Frequent recombination shapes the epidemic population structure of Planktothrix (Cyanoprokaryota) in Italian subalpine lakes

Journal of Phycology

Volumn 49, Issue 6, 2013, Pages 1107-1117

  D'Alelio, Domenico ^a,b   Salmaso, Nico ^a   Gandolfi, Andrea ^a  

^a RESEARCH AND INNOVATION CENTRE   (Italy)

^b STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

Author keywords

ClonalFrame; Cyanobacteria; Genetic recombination; Linkage disequilibrium; Population structure

Indexed keywords

CYANOBACTERIA; PLANKTOTHRIX;

EID: 84889634853     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/jpy.12116     Document Type: Article

References (62)

1. Agapow, P. M. & Burt, A. 2001. Indices of multilocus linkage disequilibrium. Mol. Ecol. Notes 1:101-2.
2. Barker, G. L. A., Handley, B. A., Vacharapiyasophon, P., Stevens, J. R. & Hayes, P. K. 2000. Allele-specific PCR shows that genetic exchange occurs among genetically diverse Nodularia (Cyanobacteria) filaments in the Baltic Sea. Microbiology 146:2865-75.
3. Beard, S. J., Davis, P. A., Iglesias-Rodriguez, D., Skulberg, O. M. & Walsby, A. E. 2000. Gas vesicle genes in Planktothrix spp. from Nordic lakes: strains with weak gas vesicles possess a longer variant of gvpC. Microbiology 146:2009-18.
4. Beard, S. J., Handley, B. A., Hayes, P. K. & Walsby, A. E. 1999. The diversity of gas vesicle genes in Planktothrix rubescens from Lake Zürich. Microbiology 145:2757-68.
5. Bergstrom, C. T., Lipsitch, M. & Levin, B. R. 2000. Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155:1505-19.
6. Bruen, T. C., Philippe, H. & Bryant, D. 2006. A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665-81.
7. Buraschi, E., Salerno, F., Monguzzi, C., Barbiero, G. & Tartari, G. 2005. Characterization of the Italian lake-types and identification of their reference sites using anthropogenic pressure factors. J. Limnol. 64:75-84.
8. Christiansen, G., Fastner, J., Erhard, M., Börner, T. & Dittmann, E. 2003. Microcystin biosynthesis in Planktothrix: genes, evolution, and manipulation. J. Bacteriol. 185:564-72.
9. Christiansen, G., Molitor, C., Philmus, B. & Kurmayer, R. 2008a. Nontoxic strains of Cyanobacteria are the result of major gene deletion events induced by a transposable element. Mol. Biol. Evol. 25:1695-704.
10. Christiansen, G., Yoshida, W. Y., Blom, J. F., Portmann, C., Gademann, K., Hemscheidt, T. & Kurmayer, R. 2008b. Isolation and structure determination of two microcystins and sequence comparison of the McyABC adenylation domains in Planktothrix species. J. Nat. Prod. 71:1881-6.
11. Cohan, F. M. 2002. What are bacterial species? Annu. Rev. Microbiol. 56:457-87.
12. Cooper, J. E. & Feil, E. J. 2004. Multilocus sequence typing - what is resolved? Trends Microbiol. 12:373-7.
13. D'Alelio, D. & Gandolfi, A. 2012. Recombination signals in rpoc1 suggest gene flow between Planktothrix (Cyanoprokaryota) species. J. Phycol. 48:1424-32.
14. D'Alelio, D., Gandolfi, A., Boscaini, A., Flaim, G., Tolotti, M. & Salmaso, N. 2011. Planktothrix populations in subalpine lakes: selection for strains with strong gas vesicles as a function of lake depth, morphometry and circulation. Freshwater Biol. 56:1481-93.
15. D'Alelio, D. & Salmaso, N. 2011. Occurrence of an uncommon Planktothrix (Cyanoprokaryota, Oscillatoriales) in a deep lake south of the Alps. Phycologia 50:379-83.
16. Deng, L. & Hayes, P. K. 2008. Evidence for cyanophages active against bloom-forming freshwater cyanobacteria. Freshwater Biol. 53:1240-52.
17. Didelot, X., Barker, M., Falush, D. & Priest, F. G. 2009. Evolution of pathogenicity in the Bacillus cereus group. Syst. Appl. Microbiol. 32:81-90.
