Subpopulation differentiation associated with nonribosomal peptide synthetase gene cluster dynamics in the cyanobacterium planktothrix spp.

Journal of Phycology

Volumn 46, Issue 4, 2010, Pages 645-652

  Rounge, Trine B ^a   Rohrlack, Thomas ^a,b   Decenciere, Beatriz ^a   Edvardsen, Bente ^a   Kristensen, Tom ^a   Jakobsen, Kjetill S ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b NORWEGIAN INSTITUTE FOR WATER RESEARCH   (Norway)

Author keywords

Chemotype; Cyanopeptolin; Horizontal gene transfer; Microcystin; Nonribosomal peptide synthesis; Planktothrix; Subpopulations

Indexed keywords

PLANKTOTHRIX;

EID: 77955261212     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2010.00856.x     Document Type: Article

References (43)

1. Challis G L, Ravel J, Townsend C A. Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem. Biol. 2000, 7:211-24.
2. Christiansen G, Kurmayer R, Liu Q, Börner T. Transposons inactivate biosynthesis of the nonribosomal peptide microcystin in naturally occurring Planktothrix spp. Appl. Environ. Microbiol. 2006, 72:117-23.
3. Fastner J, Erhard M, von Döhren H. Determination of oligopeptide diversity within a natural population of Microcystis spp. (Cyanobacteria) by typing single colonies by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Appl. Environ. Microbiol. 2001, 67:5069-76.
4. Fewer D P, Tooming-Klunderud A, Jokela J, Wahlsten M, Rouhiainen L, Kristensen T, Rohrlack T, Jakobsen K S, Sivonen K. Natural occurrence of microcystin synthetase deletion mutants capable of producing microcystins in strains of the genus Anabaena (Cyanobacteria). Microbiology 2008, 154:1007-14.
5. Gogarten J P, Doolittle W F, Lawrence J G. Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 2002, 19:2226-38.
6. Halstvedt C B, Rohrlack T, Andersen T, Skulberg O, Edvardsen B. Seasonal dynamics and depth distribution of Planktothrix spp. in Lake Steinsfjorden (Norway) related to environmental factors. J. Plankton Res. 2007, 29:471-82.
7. Huelsenbeck J P, Ronquist F. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 2001, 17:754-5.
8. Huson D H. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 1998, 14:68-73.
9. Itou Y, Ishida K, Shin S J, Murakami M. Oscillapeptins A to F, serine protease inhibitors from the three strains of Oscillatoria agardhii. Tetrahedron 1999, 55:6871-82.
10. Johnson Z I, Zinser E R, Coe A, McNulty N P, Woodward E M, Chisholm S W. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 2006, 311:1737-40.
11. Kotai J. Instructions for Preparation of Modified Nutrient Solution Z8 for Algae 1972, Publication B-11/69, Norwegian Institute for Water Research, Blindern, Oslo, pp
12. Kumar S, Tamura K, Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence. Brief. Bioinformatics 2004, 5:150-63.
13. Kurmayer R, Christiansen G, Gumpenberger M, Fastner J. Genetic identification of microcystin ecotypes in toxic cyanobacteria of the genus Planktothrix. Microbiology 2005, 151:1525-33.
14. Kurmayer R, Gumpenberger M. Diversity of microcystin genotypes among populations of the filamentous cyanobacteria Planktothrix rubescens and Planktothrix agardhii. Mol. Ecol. 2006, 15:3849-61.
15. Majewski J, Cohan F M. The effect of mismatch repair and heteroduplex formation on sexual isolation in Bacillus. Genetics 1998, 148:13-8.
16. Marahiel M A, Stachelhaus T, Mootz H D. Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 1997, 97:2651-74.
17. Martin D P, Williamson C, Posada D. RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 2005, 21:260-2.
18. 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, 185:2774-85.
19. 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, 70:6353-62.
20. Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 1986, 3:418-26.
