Skip to main content
SpringerLink
Log in

Evolution of gene orders in genomes of cyanobacteria

  • Genetics of Microorganisms
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Genomes of 23 strains of cyanobacteria were comparatively analyzed using quantitative methods of estimation of gene order similarity. It has been found that reconstructions of phylogenesis of cyanobacteria based on the comparison of the orders of genes in chromosomes and nucleotide sequences appear to be similar. This confirms the applicability of quantitative measures of similarity of gene orders for phylogenetic reconstructions. In the evolution of marine unicellular planktonic cyanobacteria, genome rearrangements are fixed with a low rate (about 3% of gene order changes per 1% of 16S rRNA changes), whereas in other groups of cyanobacteria the gene order can change several times more rapidly. The gene orders in genomes of cyanobacteria and chloroplasts preserve a considerable degree of similarity. The closest relatives of chloroplasts among the analyzed cyanobacteria are likely to be strains from hot springs belonging to the genus Synechococcus. Comparative analysis of gene orders and nucleotide sequences strongly suggests that Synechococcus strains from different environments (sea, fresh waters, hot springs) are not related and belong to evolutionally distant lines.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Liu, H., Nolla, H.A., and Campbell, L., Prochlorococcus Growth Rate and Contribution to Primary Production in the Equatorial and Subtropical North Pacific Ocean, Aquat. Microbiol. Ecol., 1997, vol. 12, pp. 39–47.

    Article  Google Scholar 

  2. Capone, D.G., Zehr, J.P., Paerl, H.W., et al., Trichodesmium, a Globally Significant Marine Cyanobacterium, Science, 1997, vol. 276, pp. 1221–1229.

    Article  CAS  Google Scholar 

  3. The Ecology of Cyanobacteria: Their Diversity in Time and Space, Whitton, B.A. and Potts, M., Eds., Dordrecht: Kluwer, 2000.

    Google Scholar 

  4. Kaneko, T., Tanaka, A., Sato, S., et al., Sequence Analysis of the Genome of the Unicellular Cyanobacterium Synechocystis sp. Strain PCC6803, DNA Res., 1995, vol. 2, pp. 153–166.

    Article  PubMed  CAS  Google Scholar 

  5. Kaneko, T., Nakamura, Y., Wolk, C.P., et al., Complete Genomic Sequence of the Filamentous Nitrogen-Fixing Cyanobacterium Anabaena sp. Strain PCC 7120, DNA Res., 2001, vol. 8, pp. 205–213.

    Article  PubMed  CAS  Google Scholar 

  6. Nakamura, Y., Kaneko, T., Sato, S., et al., Complete Genome Structure of the Thermophilic Cyanobacterium Thermosynechococcus elongates BP-1, DNA Res., 2002, vol. 9, pp. 123–130.

    Article  PubMed  CAS  Google Scholar 

  7. Nakamura, Y., Kaneko, T., Sato, S., et al., Complete Genome Structure of Gloeobacter violaceus PCC 7421, a Cyanobacterium That Lacks Thylakoids, DNA Res., 2003, vol. 10, pp. 137–145.

    Article  PubMed  CAS  Google Scholar 

  8. Palenik, B., Brahamsha, B., Larimer, F.W., et al., The Genome of a Motile Marine Synechococcus, Nature, 2003, vol. 424, pp. 1037–1042.

    Article  PubMed  CAS  Google Scholar 

  9. Palenik, B., Ren, Q., Dupont, C.L., et al., Genome Sequence of Synechococcus CC9311: Insights into Adaptation to a Coastal Environment, Proc. Natl. Acad. Sci. USA, 2006, vol. 103, pp. 13555–13559.

    Article  PubMed  CAS  Google Scholar 

  10. Dufresne, A., Salanoubat, M., Partensky, F., et al., Genome Sequence of the Cyanobacterium Prochlorococcus marinus SS120, a Nearly Minimal Oxyphototrophic Genome, Proc. Natl. Acad. Sci. USA, 2003, vol. 100, pp. 10020–10025.

