillatoria agardhii. Tetrahedron 1998, 54, 463-470.
49. Miles, C.O.; Sandvik, M.; Haande, S.; Nonga, H.; Ballot, A. First use of LC-MS analysis with thiol derivatization to differentiate [Dhb7]-from [Mdha7]-microcystins: Analysis of cyanobacterial blooms, Planktothrix cultures and European crayfish from Lake Steinsfjorden, Norway. Environ. Sci. Technol. 2013, 47, 4080-4087.
50. Smith, J.L.; Boyer, G.L. Standardization of microcystin extraction from fish tissues: A novel internal standard as a surrogate for polar and non-polar variants. Toxicon 2009, 53, 238-245.
51. Frias, H.V.; Mendes, M.A.; Cardozo, K.H.M.; Carvalho, V.M.; Tomazela, D.; Colepicolo, P.; Pinto, E. Use of electrospray tandem mass spectrometry for identification of microcystins during a cyanobacterial bloom event. Biochem. Biophys. Res. Commun. 2006, 344, 741-746.
52. Okello, W.; Portmann, C.; Erhard, M.; Gademann, K.; Kurmayer, R. Occurrence of microcystin-producing cyanobacteria in Ugandan freshwater habitats. Environ. Toxicol. 2010, 25, 367-380.
53. Fujii, K.; Ikai, Y.; Oka, H.; Suzuki, M.; Harada, K.-I. A nonempirical method using LC/MS for determination of the absolute configuration of constituent amino acids in a peptide: Combination of Marfey's method with mass spectrometry and its practical application. Anal. Chem. 1997, 69, 5146-5151.
54. Mahakhant, A.; Sano, T.; Ratanachot, P.; Tong-a-ram, T.; Srivastava, V.C.; Watanabe, M.M.; Kaya, K. Detection of microcystins from cyanobacterial water blooms in Thailand fresh water. Phycol. Res. 1998, 46, 25-29.
55. Okello, W.; Ostermaier, V.; Portmann, C.; Gademann, K.; Kurmayer, R. Spatial isolation favours the divergence in microcystin net production by Microcystis in Ugandan freshwater lakes. Water Res. 2010, 44, 2803-2814.
56. Gademann, K.; Portmann, C.; Blom, J.F.; Zeder, M.; Juttner, F. Multiple toxin production in the cyanobacterium Microcystis: Isolation of the toxic protease inhibitor cyanopeptolin 1020. J. Nat. Prod. 2010, 73, 980-984.
57. Namikoshi, M.; Rinehart, K.L.; Sakai, R.; Sivonen, K.; Carmichael, W.W. Structures of three new cyclic heptapeptide hepatotoxins produced by the cyanobacterium (blue-green alga) Nostoc sp. strain 152. J. Org. Chem. 1990, 55, 6135-6139.
58. Sivonen, K.; Namikoshi, M.; Evans, W.R.; Fardig, M.; Carmichael, W.W.; Rinehart, K.L. Three new microcystins, cyclic heptapeptide hepatotoxins, from Nostoc sp. strain 152. Chem. Res. Toxicol. 1992, 5, 464-469.
59. Sivonen, K.; Carmichael, W.W.; Namikoshi, M.; Rinehart, K.L.; Dahlem, A.M.; Niemela, S.I. Isolation and characterization of hepatotoxic microcystin homologs from the filamentous freshwater cyanobacterium Nostoc sp. strain 152. Appl. Environ. Microbiol. 1990, 56, 2650-2657.
60. Oksanen, I.; Jokela, J.; Fewer, D.P.; Wahlsten, M.; Rikkinen, J.; Sivonen, K. Discovery of rare and highly toxic microcystins from lichen-associated cyanobacterium Nostoc sp. strain IO-102-I. Appl. Environ. Microbiol. 2004, 70, 5756-5763.
61. Bolch, C.; Blackburn, S. Isolation and purification of Australian isolates of the toxic cyanobacterium; Microcystis aeruginosa; Kütz. J. Appl. Phycol. 1996, 8, 5-13.
62. Fujii, K.; Ikai, Y.; Mayumi, T.; Oka, H.; Suzuki, M.; Harada, K.-I. A nonempirical method using LC/MS for determination of the absolute configuration of constituent amino acids in a peptide: Elucidation of limitations of Marfey's method and of its separation mechanism. Anal. Chem. 1997, 69, 3346-3352.
63. Marfey, P. Determination of d-amino acids. II. Use of a bifunctional reagent, 1, 5-difluoro-2, 4-dinitrobenzene. Carlsberg Res. Commun. 1984, 49, 591-596.