Non-ribosomal peptides produced by Brazilian cyanobacterial isolates with antimicrobial activity

Microbiological Research

Volumn 166, Issue 3, 2011, Pages 161-175

  Silva Stenico, Maria Estela ^a   Silva, Caroline Souza Pamplona ^a   Lorenzi, Adriana Sturion ^a   Shishido, Tânia Keiko ^a   Etchegaray, Augusto ^b   Lira, Simone Possedente ^a   Moraes, Luiz Alberto Beraldo ^a   Fiore, Marli Fátima ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b PONTIFÍCIA UNIVERSIDADE CATÓLICA DE CAMPINAS   (Brazil)

Author keywords

Aeruginosin; Cyanobacteria; Cyanopeptolin; Genetic diversity; Mass spectrometry; Natural products

Indexed keywords

AERUGINOSIN; CYANOBACTERIA; CYANOPEPTOLIN; GENETIC DIVERSITY; NATURAL PRODUCTS;

BIODIVERSITY; CELL CULTURE; ESTERS; GENES; MASS SPECTROMETRY; METHANOL; PEPTIDES; POLYMERASE CHAIN REACTION;

BACTERIA;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; MICROCYSTIN; NONRIBOSOMAL PEPTIDE SYNTHETASE; PEPTIDE SYNTHASE; POLYKETIDE SYNTHASE; PROTEINASE INHIBITOR; SIDEROPHORE;

ANTIMICROBIAL ACTIVITY; BIOTECHNOLOGY; CYANOBACTERIUM; GENETIC ANALYSIS; INHIBITOR; MASS SPECTROMETRY; METABOLITE; METHANOL; PATHOGEN; PEPTIDE; POLYMERASE CHAIN REACTION; SIDEROPHORE; YEAST;

ARTICLE; BIOSYNTHESIS; BRAZIL; CHEMISTRY; CYANOBACTERIUM; DRUG DEVELOPMENT; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC VARIABILITY; GENETICS; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; MICROBIOLOGICAL EXAMINATION; POLYMERASE CHAIN REACTION;

ANTI-INFECTIVE AGENTS; BACTERIAL PROTEINS; BRAZIL; CYANOBACTERIA; DRUG DISCOVERY; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENETIC VARIATION; MASS SPECTROMETRY; MICROBIAL SENSITIVITY TESTS; MICROCYSTINS; PEPTIDE SYNTHASES; POLYKETIDE SYNTHASES; POLYMERASE CHAIN REACTION; PROTEASE INHIBITORS; SIDEROPHORES;

BACTERIA (MICROORGANISMS); CYANOBACTERIA; CYLINDROSPERMOPSIS; CYLINDROSPERMOPSIS RACIBORSKII; FISCHERELLA SP.; MICROCYSTIS AERUGINOSA; SYNECHOCOCCUS ELONGATUS;

EID: 79951943306     PISSN: 09445013     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micres.2010.04.002     Document Type: Article

References (60)