    Article  PubMed  CAS  Google Scholar 

  11. Rocap, G., Larimer, F.W., Lamerdin, J., et al., Genome Divergence in Two Prochlorococcus Ecotypes Reflects Oceanic Niche Differentiation, Nature, 2003, vol. 424, pp. 1042–1047.

    Article  PubMed  CAS  Google Scholar 

  12. Allewalt, J.P., Bateson, M.M., Revsbech, N.P., et al., Effect of Temperature and Light on Growth of and Photosynthesis by Synechococcus Isolates Typical of Those Predominating in the Octopus Spring Microbial Mat Community of Yellowstone National Park, Appl. Environ. Microbiol., 2006, vol. 72, pp. 544–550.

    Article  PubMed  CAS  Google Scholar 

  13. Sugita, C., Ogata, K., Shikata, M., et al., Complete Nucleotide Sequence of the Freshwater Unicellular Cyanobacterium Synechococcus elongates PCC 6301 Chromosome: Gene Content and Organization, Photosynth. Res., 2007, vol. 93, pp. 55–67.

    Article  PubMed  CAS  Google Scholar 

  14. Zakharov, I.A. and Valeev, A.K., Quantitative Analysis of the Mammalian Genome Evolution through Comparison of Genetic Maps, Dokl. Akad. Nauk SSSR, 1988, vol. 301, pp. 1213–1218.

    PubMed  CAS  Google Scholar 

  15. Zakharov, I.A., Nikiforov, V.S., and Stepanyuk, E.V., Estimates of the Combinatorial Measures Of Similarity for Orders of Homologous Genes, Russ. J. Genet., 1991, vol. 27, no. 2, pp. 367–369.

    CAS  Google Scholar 

  16. Zakharov, I.A. and Markov, A.V., Gene Orders in Genomes of Alpha-Proteobacteria: Similarity and Evolution, Russ. J. Genet., 2005, vol. 41, no. 12, pp. 1343–1351.

    Article  CAS  Google Scholar 

  17. Markov, A.V. and Zakharov, I.A., Large and Small Rearrangements in the Evolution of Prokaryotic Genomes, Russ. J. Genet., 2006, vol. 42, no. 11, pp. 1303–1312.

    Article  CAS  Google Scholar 

  18. Markov, A.V. and Zakharov, I.A., Application of Quantitative Measures of Gene Order Similarity to Phylogenetic Reconstructions (Exemplified by Bacteria of the Genus Rickettsia), Russ. J. Genet., 2008, vol. 44, no. 4, pp. 389–398.

    Article  CAS  Google Scholar 

  19. Markov, A.V. and Zakharov, I.A., Evolution of Gene Orders in Genomes of Mycoplasmas (Bacteria, Firmicutes, Mollicutes), Russ. J. Genet., 2009, vol. 45, no. 7 (in press).

  20. Tomitani, A., Knoll, A.H., Cavanaugh, C.M., and Ohno, T., The Evolutionary Diversification of Cyanobacteria: Molecular-Phylogenetic and Paleontological Perspectives, Proc. Natl. Acad. Sci. USA, 2006, vol. 103, pp. 5442–5447.

    Article  PubMed  CAS  Google Scholar 

  21. Litvaitis, M.K., A Molecular Test of Cyanobacterial Phylogeny: Inferences from Constraint Analyses, Hydrobiologia, 2002, vol. 468, pp. 135–145.

    Article  CAS  Google Scholar 

  22. Suyama, M. and Bork, P., Evolution of Prokaryotic Gene Order: Genome Rearrangements in Closely Related Species, Trends Genet., 2001, vol. 17, pp. 10–13.

    Article  PubMed  CAS  Google Scholar 

  23. Bourque, G. and Pevzner, P.A., Genome-Scale Evolution: Reconstructing Gene Orders in the Ancestral Species, Genome Res., 2002, vol. 12, no. 1, pp. 26–36.

