Genetic variation of adenylation domains of the anabaenopeptin synthesis operon and evolution of substrate promiscuity

Journal of Bacteriology

Volumn 193, Issue 15, 2011, Pages 3822-3831

  Christiansen, Guntram ^a   Philmus, Benjamin ^b,c   Hemscheidt, Thomas ^b   Kurmayer, Rainer ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b UNIVERSITY OF HAWAII   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANABAENOPEPTIN; ARGININE; HEXAPEPTIDE; PEPTIDE SYNTHASE; TYROSINE; UNCLASSIFIED DRUG;

ADENYLATION; ARTICLE; BACTERIUM; CODON; GENE INACTIVATION; GENETIC VARIABILITY; IN VITRO STUDY; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; OPERON; PEPTIDE SYNTHESIS; PHYLOGENY; PLANKTOTHRIX AGARDHII; POINT MUTATION; PRIORITY JOURNAL; PROTEIN STRUCTURE;

BACTERIAL PROTEINS; CYANOBACTERIA; EVOLUTION, MOLECULAR; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; OPERON; PEPTIDES, CYCLIC; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

CYANOBACTERIA; PLANKTOTHRIX; PLANKTOTHRIX AGARDHII;

EID: 79960390410     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00360-11     Document Type: Article

References (53)