18. Didelot, X., Bowden, R., Street, T., Golubchik, T., Spencer, C., McVean, G., Sangal, V., Anjum, M. F., Achtman, M., Falush, D. & Donnelly, P. 2011. Recombination and population structure in Salmonella enterica. PLoS Genet. 7:e1002191.
19. Didelot, X. & Falush, D. 2007. Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251-66.
20. Didelot, X. & Maiden, M. C. J. 2010. Impact of recombination on bacterial evolution. Trends Microbiol. 18:315-22.
21. Dover, G. 1982. Molecular drive: a cohesive mode of species evolution. Nature 299:111-7.
22. Excoffier, L. & Lischer, H. E. L. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10:564-7.
23. Excoffier, L., Smouse, P. E. & Quattro, J. M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479-91.
24. Figuerola, J., Green, A. J. & Santamaria, L. 2003. Passive internal transport of aquatic organisms by waterfowl in Donana, south-west Spain. Global Ecol. Biogeogr. 12:427-36.
25. Fraser, C., Hanage, W. P. & Spratt, B. G. 2007. Recombination and the nature of bacterial speciation. Science 315:476-80.
26. Ganley, A. R. D. & Kobayashi, T. 2007. Highly efficient concerted evolution in the ribosomal DNA repeats: total rDNA repeat variation revealed by whole-genome shotgun sequence data. Genome Res. 17:184-91.
27. Gelman, A. & Rubin, D. B. 1992. Inference from iterative simulation using multiple sequences. Stat. Sci. 7:457-72.
28. van Gremberghe, I., Leliaert, F., Mergeay, J., Vanormelingen, P., Van der Gucht, K., Debeer, A.-E., Lacerot, G., De Meester, L. & Vyverman, W. 2011. Lack of phylogeographic structure in the freshwater Cyanobacterium Microcystis aeruginosa suggests global dispersal. PLoS ONE 6:e19561.
29. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acid. S. 41:95-8.
30. Hillis, D. M. & Dixon, M. T. 1991. Ribosomal DNA: molecolar evolution and phylogenetic inference. Q. Rev. Biol. 66:411-53.
31. Hillis, D. M., Moritz, C., Porter, C. A. & Baker, R. J. 1991. Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science 251:308-10.
32. Holland, D. P. & Walsby, A. E. 2008. Viability of the cyanobacterium Planktothrix rubescens in the cold and dark, related to over-winter survival and summer recruitment in Lake Zürich. Eur. J. Phycol. 43:179-84.
33. Hudson, R. R. 1994. Analytical results concerning linkage disequilibrium in models with genetic transformation and conjugation. J. Evolution. Biol. 7:535-48.
34. Humbert, J. F. & Le Berre, B. 2001. Genetic diversity in two species of freshwater Cyanobacteria, Planktothrix (Oscillatoria) rubescens and P. agardhii. Arch. Hydrobiol. 150:197-206.
35. Huson, D. & Bryant, D. 2006. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23:254-67.
36. Kellogg, C. A. & Griffin, D. W. 2006. Aerobiology and the global transport of desert dust. Trends Ecol. Evol. 21:638-44.
37. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. J. Mol. Evol. 16:111-20.
38. Komárek, J. & Anagnostidis, K. 2005. Cyanoprokaryota, 2 Teil: Oscillatoriales. In Büdel, B., Gärtner, G., Krienitz, L. & Schagerl, M. [Eds.] Süßwasserflora von Mitteleuropa, Vol. 19. Spektrum Akademischer Verlag, Elsevier, Heidelberg, pp. 1-759.
39. Levin, B. R. & Bergstrom, C. T. 2000. Bacteria are different: observations, interpretations, speculations, and opinions about the mechanisms of adaptive evolution in prokaryotes. Proc. Natl Acad. Sci. USA 97:6981-5.
40. Librado, P. & Rozas, J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-2.
41. Lin, S., Wu, Z. X., Yu, G. L., Zhu, M. L., Yu, B. S. & Li, R. H. 2010. Genetic diversity and molecular phylogeny of Planktothrix (Oscillatoriales, Cyanobacteria) strains from China. Harmful Algae 9:87-97.
