Analysis of an inactive Cyanobactin biosynthetic gene cluster leads to discovery of new natural products from strains of the genus Microcystis

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Leikoski, Niina ^a   Fewer, David P ^a   Jokela, Jouni ^a   Alakoski, Pirita ^a   Wahlsten, Matti ^a   Sivonen, Kaarina ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CYANOBACTIN PEPTIDE; CYCLOPEPTIDE; DISULFIDE; NATURAL PRODUCT; PIRICYCLAMIDE PEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL OVERGROWTH; BACTERIAL STRAIN; CHEMICAL ANALYSIS; ESCHERICHIA COLI; GENE CLUSTER; GENETIC VARIABILITY; HETEROLOGOUS EXPRESSION; MICROCYSTIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDE SYNTHESIS; PHYLOGENY; PIR GENE; PROTEIN ANALYSIS; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; AMINO ACIDS; BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; DISULFIDES; ESCHERICHIA COLI; GENETIC VARIATION; MICROCYSTIS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PEPTIDES, CYCLIC; PHYLOGENY; RIBOSOMES; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84865429280     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043002     Document Type: Article

References (41)

1. Ishida K, Matsuda H, Murakami M, Yamaguchi K, (1996) Kawaguchipeptin A, a novel cyclic undecapeptide from cyanobacterium Microcystis aeruginosa (NIES-88). Tetrahedron 52: 9025-9030.
2. Ishida K, Matsuda H, Murakami M, Yamaguchi K, (1997) Kawaguchipeptin B, an antibacterial cyclic undecapeptide from the cyanobacterium Microcystis aeruginosa. J Nat Prod 60: 724-726.
3. Portmann C, Blom JF, Gademann K, Jüttner F, (2008) Aerucyclamides A and B: Isolation and synthesis of toxic ribosomal heterocyclic peptides from the cyanobacterium Microcystis aeruginosa PCC 7806. J Nat Prod 71: 1193-1196.
4. Sivonen K, Leikoski N, Fewer DP, Jokela J, (2010) Cyanobactins- ribosomal cyclic peptides produced by cyanobacteria. Appl Microbiol Biotechnol 86: 1213-1225.
5. Schmidt EW, Donia MS, (2009) Cyanobactin ribosomally synthesized peptides- a case of deep metagenome mining. Complex Enzymes in Microbial Natural Product Biosynthesis, Part A: Overview Articles and Peptides 458: 575.
6. Lee SW, Mitchell DA, Markley AL, Hensler ME, Gonzalez D, et al. (2008) Discovery of a widely distributed toxin biosynthetic gene cluster. Proc Natl Acad Sci U S A. 105: 5879-5884.
7. Donia MS, Schmidt EW, (2011) Linking chemistry and genetics in the growing cyanobactin natural products family. Chem Biol 18: 508-519.
8. McIntosh JA, Schmidt EW, (2010) Marine molecular machines: Heterocyclization in cyanobactin biosynthesis. ChemBioChem 11: 1413-1421.
9. McIntosh JA, Robertson CR, Agarwal V, Nair SK, Bulaj GW, et al. (2010) Circular logic: Nonribosomal peptide-like macrocyclization with a ribosomal peptide catalyst. J Am Chem Soc 132: 15499-15501.
10. Donia MS, Ravel J, Schmidt EW, (2008) A global assembly line for cyanobactins. Nat Chem Biol 4: 341-343.
11. McIntosh JA, Donia MS, Nair SK, Schmidt EW, (2011) Enzymatic basis of ribosomal peptide prenylation in cyanobacteria. J Am Chem Soc 133: 13698-13705.
12. Leikoski N, Fewer DP, Jokela J, Wahlsten M, Rouhiainen L, et al. (2010) Highly diverse cyanobactins in strains of the genus Anabaena. Appl Environ Microbiol 76: 701-709.
13. Schmidt EW, Nelson JT, Rasko DA, Sudek S, Eisen JA, et al. (2005) Patellamide A and biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc Natl Acad Sci U S A 102: 7315-7320.
14. Sudek S, Haygood MG, Youssef DTA, Schmidt EW, (2006) Structure of trichamide, a cyclic peptide from the bloom-forming cyanobacterium Trichodesmium erythraeum, predicted from the genome sequence. Appl Environ Microbiol 72: 4382-4387.
15. Ziemert N, Ishida K, Quillardet P, Bouchier C, Hertweck C, et al. (2008) Microcyclamide biosynthesis in two strains of Microcystis aeruginosa: From structure to genes and vice versa. Appl Environ Microbiol 74: 1791-1797.
16. Portmann C, Blom JF, Kaiser M, Brun R, Jüttner F, et al. (2008) Isolation of aerucyclamides C and D and structure revision of microcyclamide 7806A: Heterocyclic ribosomal peptides from Microcystis aeruginosa PCC 7806 and their antiparasite evaluation. J Nat Prod 71: 1891-1896.
17. Zafrir-Ilan E, Carmeli S, (2010) Two new microcyclamides from a water bloom of the cyanobacterium Microcystis sp. Tetrahedron Lett 51: 6602-6604.