1. Allen M.B., Arnon D.I. Studies on nitrogen-fixing blue-green algae. 1. Growth and nitrogen fixation by Anabaena cylindrica Lemm. Plant Phys 1955, 30:366-372.
2. Allen M.B. Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 1968, 4:1-4.
3. Azevedo S.M.F.O., Evans W.R., Carmichael W.W., Namikoshi M. First report of microcystins from a Brazilian isolate of the cyanobacterium Microcystis aeruginosa. J Appl Phycol 1994, 64:261-265.
4. Barrios-Llerena M.E., Burja A.M., Wright P.C. Genetic analysis of polyketide synthase and peptide synthetase genes in cyanobacteria as a mining tool for secondary metabolites. J Ind Microbiol Biotechnol 2007, 34:443-456.
5. Beiderbeck H., Taraz K., Budzikiewicz H., Walsby A.E. Anachelin, the siderophore of the cyanobacterium Anabaena cylindrica CCAP 1403/2A. Z Naturforsch 2000, 55:681-687.
6. Beyer S., Kunze B., Silakowski B., Müller R. Metabolic diversity in myxobacteria: identification of the myxalamid and the stigmatellin biosynthetic gene cluster of Stigmatella aurantiaca Sg a15 and a combined polyketide-(poly) peptide gene cluster from the epothilone producing strain Sorangium cellulosum So ce90. Biochem Biophys Acta 1999, 1445:185-195.
7. Biondi N., Tredici M.R., Taton A., Wilmotte A., Hodgson D.A., Losi D., et al. Cyanobacteria from benthic mats of Antarctic lakes as a source of new bioactivities. J Appl Microb 2008, 105:105-115.
8. Birnboim H.C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 1979, 7:1513-1518.
9. Cadel-Six S., Dauga C., Castets A.M., Rippka R., Bouchier C., Tandeau de Marsac N., et al. Halogenase genes in nonribosomal peptide synthetase gene clusters of Microcystis (cyanobacteria): sporadic distribution and evolution. Mol Biol Evol 2008, 25:2031-2041.
10. Coleman J.E., Wright J.L. Radiosumin B, an unusual dipeptide from the cyanobacterium Microcystis aeruginosa. J Nat Prod 2001, 64:668-670.
11. Chu F.S., Huang X., Wei R.D., Carmichael W.W. Production and characterization of antibodies against microcystins. Appl Environ Microbiol 1989, 55:1928-1933.
12. Czarnecki O., Henning M., Lippert I., Welker M. Identification of peptide metabolites of Microcystis (cyanobacteria) that inhibit trypsin-like activity in planktonic herbivorous Daphnia (Cladocera). Environ Microbiol 2006, 8:77-87.
13. de Caire G.Z., de Cano M.S., de Mulé M.C.Z., de Halperin D.R. Screening of cyanobacterial bioactive compounds against human pathogens. Int J Exp Bot Phyton 1993, 54:59-65.
14. Erhard M., von Döhren H., Jungblut P.R. Rapid identification of the new anabaenopeptin G from Planktothrix agardhii HUB 011 using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 1999, 13:337-343.
15. Ersmark K., DelValle J.R., Hanessian S. Chemistry and biology of the aeruginosin family of serine protease inhibitors. Angew Chem Int Ed Engl 2008, 47:1202-1223.
16. Etchegaray A., Rabelo E., Dieckmann R., Moon D.H. Algicide production by filamentous cyanobacterium Fischerella sp. CENA 19. J Appl Phycol 2004, 16:237-243.
17. Fiore M.F., Moon D.H., Tsai S.M., Lee H., Trevors J.T. Miniprep DNA isolation from unicellular and filamentous cyanobacteria. J Microbiol Methods 2000, 39:159-169.
18. Fiore M.F., Genuário D.B., da Silva C.S.P., Shishido T.K., Moraes L.A.B., Cantúsio Neto R., et al. Microcystin production by a freshwater spring cyanobacterium of the genus Fischerella. Toxicon 2009, 53:754-761.
19. Frangeul L., Quillardet P., Castets A.M., Humbert J.F., Matthijs H.C.P., Cortez D., et al. Highly plastic genome of Microcystis aeruginosa PCC7806, anubiquitous toxic freshwater cyanobacterium. BMC Genomics 2008, 9:274.
20. Goldman S.J., Lammers P.J., Berman M.S., Sanders-Loehr J. Siderophore-mediated iron uptake in different strains of Anabaena sp. J Bacteriol 1983, 156:1144-1150.