42. Lodders, N., Stackebrandt, E. & Nubel, U. 2005. Frequent genetic recombination in natural populations of the marine Cyanobacterium Microcoleus chthonoplastes. Environ. Microbiol. 7:434-42.
43. Maiden, M. C. J., Bygraves, J. A., Feil, E., Morelli, G., Russell, J. E., Urwin, R., Zhang, Q. et al. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl Acad. Sci. USA 95:3140-5.
44. Maynard Smith, J. 1994. Estimating the minimum rate of genetic transformation in bacteria. J. Evolution. Biol. 7:525-34.
45. Maynard Smith, J., Smith, N. H., Orourke, M. & Spratt, B. G. 1993. How clonal are Bacteria? Proc. Natl Acad. Sci. USA 90:4384-8.
46. Messineo, V., Bogialli, S., Melchiorre, S., Sechi, N., Lugliè, A., Casiddu, P., Mariani, M. A. et al. 2009. Cyanobacterial toxins in Italian freshwaters. Limnologica 39:95-106.
47. Milne, I., Lindner, D., Bayer, M., Husmeier, D., McGuire, G., Marshall, D. F. & Wright, F. 2008. TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25:126-7.
48. Modi, R. I. & Adams, J. 1991. Coevolution in bacterial-plasmid populations. Evolution 45:656-67.
49. Papke, R. T. & Ward, D. M. 2004. The importance of physical isolation to microbial diversification. FEMS Microbiol. Ecol. 48:293-303.
50. Ramírez-Soriano, A., Ramos-Onsins, S. E., Rozas, J., Calafell, F. & Navarro, A. 2008. Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics 179:555-67.
51. Rounge, T. B., Rohrlack, T., Decenciere, B., Edvardsen, B., Kristensen, T. & Jakobsen, K. S. 2010. Subpopulation differentiation associated with nonribosomal peptide synthetase gene cluster dynamics in the Cyanobacterium Planktothrix spp. J. Phycol. 46:645-52.
52. Rounge, T. B., Rohrlack, T., Kristensen, T. & Jakobsen, K. S. 2008. Recombination and selectional forces in cyanopeptolin NRPS operons from highly similar, but geographically remote Planktothrix strains. BMC Microbiol. 8:141.
53. Salmaso, N., Buzzi, F., Garibaldi, L., Morabito, G. & Simona, M. 2012. Effects of nutrient availability and temperature on phytoplankton development: a case study from the large lakes south of the Alps. Aquat. Sci. 74:555-70.
54. Sheppard, S. K., McCarthy, N. D., Falush, D. & Maiden, M. C. J. 2008. Convergence of Campylobacter species: implications for bacterial evolution. Science 320:237-9.
55. Stanier, R. Y., Kunisawa, R., Mandel, M. & Cohen-Bazire, G. 1971. Purification and properties of unicellular blue-green algae (Order Chroococcales). Bacteriol. Rev. 35:171-205.
56. Suda, S., Watanabe, M. M., Otsuka, S., Mahakahant, A., Yongmanitchai, W., Nopartnaraporn, N., Liu, Y. & Day, J. G. 2002. Taxonomic revision of water-bloom-forming species of oscillatorioid cyanobacteria. Int. J. Syst. Evol. Micr. 52:1577-95.
57. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-95.
58. Tanabe, Y., Kasai, F. & Watanabe, M. M. 2007. Multilocus sequence typing (MLST) reveals high genetic diversity and clonal population structure of the toxic cyanobacterium Microcystis aeruginosa. Microbiology 153:3695-703.
59. Tanabe, Y., Sano, T., Kasai, F. & Watanabe, M. M. 2009. Recombination, cryptic clades and neutral molecular divergence of the microcystin synthetase (mcy) genes of toxic cyanobacterium Microcystis aeruginosa. BMC Evol. Biol. 9:115.
60. Tanabe, Y. & Watanabe, M. M. 2011. Local expansion of a panmictic lineage of water bloom-forming cyanobacterium Microcystis aeruginosa. PLoS ONE 6:e17085.
61. Thompson, J. D., Higgins, D. G. & Gibson, T. J. 1994. Clustal W - Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-80.
62. Thompson, L. R., Zeng, Q., Kelly, L., Huang, K. H., Singerc, A. U., Stubbe, J. & Chisholm, S. W. 2011. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc. Natl Acad. Sci. USA 108:E757-64.