1. Beresovsky, D., et al. 2006. Toxins and biologically active secondary metabolites of Microcystis sp. isolated from Lake Kinneret. Isr. J. Chem. 46:79-87.
2. Bonnard, I., et al. 2007. Total structure and inhibition of tumor cell proliferation of laxaphycins. J. Med. Chem. 50:1266-1279.
3. Bubik, A., B. Sedmak, M. Novinec, B. Lenarcic, and T. T. Lah. 2008. Cytotoxic and peptidase inhibitory activities of selected non-hepatotoxic cyclic peptides from cyanobacteria. Biol. Chem. 389:1339-1346.
4. Christiansen, G., J. Fastner, M. Erhard, T. Börner, and E. Dittmann. 2003. Microcystin biosynthesis in Planktothrix: genes, evolution, and manipulation. J. Bacteriol. 185:564-572.
5. Christiansen, G., C. Molitor, B. Philmus, and R. Kurmayer. 2008. Nontoxic strains of cyanobacteria are the result of major gene deletion events induced by a transposable element. Mol. Biol. Evol. 25:1695-1704.
6. Christiansen, G., et al. 2008. Isolation and structure determination of two microcystins and sequence comparisons of McyABC adenylation domains in Planktothrix species. J. Nat. Prod. 71:1881-1886.
7. Conti, E., T. Stachelhaus, M. A. Marahiel, and P. Brick. 1997. Structural basis for the activation of phenylalanine in the non-ribosomal biosynthesis of gramicidin S. EMBO J. 16:4174-4183.
8. Erhard, M., H. von Döhren, and P. Jungblut. 1999. 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. 13:337-343.
9. Felsenstein, J. 1989. PHYLIP-Phylogeny Inference Package (version 3.2). Cladistics 5:164-166.
10. Fewer, D. P., et al. 2007. Recurrent adenylation domain replacement in the microcystin synthetase gene cluster. BMC Evol. Biol. 7:183.
11. Fischbach, M. A., and C. T. Walsh. 2006. Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms. Chem. Rev. 106:3468-3496.
12. Franche, C., and T. Damerval. 1988. Test on nif probes and DNA hybridizations. Methods Enzymol. 167:803-808.
13. Frankmölle, W. P., G. Knübel, R. E. Moore, and G. M. L. Patterson. 1992. Antifungal cyclic peptides from the terrestrial blue-green alga Anabaena laxa. II. Structures of laxaphycins A, B, D and E. J. Antibiot. (Tokyo) 45:1458-1466.
14. Gkelis, S., T. Lanares, and K. Sivonen. 2006. The presence of microcystins and other cyanobacterial bioactive peptides in aquatic fauna collected from Greek freshwaters. Aquat. Toxicol. 78:32-41.
15. Golakoti, T., et al. 1995. Structure determination, conformational analysis, chemical stability studies, and antitumor evaluation of the cryptophycins. Isolation of 18 new analogs from Nostoc sp. strain GSV 224. J. Am. Chem. Soc. 117:12030-12049.
16. Golakoti, T., W. Y. Yoshida, S. Chaganty, and R. E. Moore. 2000. Isolation and structures of nostopeptolides A1, A2 and A3 from the cyanobacterium Nostoc sp. GSV224. Tetrahedron 56:9093-9102.
17. Grach-Pogrebinsky, O., and S. Carmeli. 2008. Three novel anabaenopeptins from the cyanobacterium Anabaena sp. Tetrahedron 64:10233-10238.
18. Harada, K., K. Fujii, T. Shimada, and M. Suzuki. 1995. Two cyclic peptides, anabaenopeptins, a third group of bioactive compounds from the cyanobacterium Anabaena flos-aquae NRC 525-17. Tetrahedron Lett. 36:1511-1514.
19. Hoffmann, D., J. M. Hevel, R. E. Moore, and B. S. Moore. 2003. Sequence analysis and biochemical characterization of the nostopeptolide A biosynthetic gene cluster from Nostoc sp. GSV224. Gene 311:171-180.
20. Ishida, K., et al. 2007. Biosynthetic pathway and structure analysis of aeruginoside 126A and B, cyanobacterial peptide glycosides bearing an unusual 2-carboxy-6-hydroxyoctahydroindole moiety. Chem. Biol. 14:565-576.
21. Itou, Y., S. Suzuki, K. Ishida, and M. Murakami. 1999. Anabaenopeptins G and H, potent carboxypeptidase A inhibitors from the cyanobacterium Oscillatoria agardhii (NIES-595). Bioorg. Med. Chem. Lett. 9:1243-1246.
22. Kosol, S., J. Schmidt, and R. Kurmayer. 2009. Variation in peptide net production and growth among strains of the toxic cyanobacterium Planktothrix spp. Eur. J. Phycol. 44:49-62.
23. Kurmayer, R., G. Christiansen, J. Fastner, and T. Börner. 2004. Abundance of active and inactive microcystin genotypes in populations of the toxic cyanobacterium Planktothrix spp. Environ. Microbiol. 6:831-841.
24. Kurmayer, R., G. Christiansen, M. Gumpenberger, and J. Fastner. 2005. Genetic identification of microcystin ecotypes in toxic cyanobacteria of the genus Planktothrix. Microbiology 151:1525-1533.
25. Kurmayer, R., E. Dittmann, J. Fastner, and I. Chorus. 2002. Diversity of microcystin genes within a population of the toxic cyanobacterium Microcystis spp. in Lake Wannsee (Berlin, Germany). Microb. Ecol. 43:107-118.
