Combined LC-MS/MS and Molecular Networking Approach Reveals New Cyanotoxins from the 2014 Cyanobacterial Bloom in Green Lake, Seattle

Environmental Science and Technology

Volumn 49, Issue 24, 2015, Pages 14301-14310

  Teta, Roberta ^a   Della Sala, Gerardo ^a   Glukhov, Evgenia ^b   Gerwick, Lena ^b   Gerwick, William H ^b   Mangoni, Alfonso ^a   Costantino, Valeria ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PEPTIDES; RNA; TOXIC MATERIALS;

ANALYSIS OF LIQUIDS; BIOSYNTHETIC GENE; CYANOBACTERIAL BLOOMS; CYCLIC PEPTIDES; HARMFUL ALGAL BLOOMS; METAGENOMIC ANALYSIS; MICROCYSTIS AERUGINOSA; STRUCTURE ELUCIDATION;

LAKES;

BACTERIAL TOXIN; CYANOTOXIN; CYCLOPEPTIDE; FERINTOIC ACID C; FERINTOIC ACID D; HEXAPEPTIDE; INTERNAL TRANSCRIBED SPACER; MICROCYSTIN; MICROCYSTIN MHTYR; RIBOSOME RNA; RNA 16S; TOXIN; UNCLASSIFIED DRUG; THIOL DERIVATIVE;

ALGAL BLOOM; CYANOBACTERIUM; LAKE WATER; MASS SPECTROMETRY; MOLECULAR ANALYSIS; RNA; TOXIN;

ALGAL BLOOM; ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BIOSYNTHESIS; CONTROLLED STUDY; CYANOBACTERIUM; GENE SEQUENCE; LAKE; LIQUID CHROMATOGRAPHY TANDEM MASS SPECTROMETRY; METAGENOMICS; MICROCYSTIS AERUGINOSA; MOLECULAR MODEL; MOLECULAR NETWORKING; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN METHYLATION; TANDEM MASS SPECTROMETRY; TOXIN STRUCTURE; UNITED STATES; ANALYSIS; CHEMISTRY; GENETICS; LIQUID CHROMATOGRAPHY; METAGENOME; METHYLATION; MICROCYSTIS; PROCEDURES; STANDARD; WASHINGTON;

SEATTLE; UNITED STATES; WASHINGTON [UNITED STATES];

ALGAE; CYANOBACTERIA; MICROCYSTIS AERUGINOSA;

CHROMATOGRAPHY, LIQUID; CYANOBACTERIA; HARMFUL ALGAL BLOOM; LAKES; METAGENOME; METHYLATION; MICROCYSTINS; MICROCYSTIS; REFERENCE STANDARDS; RNA, RIBOSOMAL; SULFHYDRYL COMPOUNDS; TANDEM MASS SPECTROMETRY; WASHINGTON;

EID: 84950151431     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.5b04415     Document Type: Article

References (53)