    PubMed  CAS  Google Scholar 

  24. Korbel, J.O., Snel, B., Huynen, M.A., and Bork, P., SHOT: A Web Server for the Construction of Genome Phylogenies, Trends Genet., 2002, vol. 18, pp. 158–162.

    Article  PubMed  CAS  Google Scholar 

  25. Sankoff, D. and Nadeau, J.H., Chromosome Rearrangements in Evolution: From Gene Order to Genome Sequence and Back, Proc. Natl. Acad. Sci. USA, 2003, vol. 100, pp. 11188–11189.

    Article  PubMed  CAS  Google Scholar 

  26. Tang, J. and Moret, B.M.E., Scaling up Accurate Phylogenetic Reconstruction From Gene-Order Data, Bioinformatics, 2003, vol. 19, suppl. 1, pp. i305–i312.

    Article  Google Scholar 

  27. Raymond, J., Zhaxybayeva, O., Gogarten, J.P., et al., Whole-Genome Analysis of Photosynthetic Prokaryotes, Science, 2002, vol. 298, no. 5598, pp. 1616–1620.

    Article  PubMed  CAS  Google Scholar 

  28. Zhaxybayeva, O., Gogarten, J.P., Charlebois, R.L., et al., Phylogenetic Analyses of Cyanobacterial Genomes: Quantification of Horizontal Gene Transfer Events, Genome Res., 2006, vol. 16, no. 9, pp. 1099–1108.

    Article  PubMed  CAS  Google Scholar 

  29. Coenye, T. and Vandamme, P., Organisation of the S10, spc and alpha Ribosomal Protein Gene Clusters in Prokaryotic Genomes, FEMS Microbiol. Lett., 2005, vol. 242, pp. 117–126.

    Article  PubMed  CAS  Google Scholar 

  30. Awramik, S.M., The Oldest Records of Photosynthesis, Photosynth. Res., 1992, vol. 33, pp. 75–89.

    Article  PubMed  CAS  Google Scholar 

  31. Walsh, M.M., Microfossils and Possible Microfossils from the Early Archean Onverwacht Group, Barberton Mountain Land, South Africa, Precambrian Res., 1992, vol. 54, pp. 271–293.

    Article  PubMed  CAS  Google Scholar 

  32. Schopf, J.W., Microfossils of the Early Archean Apex Chert: New Evidence of the Antiquity of Life, Science, 1993, vol. 260, pp. 640–646.

    Article  PubMed  CAS  Google Scholar 

  33. Brasier, M.D., Green, O.R., Jephcoat, A.P., et al., Questioning the Evidence for Earth’s Oldest Fossils, Nature, 2002, vol. 416, pp. 76–81.

    Article  PubMed  Google Scholar 

  34. Battistuzzi, F.U., Feijao, A., and Hedges, S.B., A Genomic Timescale of Prokaryote Evolution: Insights into the Origin of Methanogenesis, Phototrophy, and the Colonization of Land, BMC Evol. Biol., 2004, vol. 4, p. 44.

    Article  PubMed  Google Scholar 

  35. Gould, S.B., Waller, R.F., and McFadden, G.I., Plastid Evolution, Annu. Rev. Plant Biol., 2008, vol. 59, pp. 491–517.

    Article  PubMed  CAS  Google Scholar 

  36. Rozanov, A.Yu., Bacterial Paleontology, Sedimentogenesis and Early Stages of Biosphere Evolution, Sovremennye problemy geologii, (Modern Problems in Geology), Gavrilov, Yu.O. and Khutorskoy, M.D., Eds., issue 565 of Tr. Geol. Inst. Russ. Akad. Nauk, 2004, pp. 448–462.

  37. Fedonkin, M.A., Two Life Chronicles: Experience of Comparison (Paleobiology and Genomics about the Early Stages of Biosphere Evolution), Problemy geologii i mineralogii (Problems of Geology and Minerology), Pystin, A.M., Ed., Syktyvkar: Geoprint, 2006, pp. 331–350.

