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An Evaluation of Four Phylogenetic Markers in Nostoc: Implications for Cyanobacterial Phylogenetic Studies at the Intrageneric Level

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Abstract

The success of some phylogenetic markers in cyanobacteria owes to the design of cyanobacteria-specific primers, but a few studies have directly investigated the evolution “behavior” of the loci. In this study, we performed a case study in Nostoc to evaluate rpoC1, hetR, rbcLX, and 16S rRNA–tRNAIle–tRNAAla-23S rRNA internal transcribed spacer (ITS) as phylogenetic markers. The results indicated that the gene trees of these loci are not congruent with the phylogeny based on 16S rRNA gene. The mechanisms contributing to the incongruence include randomized variation and recombination. As the results suggested, one should be careful to choose the molecular markers for phylogenetic reconstruction at the intrageneric level in cyanobacteria.

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References

  1. Archie J (1989) A randomization test for phylogenetic information in systematic data. Syst Zool 38:239–252

    Article  Google Scholar 

  2. Boyer S, Flechtner V, Johansen J (2001) Is the 16S–23S rRNA internal transcribed spacer region a good tool for use in molecular systematics and population genetics? A case study in cyanobacteria. Mol Biol Evol 18:1057–1069

    PubMed  CAS  Google Scholar 

  3. Brocchieri L (2001) Phylogenetic inferences from Molecular sequences: Review and critique. Theor Popul Biol 59:27–40

    Article  PubMed  CAS  Google Scholar 

  4. Dodds W, Gudder D (1995) The ecology of Nostoc. J Phycol 32:2–18

    Article  Google Scholar 

  5. Farris J, Kallersjo M, Kluge A et al (1994) Testing significance of incongruence. Cladistics 10:315–319

    Article  Google Scholar 

  6. Gaitler N, Gouy M (1995) Inferring phylogenies from DNA sequences of unequal base compositions. Proc Natl Acad Sci U S A 92:11317–11321

    Article  Google Scholar 

  7. Galtier N, Gouy M, Gautier C (1996) SeaView and Phylo Win, two graphic tools for sequence alignment and molecular phylogeny. Comput Applic Biosci 12:543–548

    CAS  Google Scholar 

  8. Gibbs M, Armstrong J, Gibbs A (2000) Sister-scanning: A Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582

    Article  PubMed  CAS  Google Scholar 

  9. Gugger M, Lyra C, Henriksen P et al (2002) Phylogenetic comparison of the cyanobacterial genera Anabaena and Aphanizomenon. Int J Syst Evol Microbiol 52:1867–1880

    Article  PubMed  CAS  Google Scholar 

  10. Hillis D, Huelsenbeck J (1992) Signal, noise, and reliability in molecular phylogenetic analyses. J Hered 83:189–195

    PubMed  CAS  Google Scholar 

  11. Janasson S, Wouters J, Bergman B et al (1999) Host specificity in the Richelia-diatom symbiosis showed by hetR gene sequence analysis. Environ Microbiol 1:431–438

    Article  Google Scholar 

  12. Janson S, Graneli E (2002) Phylogenetic analyses of nitrogen-fixing cyanobacteria from the Baltic Sea show sequence anomalies in the phycocyanin operon. Int J Syst Evol Microbiol 52:1397–1404

    Article  PubMed  CAS  Google Scholar 

  13. Janson S, Matveyev A, Bergman B (1998) The presence and expression of hetR in the nonheterocystous cyanobacterium Symploca PCC 8002. FEMS Microbiol Lett 168:173–179

    Article  PubMed  CAS  Google Scholar 

  14. Komárek J, Anagnostidis K (1989) Modern approach to the classification system of Cyanophytes 4-Nostocales. Arch Hydrobiol 82(Suppl.):247–345

    Google Scholar 

  15. Kumar S, Tamura K, Nei M (2004) Mega3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. 5:150–163

  16. Kurland C (2000) Something for everyone. Horizontal gene transfer in evolution. EMBO Rep 1:92–95

    Article  PubMed  CAS  Google Scholar 

  17. Laamanen M, Forsstrom L, Sivonen K (2002) Diversity of Aphanizomenon flos-aquae (cyanobacterium) populations along a Baltic Sea salinity gradient. Appl Environ Microbiol 68:5296–5303

    PubMed  CAS  Google Scholar 

  18. Lockhart P, Steel M, Hendy M et al (1994) Recovering evolutionary trees under a more realistic model of sequence evolution. Mol Biol Evol 11:605–612

    CAS  PubMed  Google Scholar 

  19. Lorenz M, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602

    PubMed  CAS  Google Scholar 

  20. Lyra C, Laamanen M, Lehtimaki J et al (2005) Benthic cyanobacteria of the genus Nodularia are nontoxic, without gas vacuoles, able to glide and genetically more diverse than planktonic Nodularia. Int J Syst Evol Microbiol 55:555–568

    Article  PubMed  CAS  Google Scholar 

  21. Manen J, Falquet J (2002) The cpcB-cpcA locus as a tool for the genetic characterization of the genus Arthrospira (Cyanobacteria): Evidence for horizontal transfer. Int J Syst Evol Microbiol 52:861–867

    Article  PubMed  CAS  Google Scholar 

  22. Martin D, Rybicki E (2000) RDP: Detection for recombination amongst aligned sequences. Bioinformatics 16:562–563

    Article  PubMed  CAS  Google Scholar 

  23. Martin D, Willamson C, Posada D (2005) RDP2: Recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262

    Article  PubMed  CAS  Google Scholar 

  24. Mes T, Stal L (2005) Variable selection pressures across lineages in Trichodesmim and related cyanobacteria based on the heterocyst differentiation protein gene hetR. Gene 346:163–171