21. Papke R T, Zhaxybayeva O, Feil E J, Sommerfeld K, Muise D, Doolittle W F. Searching for species in haloarchaea. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14092-7.
22. Pigliucci M. Evolution of phenotypic plasticity: where are we going now? Trends Ecol. Evol. 2005, 20:481-6.
23. Posada D, Crandall K A. MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-8.
24. Rocap G, Distel D L, Waterbury J B, Chisholm S W. Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl. Environ. Microbiol. 2002, 68:1180-91.
25. Rohrlack T, Christoffersen K, Hansen P E, Zhang W, Czarnecki O, Henning M, Fastner J, Erhard M, Neilan B A, Kaebernick M. Isolation, characterization, and quantitative analysis of microviridin J, a new Microcystis metabolite toxic to Daphnia. J. Chem. Ecol. 2003, 29:1757-70.
26. Rohrlack T, Edvardsen B, Skulberg R, Halstvedt C B, Utkilen H C, Ptacnik R, Skulberg O M. Oligopeptide chemotypes of the toxic freshwater cyanobacterium Planktothrix can form subpopulations with dissimilar ecological traits. Limnol. Oceanogr. 2008, 53:1279-93.
27. Rohrlack T, Skulberg R, Skulberg O M. Distribution of oligopeptide chemotypes of the cyanobacterium Planktothrix and their persistence in selected lakes in Fennoscandia. J. Phycol. 2009, 45:1259-65.
28. Ronquist F, Huelsenbeck J P. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-4.
29. Rounge T B, Rohrlack T, Kristensen T, Jakobsen K S. Recombination and selectional forces in cyanopeptolin NRPS operons from highly similar, but geographically remote Planktothrix strains. BMC Microbiol. 2008, 8:141.
30. Rounge T B, Rohrlack T, Nederbragt A J, Kristensen T, Jakobsen K S. A genome-wide analysis of non-ribosomal peptide synthetase gene clusters and their peptides in a single Planktothrix rubescens strain. BMC Genomics 2009, 10:396.
31. 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. Microbiol. 2007, 73:7322-30.
32. Rozas J, Sanchez-DelBarrio J C, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19:2496-7.
33. Rudi K, Skulberg O M, Jakobsen K S. Evolution of cyanobacteria by exchange of genetic material among phyletically related strains. J. Bacteriol. 1998, 180:3453-61.
34. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-90.
35. Tanabe Y, Kaya K, Watanabe M M. Evidence for recombination in the microcystin synthetase (mcy) genes of toxic cyanobacteria Microcystis spp. J. Mol. Evol. 2004, 58:633-41.
36. Thomas C M, Nielsen K M. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat. Rev. Microbiol. 2005, 3:711-21.
37. Tooming-Klunderud A, Fewer D P, Rohrlack T, Jokela J, Rouhiainen L, Sivonen K, Kristensen T, Jakobsen K S. Evidence for positive selection acting on microcystin synthetase adenylation domains in three cyanobacterial genera. BMC Evol. Biol. 2008a, 8:256.
38. Tooming-Klunderud A, Mikalsen B, Kristensen T, Jakobsen K S. The mosaic structure of the mcyABC operon in Microcystis. Microbiology 2008b, 154:1886-99.
39. Tooming-Klunderud A, Rohrlack T, Shalchian-Tabrizi K, Kristensen T, Jakobsen K S. Structural analysis of a non-ribosomal halogenated cyclic peptide and its putative operon from Microcystis: implications for evolution of cyanopeptolins. Microbiology 2007, 153:1382-93.
40. 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 2004a, 150:1785-96.
41. Welker M, Christiansen G, von Döhren H. Diversity of coexisting Planktothrix (cyanobacteria) chemotypes deduced by mass spectral analysis of microcystins and other oligopeptides. Arch. Microbiol. 2004b, 182:288-98.
42. Yepremian C, Gugger M F, Briand E, Catherine A, Berger C, Quiblier C, Bernard C. Microcystin ecotypes in a perennial Planktothrix agardhii bloom. Water Res. 2007, 41:4446-56.
43. Zhaxybayeva O, Gogarten J P, Charlebois R L, Doolittle W F, Papke R T. Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res. 2006, 16:1099-108.