1. Pettit, G. R.; Kamano, Y.; Herald, C. L.; Tuinman, A. A.; Boettner, F. E.; Kizu, H.; Schmidt, J. M.; Baczynskyj, L.; Tomer, K. B.; Bontems, R. J. The isolation and structure of a remarkable marine animal antineoplastic constituent: dolastatin 10 J. Am. Chem. Soc. 1987, 109, 6883-6885 10.1021/ja00256a070
2. Schwartz, R. E.; Hirsch, C. F.; Sesin, D. F.; Flor, J. E.; Chartrain, M.; Fromtling, R. E.; Harris, G. H.; Salvatore, M. J.; Liesch, J. M.; Yudin, K. Pharmaceuticals from cultured algae J. Ind. Microbiol. 1990, 5, 113-123 10.1007/BF01573860
3. Gerwick, W. H.; Proteau, P. J.; Nagle, D. G.; Hamel, E.; Blokhin, A.; Slate, D. L. Structure of curacin A, a novel antimitotic, antiproliferative, and brine shrimp toxic natural product from the marine cyanobacterium Lyngbya majuscula J. Org. Chem. 1994, 59, 1243-1245 10.1021/jo00085a006
4. Dixit, R. B.; Suseela, M. R. Cyanobacteria: potential candidates for drug discovery Antonie van Leeuwenhoek 2013, 103, 947-61 10.1007/s10482-013-9898-0
5. Della Sala, G.; Hochmuth, T.; Costantino, V.; Teta, R.; Gerwick, W.; Gerwick, L.; Piel, J.; Mangoni, A. Polyketide genes in the marine sponge Plakortis simplex: a new group of mono-modular type I polyketide synthases from sponge symbionts Environ. Microbiol. Rep. 2013, 5, 809-818 10.1111/1758-2229.12081
6. Della Sala, G.; Hochmuth, T.; Teta, R.; Costantino, V.; Mangoni, A. Polyketide synthases in the microbiome of the marine sponge Plakortis halichondrioides: a metagenomic update Mar. Drugs 2014, 12, 5425-5440 10.3390/md12115425
7. Luesch, H.; Moore, R. E.; Paul, V. J.; Mooberry, S. L.; Corbett, T. H. Isolation of dolastatin 10 from the marine cyanobacterium Symploca species VP642 and total stereochemistry and biological evaluation of its analogue symplostatin 1 J. Nat. Prod. 2001, 64, 907-910 10.1021/np010049y
8. Esposito, G.; Teta, R.; Miceli, R.; Ceccarelli, L. S.; Della Sala, G.; Camerlingo, R.; Irollo, E.; Mangoni, A.; Pirozzi, G.; Costantino, V. Isolation and assessment of the in vitro anti-tumor activity of smenothiazole A and B, chlorinated thiazole-containing peptide/polyketides from the caribbean sponge Mar. Drugs 2015, 13, 444-459 16. 10.3390/md13010444
9. Edwards, D. J.; Marquez, B. L.; Nogle, L. M.; McPhail, K.; Goeger, D. E.; Roberts, M. A.; Gerwick, W. H. Structure and biosynthesis of the jamaicamides, new mixed polyketide-peptide neurotoxins from the marine cyanobacterium Lyngbya majuscula Chem. Biol. 2004, 11, 817-823 10.1016/j.chembiol.2004.03.030
10. Carvalho, L.; McDonald, C.; de Hoyos, C.; Mischke, U.; Phillips, G.; Borics, G.; Poikane, S.; Skjelbred, B.; Solheim, A. L.; Van Wichelen, J.; Cardoso, A. C. Sustaining recreational quality of European lakes: minimizing the health risks from algal blooms through phosphorus control J. Appl. Ecol. 2013, 50, 315-323 10.1111/1365-2664.12059
11. Digamber Rao, B.; Babu Ramesh, M.; Ellaswamy, N. Cyanotoxins and their potential applications: A review Nat. Environ. Poll. Technol. 2015, 14, 203-209
12. Rao, P. V.; Gupta, N.; Bhaskar, A. S.; Jayaraj, R. Toxins and bioactive compounds from cyanobacteria and their implication on human health J. Environ. Biol. 2002, 23, 215-224
13. USEPA. EPA FY 2016 Congressional Justification. Report EPA-190-R-15-001. United States Environmental Agency: Washington, DC, 2015.
14. Watrous, J.; Roach, P.; Alexandrov, T.; Heath, B. S.; Yang, J. Y.; Kersten, R. D.; van der Voort, M.; Pogliano, K.; Gross, H.; Raaijmakers, J. M.; Moore, B. S.; Laskin, J.; Bandeira, N.; Dorrestein, P. C. Mass spectral molecular networking of living microbial colonies Proc. Natl. Acad. Sci. U. S. A. 2012, 109, E1743-E1752 10.1073/pnas.1203689109
15. Crowley, B. M.; Mori, Y.; McComas, C. C.; Tang, D.; Boger, D. L. Total Synthesis of the Ristocetin Aglycon J. Am. Chem. Soc. 2004, 126, 4310-4317 10.1021/ja039795a
16. ProteoWizard Software Foundation; http://proteowizard.sourceforge.net/tools.shtml (accessed May 11, 2015).