21. Gorham P.R., McLachlan J., Hammer T., Kim W.K. Isolation and culture of toxic strains of Anabaena flos-aquae (Lyngb.) de Bréb. Verh Int Verein Theor Angew Limnol 1964, 15:796-804.
22. Harada K., Fujii K., Shimada T., Suzuki M., Sano H., Adachi K., et al. 2 cyclic-peptides, anabaenopeptins, a 3rd group of bioactive compounds from the cyanobacterium Anabaena-flos-aquae NRC-525-17. Tetrahedron Lett 1995, 36:1511-1514.
23. Harada K., Mayumi T., Shimada T., Fujii K., Kondo F., Park H.D., et al. Co-production of microcystins and aeruginopeptins by natural cyanobacterial bloom. Environ Toxicol 2001, 16:298-305.
24. Ishida K., Murakami M., Matsuda H., Yamaguchi K. Micropeptin 90, a plasmin and trypsin inhibitor from the blue-green alga Microcystis aeruginosa (NIES-90). Tetrahedron Lett 1995, 36:3535-3538.
25. Ishida K., Matsuda H., Murakami M., Yamaguchi K. Kawaguchipeptin B, an antibacterial cyclic undecapeptide from the cyanobacterium Microcystis aeruginosa. J Nat Prod 1997, 60:724-726.
26. Ishida K., Welker M., Christiansen G., Cadel-Six S., Bouchier C., Dittmann E., et al. Plasticity and evolution of aeruginosin biosynthesis in cyanobacteria. Appl Environ Microbiol 2009, 75:2017-2026.
27. Ito Y., Butler A. Structure of synechobactins, new siderophores of the marine cyanobacterium Synechococcus sp. PCC7002. Limnol Oceanogr 2005, 50:1918-1923.
28. Jaki B., Orjala J., Bürgi H.-R., Sticher O. Biological screening of cyanobacteria for antimicrobial and molluscicidal activity, brine shrimp lethality, and cytotoxicity. Pharm Biol 1999, 37:138-143.
29. Kalaitzis J.A., Lauro F.M., Neilan B.A. Mining cyanobacterial genomes for genes encoding complex biosynthetic pathways. Nat Product Rep 2009, 26:1447-1465.
30. Kaya K., Sano T., Beattie K.A., Codd G.A. Nostocyclin, a novel 3-amino-6-hydroxy-2-piperidone-containing cyclic depsipeptide from the cyanobacterium Nostoc sp. Tetrahedron Lett 1996, 37:6725-6728.
31. Kreitlow S., Mundt S., Lindequist U. Cyanobacteria - a potential source of new biologically active substances. J Biotechnol 1999, 70:61-66.
32. Kumar S., Tamura K., Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 2004, 5:150-163.
33. Lawrence J.F., Niedzwiadek B., Menard C., Lau B.P., Lewis D., Kuper-Goodman T., et al. Comparison of liquid chromatography/mass spectrometry. ELISA, and phosphatase assay for the determination of microcystins in blue-green algae products. J AOAC Int 2001, 84:1035-1044.
34. Marahiel M.A., Stachelhaus T., Mootz H.D. Modular peptide synthetases involved in non-ribosomal peptide synthesis. Chem Rev 1997, 97:2651-2673.
35. Meißner K., Dittmann E., Börner T. Toxic and nontoxic strains of the cyanobacterium Microcystis aeruginosa contain sequences homologous to peptide synthetase genes. FEMS Microbiol Lett 1996, 135:295-303.
36. Miethke M., Marahiel M.A. Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 2007, 71:413-451.
37. Moffitt M.C., Neilan B.A. Characterization of the nodularin synthetase gene cluster and proposed theory of the evolution of cyanobacterial hepatotoxins. Appl Environ Microbiol 2004, 70:6353-6362.
38. Murakami M., Sun Q., Ishida K., Matsuda H., Okino T., Yamaguchi K. Microviridins, elastase inhibitors from the cyanobacterium Nostoc minutum (NIES-26). Phytochemistry 1997, 45:1197-1202.
39. Nagle D.G., Gerwick W.H. Nakienones A-C and nakitriol, new cytotoxic cyclic C11 metabolites from an Okinawan cyanobacterial (Synechocystis sp.) overgrowth of coral. Tetrahedron Lett 1995, 36:849-852.
40. Namikoshi M., Rinehart K.L. Bioactive compounds produced by cyanobacteria. J Ind Microbiol 1996, 17:373-384.
41. Neilan B.A., Dittmann E., Rouhiainen L., Bass R.A., Schaub V., Sivonen K., et al. Nonribosomal peptide synthesis and toxigenicity of cyanobacteria. J Bacteriol 1999, 181:4089-4097.