    Google Scholar 

  38. Schopf, J.W., Are the Oldest Fossils Cyanobacteria? Evolution of Microbial Life, Roberts, D.M., Sharp, P., Alderson G., and Collins, M., Eds., Cambridge: Cambridge Univ. Press, 1996, pp. 23–62.

    Google Scholar 

  39. Zavarzin, G.A., The Evolution of Prokaryotes, in Evolyutsiya i biotsenoticheskie krizisy (Evolution and the Biocoenotic Crises), Moscow: Nauka, 1987, pp. 144–158.

    Google Scholar 

  40. Sergeev, V.N., Cyanobacterial Communities during the Early Stages of Biosphere Evolution, in Problemy doantropogennoi evolyutsii biosfery (Problems of Pre-Anthropogenic Evolution of the Biosphere), Moscow: Nauka, 1993, pp. 254–265.

    Google Scholar 

  41. Brocks, J.J., Logan, G.A., Buick, R., and Summons, R.E., Archean Molecular Fossils and the Early Rise of Eukaryotes, Science, 1999, vol. 285, pp. 1033–1036.

    Article  PubMed  CAS  Google Scholar 

  42. Summons, R.E., Jahnke, L.L., Hope, J.M., and Logan, G.A., 2-Methylhopanoids as Biomarkers for Cyanobacterial Oxygenic Photosynthesis, Nature, 1999, vol. 400, pp. 554–557.

    Article  PubMed  CAS  Google Scholar 

  43. The Proterozoic Biosphere: A Multidisciplinary Study, Schopf, J.W. and Klein, C., Eds., Cambridge: Cambridge Univ. Press, 1992.

    Google Scholar 

  44. Altermann, W. and Schopf, J.W., Microfossils from the Neoarchean Campbell Group, Griqualand West Sequence of the Transvaal Supergroup, and Their Paleoenvironmental and Evolutionary Implications, Precambrian Res., 1995, vol. 75, no. 1, pp. 65–90.

    Article  PubMed  CAS  Google Scholar 

  45. Arndt, N.T., Nelson, D.R., Compston, W., et al., The Age of the Fortescue Group, Hamersley Basin, Western Australia, from Ion Microprobe Zircon U-Pb Results, Austral. J. Earth Sci., 1991, vol. 38, no. 3, pp. 261–281.

    Article  Google Scholar 

  46. Vasconcelos, A.T.R., Ferreira, H.B., and Bizarro, C.V., Swine and Poultry Pathogens: The Complete Genome Sequences of Two Strains Of Mycoplasma hyopneumoniae and a Strain of Mycoplasma synoviae, J. Bacteriol., 2005, vol. 187, pp. 5568–5577.

    Article  PubMed  CAS  Google Scholar 

  47. Nozaki, H., A New Scenario of Plastid Evolution: Plastid Primary Endosymbiosis before the Divergence of the “Plantae,” Emended, J. Plant Res., 2005, vol. 118, pp. 247–255.

    Article  PubMed  Google Scholar 

  48. Deusch, O., Landan, G., Roettger, M., et al., Genes of Cyanobacterial Origin in Plant Nuclear Genomes Point to a Heterocyst-Forming Plastid Ancestor, Mol. Biol. Evol., 2008, vol. 25, pp. 748–761.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Paleontological Institute, Russian Academy of Sciences, Moscow, 117997, Russia

    A. V. Markov

  2. Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, 119991, Russia

    I. A. Zakharov

Authors
  1. A. V. Markov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. A. Zakharov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. V. Markov.

Additional information

Original Russian Text © A.V. Markov, I.A. Zakharov, 2009, published in Genetika, 2009, Vol. 45, No. 8, pp. 1036–1047.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Markov, A.V., Zakharov, I.A. Evolution of gene orders in genomes of cyanobacteria. Russ J Genet 45, 906–916 (2009). https://doi.org/10.1134/S1022795409080031

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795409080031

Keywords

Search

Navigation