18. Raveh A, Moshe S, Evron Z, Flescher E, Carmeli S, (2010) Novel thiazole and oxazole containing cyclic hexapeptides from a waterbloom of the cyanobacterium Microcystis sp. Tetrahedron 66: 2705-2712.
19. Kaneko T, Nakajima N, Okamoto S, Suzuki I, Tanabe Y, et al. (2007) Complete genomic structure of the bloom-forming toxic cyanobacterium Microcystis aeruginosa NIES-843. DNA Research 14: 247-256.
20. Lagerwed FM, van de Weert M, Heerma W, Haverkamp J, (1996) Identification of oxidized methionine in peptides. Rapid Commun Mass Spectrometry 10: 1905-1910.
21. Neitz S, Jurgens M, Kellmann M, Schulz-Knappe P, Schrader M, (2001) Screening for disulfide-rich peptides in biological sources by carboxyamidomethylation in combination with differential matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrometry 15: 1586-1592.
22. Leet JE, Liu X, Drexler DM, Cantone JL, Huang S, et al. (2008) Cytotoxic Xanthones from Psorospermum molluscum from the Madagascar Rain Forest. J Nat Prod 71: 460-463.
23. Burja AM, Banaigs B, Abou-Mansour E, Burgess JG, Wright PC, (2001) Marine cyanobacteria- a prolific source of natural products. Tetrahedron 57: 9347-9977.
24. Van Wagoner RM, Drummond AK, Wright JLC, (2007) Biogenetic diversity of cyanobacterial metabolites. Adv Appl Microbiol 61: 89-217.
25. Ireland C, Scheuer PJ, (1980) Ulicyclamide and ulithiacyclamide, two new small peptides from a marine tunicate. J Am Chem Soc 102: 5688-5691.
26. Ireland CM, Durso AR, Newman RA, Hacker MP, (1982) Antineoplastic cyclic peptides from the marine tunicate Lissoclinum patella. J Org Chem 47: 1807-1811.
27. Williams DE, Moore RE, Paul VJ, (1989) The structure of ulithiacyclamide B. Antitumor evaluation of cyclic peptides and macrolides from Lissoclinum patella. J Nat Prod 52: 732-739.
28. Fu X, Do T, Schmitz FJ, Andrusevich V, Engel MH, (1998) New cyclic peptides from the ascidian Lissoclinum patella. J Nat Prod 61: 1547-1551.
29. Donia MS, Hathaway BJ, Sudek S, Haygood MG, Rosovitz MJ, et al. (2006) Natural combinatorial peptide libraries in cyanobacterial symbionts of marine ascidians. Nat Chem Biol 2: 729-735.
30. Cascales L, Craik DJ, (2010) Naturally occurring circular proteins: Distribution, biosynthesis and evolution. Org Biomol Chem 8: 5035-5047.
31. Baumann HI, Keller S, Wolter FE, Nicholson GJ, Jung G, et al. (2007) Planktocyclin, a cyclooctapeptide protease inhibitor produced by the freshwater cyanobacterium Planktothrix rubescens. J Nat Prod 70: 1611-1615.
32. Gelb MH, (1997) Protein prenylation, et cetera - signal transduction in two dimensions. Science 275: 1750-1751.
33. Oman TJ, van der Donk WA, (2010) Follow the leader: The use of leader peptides to guide natural product biosynthesis. Nat Chem Biol 6: 9-18.
34. Frangeul L, Quillardet P, Castets A-M, Humbert J-F, Matthijs HCP, et al. (2008) Highly plastic genome of Microcystis aeruginosa PCC 7806, a ubiquitous toxic freshwater cyanobacterium. BMC Genomics 9: 274.
35. Lin S, Haas S, Zemojtel T, Xiao P, Vingron M, et al. (2011) Genome-wide comparison of cyanobacterial transposable elements, potential genetic diversity indicators. Gene 473: 139-149.
36. Fewer DP, Halinen K, Sipari H, Bernardová K, Mänttäri M, et al. (2011) Non-autonomous transposable elements associated with inactivation of microcystin gene clusters in strains of the genus Anabaena isolated from the Baltic Sea. Environ Microbiol Reports 3: 189-194.
37. Kotai J (1972) Instructions for preparation of modified nutrient solution Z8 for algae. Norwegian Institute for Water Research, Oslo. 11/69.
38. Leikoski N, Fewer DP, Sivonen K, (2009) Widespread occurrence and lateral transfer of the cyanobactin biosynthesis gene cluster in cyanobacteria. Appl Environ Microbiol 75: 853-857.
39. Neitz S, Jurgens M, Kellmann M, Schulz-Knappe P, Schrader M, (2001) Screening for disulfide-rich peptides in biological sources by carboxyamidomethylation in combination with differential matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrometry 15: 1586-1592.
40. Felsenstein J, (1989) PHYLIP-phylogeny inference package (version 3.2). Cladistics 5: 164-166.
41. Nübel U, Garcia-Pichel F, Muyzer G, (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63: 3327-3332.