26. Kurmayer, R., and M. Gumpenberger. 2006. Diversity of microcystin genotypes among populations of the filamentous cyanobacteria Planktothrix rubescens and Planktothrix agardhii. Mol. Ecol. 15:3849-3861.
27. Lipmann, F. 1971. Attempts to map a process evolution of peptide biosynthesis. Science 173:875-884.
28. Marahiel, M. A., T. Stachelhaus, and H. D. Mootz. 1997. Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 97: 2651-2674.
29. Mehner, C., et al. 2008. New peptolides from the cyanobacterium Nostoc insulare as selective and potent inhibitors of human leukocyte elastase. Chembiochem 9:2692-2703.
30. Mikalsen, B., et al. 2003. Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains. J. Bacteriol. 185:2774-2785.
31. Murakami, M., H. J. Shin, H. Matsuda, K. Ishida, and K. Yamaguchi. 1997. A cyclic peptide, anabaenopeptin B, from the cyanobacterium Oscillatoria agardhii. Phytochemistry 44:449-452.
32. Murakami, M., S. Suzuki, Y. Itou, S. Kodani, and K. Ishida. 2000. New anabaenopeptins, potent carboxypeptidase-A inhibitors from the cyanobacterium Aphanizomenon flos-aquae. J. Nat. Prod. 63:1280-1282.
33. Neilan, B. A., et al. 1999. Nonribosomal peptide synthesis and toxigenicity of cyanobacteria. J. Bacteriol. 181:4089-4097.
34. Okumura, H., B. Philmus, C. Portmann, and T. Hemscheidt. 2009. Homotyrosine-containing cyanopeptolins 880 and 960 and anabaenopeptins 908 and 915 from Planktothrix agardhii CYA 126/8. J. Nat. Prod. 72:172-176.
35. O'Maille, P. E., et al. 2008. Quantitative exploration of the catalytic landscape separating divergent plant sesquiterpene synthases. Nat. Chem. Biol. 4:617-623.
36. Philmus, B., G. Christiansen, W. Yoshida, and T. Hemscheidt. 2008. Posttranslational modification in microviridin biosynthesis. Chembiochem 9:3066-3073.
37. Rausch, C., T. Weber, O. Kohlbacher, W. Wohlleben, and D. Huson. 2005. Specificity prediction of adenylation domains in nonribosomal peptide synthetases (NRPS) using transductive support vector machines (TSVMs). Nucleic Acids Res. 33:5799-5808.
38. Reshef, V., and S. Carmeli. 2002. Schizopeptin 791, a new anabaenopeptinlike cyclic peptide from the cyanobacterium Schizothrix sp. J. Nat. Prod. 65:1187-1189.
39. Rouhiainen, L., J. Jokela, D. P. Fewer, M. Urmann, and K. Sivonen. 2010. Two alternative starter modules for the non-ribosomal biosynthesis of specific anabaenopeptin variants in Anabaena (Cyanobacteria). Chem. Biol. 17:265-273.
40. Sano, T., and K. Kaya. 1995. Oscillamide Y, a chymotrypsin inhibitor from toxic Oscillatoria agardhii. Tetrahedron Lett. 36:5933-5936.
41. Sano, T., T. Usui, K. Ueda, H. Osada, and K. Kaya. 2001. Isolation of new protein phosphatase inhibitors from two cyanobacteria species, Planktothrix spp. J. Nat. Prod. 64:1052-1055.
42. Sawyer, S. 1999. GENECONV: a computer package for the statistical detection of gene conversion. Distributed by the author. Department of Mathematics, Washington University, St. Louis, MO. http://www.math.wustl.edu/~sawyer/geneconv/index.html.
43. Shin, H. J., H. Matsuda, M. Murakami, and K. Yamaguchi. 1997. Anabaenopeptins E and F, two new cyclic peptides from the cyanobacterium Oscillatoria agardhii (NIES 204). J. Nat. Prod. 60:139-141.
44. Stachelhaus, T., H. D. Mootz, and M. A. Marahiel. 1999. The specificityconferring code of adenylation domains in nonribosomal peptide synthetases. Chem. Biol. 6:493-505.
45. Tooming-Klunderud, A., et al. 2008. Evidence for positive selection acting on microcystin synthetase adenylation domains in three cyanobacterial genera. BMC Evol. Biol. 8:256.
46. Walther, T., S. Renner, H. Waldmann, and H. D. Arndt. 2009. Synthesis and structure-activity correlation of a brunsvicamide-inspired cyclopeptide collection. Chembiochem 10:1153-1162.
47. Welker, M., and M. Erhard. 2007. Consistency between chemotyping of single filaments of Planktothrix rubescens (Cyanobacteria) by MALDI-TOF and the peptide patterns of strains determined by HPLC-MS. J. Mass Spectrom. 42:1062-1068.
48. Welker, M., and H. von Döhren. 2006. Cyanobacterial peptides-nature's own combinatorial biosynthesis. FEMS Microbiol. Rev. 30:530-563.
49. Williams, D. E., M. Craig, C. F. B. Holmes, and R. J. Andersen. 1996. Ferintoic acids A and B, new cyclic hexapeptides from the freshwater cyanobacterium Microcystis aeruginosa. J. Nat. Prod. 59:570-575.
50. Yamaki, H., N. Sitachitta, T. Sano, and K. Kaya. 2005. Two new chymotrypsin inhibitors isolated from the cyanobacterium Microcystis aeruginosa NIES-88. J. Nat. Prod. 68:14-18.
51. Yang, Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13:555-556.
52. Yang, Z., and R. Nielsen. 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol. 19:908-917.
53. Yang, Z. H., W. S. W. Wong, and R. Nielsen. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22:1107-1118.