17. UCSD ComputationalMass Spectrometer Website; http://gnps.ucsd.edu/ (accessed July 29, 2015).
18. Cytoscape Software; http://www.cytoscape.org/ (accessed June 15, 2015).
19. Cytoscape Software FM3 plug-in; http://apps.cytoscape.org/apps/fm3 (accessed June 15, 2015).
20. Boutte, C.; Grubisic, S.; Balthasart, P.; Wilmotte, A. Testing of primers for the study of cyanobacterial molecular diversity by DGGE J. Microbiol. Methods 2006, 65, 542-550 10.1016/j.mimet.2005.09.017
21. Janse, I.; Meima, M.; Kardinaal, W. E. A.; Zwart, G. High resolution differentiation of cyanobacteria by using rRNA internal transcribed spacer denaturing gradient gel electrophoresis Appl. Environ. Microbiol. 2003, 69, 6634-6643 10.1128/AEM.69.11.6634-6643.2003
22. Brett, N. A.; Dittmann, E.; Rouhiainen, L. R.; Bass, A.; Schaub, V.; Sivonen, K.; Borner, T. Nonribosomal Peptide Synthesis and Toxigenicity of Cyanobacteria J. Bacteriol. 1999, 181, 4089-4097
23. Cole, J. R.; Wang, Q.; Cardenas, E.; Fish, J.; Chai, B.; Farris, R. J.; Kulam-Syed-Mohideen, A. S.; McGarrell, D. M.; Marsh, T.; Garrity, G. M.; Tiedje, J. M. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis Nucleic Acids Res. 2009, 37, D141-D145 10.1093/nar/gkn879
24. Altschul, S. F.; Madden, T. L.; Schaffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 1997, 25, 3389-3402 10.1093/nar/25.17.3389
25. Yang, J. Y.; Sanchez, L. M.; Rath, C. M.; Liu, X.; Boudreau, P. D.; Bruns, N.; Glukhov, E.; Wodtke, A.; de Felicio, R.; Fenner, A.; Wong, W. R.; Linington, R. G.; Zhang, L.; Debonsi, H. M.; Gerwick, W. H.; Dorrestein, P. C. Molecular Networking as a Dereplication Strategy J. Nat. Prod. 2013, 76, 1686-1699 10.1021/np400413s
26. Carmichael, W. W.; Beasley, V.; Bunner, D. L.; Eloff, J. N.; Falconer, I.; Gorham, P.; Harada, K.; Krishnamurthy, T.; Yu, M. J.; Moore, R. E. Naming of cyclic heptapeptide toxins of cyanobacteria (blue-green algae) Toxicon 1988, 26, 971-973 10.1016/0041-0101(88)90195-X
27. Williams, D. E.; Craig, M.; Holmes, C. F. B.; Andersen, R. J. Ferintoic acids A and B, new cyclic hexapeptides from the freshwater cyanobacterium Microcystis aeruginosa J. Nat. Prod. 1996, 59, 570-575 10.1021/np960108l
28. Portmann, C.; Blom, J. F.; Gademann, K.; Juttner, F. Aerucyclamides A and B: isolation and synthesis of toxic ribosomal heterocyclic peptides from the cyanobacterium Microcystis aeruginosa PCC 7806 J. Nat. Prod. 2008, 71, 1193-1196 10.1021/np800118g
29. Tillet, D.; Dittman, E.; Erhard, M.; Von Dörhen, 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 10.1016/S1074-5521(00)00021-1
30. Van Wagoner, R. M.; Drummond, A. K.; Wright, J. L. C. Biogenetic diversity of cyanobacterial metabolites Adv. Appl. Microbiol. 2007, 61, 89-217 10.1016/S0065-2164(06)61004-6
31. Puddick, J. Spectroscopic Investigations of oligopeptides from aquatic cyanobacteria: Characterisation of new oligopeptides, development of microcystin quantification tools and investigations into microcystin production. Ph.D. Thesis, University of Waikato, Hamilton, New Zealand, 2013; http://researchcommons.waikato.ac.nz/handle/10289/7289 (accessed October 10, 2015).
32. Mackintosh, C.; Beattie, K. A.; Klumpp, S.; Cohen, P.; Codd, G. A. Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants FEBS Lett. 1990, 264, 187-192 10.1016/0014-5793(90)80245-E
33. Carmichael, W. W. Cyanobacteria secondary metabolites-the cyanotoxins J. Appl. Bacteriol. 1992, 72, 445-459 10.1111/j.1365-2672.1992.tb01858.x
34. Liu, W.-T.; Ng, J.; Meluzzi, D.; Bandeira, N.; Gutierrez, M.; Simmons, T. L.; Schultz, A. W.; Linington, R. G.; Moore, B. S.; Gerwick, W. H.; Pevzner, P. A.; Dorrestein, P. C. Interpretation of Tandem Mass Spectra Obtained from Cyclic Nonribosomal Peptides Anal. Chem. 2009, 81, 4200-4209 10.1021/ac900114t
35. Mayumi, T.; Kato, H.; Imanishi, S.; Kawasaki, Y.; Hasegawa, M.; Harada, K. Structural characterization of microcystins by LC/MS/MS under ion trap conditions J. Antibiot. 2006, 59, 710-719 10.1038/ja.2006.95