    Article  PubMed  CAS  Google Scholar 

  25. Ochman H, Lawrence J, Groisman E (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304

    Article  PubMed  CAS  Google Scholar 

  26. Otsuka S, Suda S, Li R et al (1999) Phylogenetic relation between toxic and nontoxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence. FEMS Microbiol Lett 172:15–21

    Article  PubMed  CAS  Google Scholar 

  27. Palenik B (1994) Cyanobacterial community structures as seen from RNA polymerase gene sequence analysis. Appl Environ Microbiol 60:3212–3219

    PubMed  CAS  Google Scholar 

  28. Philippe H, Forterre P (1999) The rooting of the universal tree of life is not reliable. J Mol Evol 49:509–523

    Article  PubMed  CAS  Google Scholar 

  29. Posada D (2002) Evaluation of methods for detecting recombination from DNA sequences: Empirical data. Mol Biol Evol 19:708–717

    PubMed  CAS  Google Scholar 

  30. Posada D, Crandall K (1998) Modeltest: Testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  31. Posada D, Crandall K (2001) Performance of methods for detecting recombination from DNA sequences: Computer simulations. Proc Natl Acad Sci U S A 98:13757–13762

    Article  PubMed  CAS  Google Scholar 

  32. Rajaniemi P, Hrouzek P, Kastovska K et al (2005) Phylogeny and morphologic evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int J Syst Evol Microbiol 51:505–512

    Google Scholar 

  33. Rantala A, Fewer D, Hisbergues M et al (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc Natl Acad Sci U S A 101:568–573

    Article  PubMed  CAS  Google Scholar 

  34. Rikkinen J, Oksanen I, Lohtander K (2002) Lichen guilds share related cyanobacterial symbionts. Science 297:357

    Article  PubMed  CAS  Google Scholar 

  35. Rippka R, Castenholz RW, Herdman M (2001) Subsection. In: Boone DR, Castenholz RW (eds) Bergey’s Manual of Systematic Bacteriology, vol 1. 2nd. New York, NY: Springer, pp 562–566 [Formerly Nostocales Castenholz (1989b) Sensu Rippka, Deruelles, Waterbury, Herdman and Stanier 1979]

  36. Rocap G, Distel D, Waterbury J et al (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S–23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68:1180–1191

    Article  PubMed  CAS  Google Scholar 

  37. Rudi K, Skulberg O, Jakobsen K (1998) Evolution of cyanobacteria by exchange of genetic material among phyletically related strains. J Bacteriol 180:3453–3461

    PubMed  CAS  Google Scholar 

  38. Salminen N, Carr J, Burke D et al (1996) Identification of break points in intergenotypic recombinants of HIV–1 by bootscanning. AIDS Res Hum Retrovir 11:1423–1425

    Article  Google Scholar 

  39. 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. Available at: http://www.math.wustl.edu/~sawyer

  40. Shen P, Huang H (1986) Homologous recombination in Escherichia coli dependence on substrate length and homology. Genetics 112:441–457

    PubMed  CAS  Google Scholar 

  41. Shimodaira H, Hasegawa W (1999) Multiple comparisons of log-likehoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116

    CAS  Google Scholar 

  42. Smith J (1992) Analyzing the mosaic structure of genes. J Mol Evol 34:126–129

    PubMed  CAS  Google Scholar 

  43. Svenning M, Eriksson T, Rasmussen U (2005) Phylogeny of symbiotic cyanobacteria within the genus Nostoc based on 16S rRNA sequence analyses. Arch Microbiol 183:19–26

    Article  PubMed  CAS  Google Scholar 

  44. Swofford D (2001) PAUP* 4.0: Phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland, UK

    Google Scholar 

  45. Tanabe Y, Kaya K, Watanabe M (2004) Evidence for recombination in the microcystin synthetase (mcy) genes of toxic cyanobacteria Microcystis spp. J Mol Evol 58:633–641

    Article  PubMed  CAS  Google Scholar 

  46. Templeton A (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans the apes. Evolution 37:221–244

    Article  CAS  Google Scholar 

  47. Thompson J, Gibson T, Plewniak F et al (1997) The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  48. Wilmotte A, Van der Auwera G, De Wachter R (1993) Structure of the 16S ribosomal RNA of the thermophilic cyanobacterium Chlorogloeopsis HTF (‘Mastigocladus laminosus HTF’) strain PCC7518, and phylogenetic analysis. FEBS Lett 317:96–100

    Article  PubMed  CAS  Google Scholar 

  49. Yang Z (1996) Among-site rate variation and its impact on phylogenetic analysis. Tree 11:367–372

    Google Scholar 

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Acknowledgments

This study was funded by the Natural Science project of Hubei Province (2004AB127), China. We thank Dr. Xudong Xu for kindly providing experimental materials for TA clone and Dr. Renhui Li for critically reading the manuscript and providing helpful comments.

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Authors and Affiliations

  1. State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    D. Han, Y. Fan & Z. Hu

  2. Graduate School, Chinese Academy of Sciences, Beijing, 100039, China

    D. Han & Y. Fan

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  1. D. Han
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  2. Y. Fan
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  3. Z. Hu
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Correspondence to Z. Hu.

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Han, D., Fan, Y. & Hu, Z. An Evaluation of Four Phylogenetic Markers in Nostoc: Implications for Cyanobacterial Phylogenetic Studies at the Intrageneric Level. Curr Microbiol 58, 170–176 (2009). https://doi.org/10.1007/s00284-008-9302-x

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  • DOI: https://doi.org/10.1007/s00284-008-9302-x

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