42. Neuhof T., Schmieder P., Preussel K., Dieckmann R., Pham H., Bartl F., et al. Hassallidin A, a glycosylated lipopeptide with antifungal activity from the cyanobacterium Hassallia sp. J Nat Prod 2005, 68:695-700.
43. Oliveira A.C.P., Magalhães V.F., Soares R.M., Azevedo S.M.F.O. Influence of drinking water composition on quantitation and biological activity of dissolved microcystin (cyanotoxin). Environ Toxicol 2005, 20:126-130.
44. Pawar S.T., Puranik P.R. Screening of terrestrial and freshwater halotolerant cyanobacteria for antifungal activities. World J Microbiol Biotechnol 2008, 24:1019-1025.
45. Ploutno A., Carmeli S. Modified peptides from a water bloom of the cyanobacterium Nostoc sp. Tetrahedron 2002, 58:9949-9957.
46. Ploutno A., Shoshan M., Carmeli S. Three novel protease inhibitors from a natural bloom of the cyanobacterium Microcystis aeruginosa. J Nat Prod 2002, 65:973-978.
47. Rounge T.B., Rohrlack T., Tooming-Klunderud A., Kristensen T., Jakobsen K.S. Comparison of cyanopeptolin genes in Planktothrix, Microcystis, and Anabaena strains: evidence for independent evolution within each genus. Appl Environ Microb 2007, 73:7322-7330.
48. Schwyn B., Neilands J.B. Universal chemical assay for the detection and determination of siderophores. Anal Biochem 1987, 160:46-56.
49. Sant'Anna CL, Carvalho LR, Fiore MF, Silva-Stenico ME, Lorenzi AS, Rios FR, et al. Highly toxic Microcystis aeruginosa strain, isolated from São Paulo-Brazil, produce hepatotoxins and paralytic shellfish poison neurotoxins. Neurotoxicity Res 2010; doi:10.1007/s12640-010-9177-z.
50. Silva-Stenico M.E., Pacheco F.T.H., Rodrigues J.L.M., Tsai S.M. Growth and siderophore production of Xylella fastidiosa under iron-limited condition. Microb Res 2005, 160:429-436.
51. Silva-Stenico M.E., Cantúsio Neto R., Alves I.R., Moraes L.A.B., Shishido T.K., Fiore M.F. Hepatotoxin microcystin-LR extraction optimization. J Braz Chem Soc 2009, 20:535-542.
52. Singh I.P., Milligan K.E., Gerwick W.H. Tanikolide, a toxic and antifungal lactone from the marine cyanobacterium Lyngbya majuscule. J Nat Prod 1999, 62:1333-1335.
53. Svircev Z., Cetojevic-Simin D., Simeunovic J., Karaman M., Stojanovic D. Antibacterial, antifungal and cytotoxic activity of terrestrial cyanobacterial strains from Serbia. Sci China Ser C-Life Sci 2008, 51:941-947.
54. Tillett D., Dittmann E., Erhard M., von Dohren H., Borner 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.
55. Tsukamoto S., Painuly P., Young K.A., Yang X.M., Shimizu Y., Cornell L. Microcystilide-A - a novel cell-differentiation-promoting depsipeptide from Microcystis aeruginosa NO-15-1840. J Am Chem Soc 1993, 115:11046-11047.
56. Volk R.-B., Furkert F.H. Antialgal, antibacterial and antifungal activity of two metabolites produced and excreted by cyanobacteria during growth. Microbiol Res 2006, 161:180-186.
57. Welker M., Brunke M., Preussel K., Lippert I., von Döhren H. Diversity and distribution of Microcystis (cyanobacteria) oligopeptide chemotypes from natural communities studied by single-colony mass spectrometry. Microbiology 2004, 150:1785-1796.
58. Winkelmann G. Specificity of iron transport in bacteria and fungi. Handbook of microbial chelates 1991, 65-106. CRC. G. Winkelmann (Ed.).
59. Zainuddin E.N., Mundt S., Wegner U., Mentel R. Cyanobacteria a potential source of antiviral substances against influenza virus. Med Microbiol Immunol 2002, 191:181-182.
60. Zulpa G., Zaccaro M.C., Boccazzi F., Parada J.L., Storni M. Bioactivity of intra and extracellular substances from cyanobacteria and lactic acid bacteria on " wood blue stain" fungi. Biol Control 2003, 27:345-348.