36. Benke, P. I.; Vinay Kumar, M. C. S.; Pan, D.; Swarup, S. A mass spectrometry-based unique fragment approach for the identification of microcystins Analyst 2015, 140, 1198-1206 10.1039/C4AN01702A
37. Namikoshi, M.; Sun, F.; Choi, B. W.; Rinehart, K. L.; Carmichael, W. W.; Evans, W. R.; Beasley, V. R. 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. 1995, 60, 3671-3679 10.1021/jo00117a017
38. Sano, T.; Takagi, H.; Nagano, K.; Nishikawa, M.; Kaya, K. Accurate LC-MS analyses for microcystins using per-15N-labeled microcystins Anal. Bioanal. Chem. 2011, 399, 2511-2516 10.1007/s00216-010-4639-y
39. Medina, R. A.; Goeger, D. E.; Hills, P.; Mooberry, S. L.; Huang, N.; Romero, L. I.; Ortega-Barria, E.; Gerwick, W. H.; McPhail, K. L. Coibamide A, a Potent Antiproliferative Cyclic Depsipeptide from the Panamanian Marine Cyanobacterium Leptolyngbya sp J. Am. Chem. Soc. 2008, 130, 6324-6325 10.1021/ja801383f
40. 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. Sci. Technol. 2012, 46, 8937-8944 10.1021/es301808h
41. Harada, K.; Fujii, K.; Shimada, T.; Suzuki, M.; Sano, H.; Adachi, K.; Carmichael, W. W. Two cyclic peptides, anabaenopeptins, a third group of bioactive compounds from the cyanobacterium Anabaena flos-aquae NRC 525-17 Tetrahedron Lett. 1995, 36, 1511-1514 10.1016/0040-4039(95)00073-L
42. Fujii, K.; Sivonen, K.; Nakano, T.; Harada, K. I. Structural elucidation of cyanobacterial peptides encoded by peptide synthetase gene in Anabaena species Tetrahedron 2002, 58, 6863-6871 10.1016/S0040-4020(02)00747-0
43. Gkelis, S.; Lanaras, T.; Sivonen, K. The presence of microcystins and other cyanobacterial bioactive peptides in aquatic fauna collected from Greek freshwaters Aquat. Toxicol. 2006, 78, 32-41 10.1016/j.aquatox.2006.02.001
44. Itou, Y.; Suzuki, S.; Ishida, K.; Murakami, M. Anabaenopeptins G and H, potent carboxypeptidase A inhibitors from the cyanobacterium Oscillatoria agardhii (NIES-595) Bioorg. Med. Chem. Lett. 1999, 9, 1243-1246 10.1016/S0960-894X(99)00191-2
45. Kruger, T.; Christian, B.; Luckas, B. Development of an analytical method for the unambiguous structure elucidation of cyclic peptides with special appliance for hepatotoxic desmethylated microcystins Toxicon 2009, 54, 302-312 10.1016/j.toxicon.2009.04.020
46. Stachelhaus, T.; Mootz, H. D.; Marahiel, M. A. The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases Chem. Biol. 1999, 6, 493-505 10.1016/S1074-5521(99)80082-9
47. Tooming-Klunderud, A.; Fewer, D. P.; Rohrlack, T. et al. Evidence for positive selection acting on microcystin synthetase adenylation domains in three cyanobacterial genera BMC Evol. Biol. 2008, 8, 256 10.1186/1471-2148-8-256
48. Conti, E.; Stachelhaus, T.; Marahiel, M. A.; Brick, P. Structural basis for the activation of phenylalanine in the nonribosomal biosynthesis of gramicidin S EMBO 1997, 16, 4174-4183 10.1093/emboj/16.14.4174
49. Mikalsen, B. G.; Boison, O. M.; Skulberg, J.; Fastner, W.; Davies, T. M. et al. Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis Strains J. Bacteriol. 2003, 185, 2774-2785 10.1128/JB.185.9.2774-2785.2003
50. Rouhiainen, L.; Jokela, J.; Fewer, D. P.; Urmann, M.; Sivonen, K. Two Alternative Starter Modules for the Non-Ribosomal Biosynthesis of Specific Anabaenopeptin Variants in Anabaena (Cyanobacteria) Chem. Biol. 2010, 17, 265-273 10.1016/j.chembiol.2010.01.017
51. Guidelines for safe recreational water environments. Volume 1: Coastal and fresh waters; http://www.who.int/water-sanitation-health/bathing/srwe1execsum/en/index6.html# (accessed August 31, 2015).
52. Lega, M.; Kosmatka, J.; Ferrara, C.; Russo, F.; Napoli, R. M. A.; Persechino, G. Using Advanced Aerial Platforms and Infrared Thermography to Track Environmental Contamination Environ. Forensics 2012, 13, 332-338 10.1080/15275922.2012.729002
53. 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 10.1128/AEM.70.10.5756-5763.2004