1887

Abstract

In heterocystous cyanobacteria, heterocyst differentiation is accompanied by developmentally regulated DNA rearrangements that occur within the and genes, referred to as the and elements. These elements are segments of DNA that are embedded within the coding region of each gene and range from 4 to 24 kb in length. The and elements are independently excised from the genome during the later stages of differentiation by the site-specific recombinases, XisA and XisC, respectively, which are encoded within the elements themselves. Here we examine the variation and evolution of the and elements by comparing full-length and element sequences and by phylogenetic analysis of and gene sequences. There is considerable variation in the size and composition of the and elements, however, conserved regions are also present within representatives of each element. The data suggest that the and elements have undergone a complex pattern of insertions, deletions, translocations and sequence divergence over the course of evolution, but that conserved regions remain.

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2011-12-01
2024-03-29
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References

  1. Adams D. G., Duggan P. S. 1999; Heterocyst and akinete differentiation in cyanobacteria. New Phytol 144:3–33 [View Article]
    [Google Scholar]
  2. Alvey R. M., Karty J. A., Roos E., Reilly J. P., Kehoe D. M. 2003; Lesions in phycoerythrin chromophore biosynthesis in Fremyella diplosiphon reveal coordinated light regulation of apoprotein and pigment biosynthetic enzyme gene expression. Plant Cell 15:2448–2463 [View Article][PubMed]
    [Google Scholar]
  3. Böhme H. 1998; Regulation of nitrogen fixation in heterocyst-forming cyanobacteria. Trends Plant Sci 3:346–351 [View Article]
    [Google Scholar]
  4. Bremer K. 1994; Branch support and tree stability. Cladistics 10:295–304 [View Article]
    [Google Scholar]
  5. Brusca J. S., Hale M. A., Carrasco C. D., Golden J. W. 1989; Excision of an 11-kilobase-pair DNA element from within the nifD gene in Anabaena variabilis heterocysts. J Bacteriol 171:4138–4145[PubMed]
    [Google Scholar]
  6. Brusca J. S., Chastain C. J., Golden J. W. 1990; Expression of the Anabaena sp. strain PCC 7120 xisA gene from a heterologous promoter results in excision of the nifD element. J Bacteriol 172:3925–3931[PubMed]
    [Google Scholar]
  7. Canchaya C., Proux C., Fournous G., Bruttin A., Brüssow H. 2003; Prophage genomics. Microbiol Mol Biol Rev 67:238–276 [View Article][PubMed]
    [Google Scholar]
  8. Carrasco C. D., Golden J. W. 1995; Two heterocyst-specific DNA rearrangements of nif operons in Anabaena cylindrica and Nostoc sp. strain Mac. Microbiology 141:2479–2487 [View Article][PubMed]
    [Google Scholar]
  9. Carrasco C. D., Ramaswamy K. S., Ramasubramanian T. S., Golden J. W. 1994; Anabaena xisF gene encodes a developmentally regulated site-specific recombinase. Genes Dev 8:74–83 [View Article][PubMed]
    [Google Scholar]
  10. Carrasco C. D., Buettner J. A., Golden J. W. 1995; Programmed DNA rearrangement of a cyanobacterial hupL gene in heterocysts. Proc Natl Acad Sci U S A 92:791–795 [View Article][PubMed]
    [Google Scholar]
  11. Carrasco C. D., Holliday S. D., Hansel A., Lindblad P., Golden J. W. 2005; Heterocyst-specific excision of the Anabaena sp. strain PCC 7120 hupL element requires xisC . J Bacteriol 187:6031–6038 [View Article][PubMed]
    [Google Scholar]
  12. Casjens S. 2003; Prophages and bacterial genomics: what have we learned so far?. Mol Microbiol 49:277–300 [View Article][PubMed]
    [Google Scholar]
  13. Chastain C. J., Brusca J. S., Ramasubramanian T. S., Wei T. F., Golden J. W. 1990; A sequence-specific DNA-binding factor (VF1) from Anabaena sp. strain PCC 7120 vegetative cells binds to three adjacent sites in the xisA upstream region. J Bacteriol 172:5004–5051
    [Google Scholar]
  14. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evol 39:783–791 [View Article]
    [Google Scholar]
  15. Golden J. W., Robinson S. J., Haselkorn R. 1985; Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena . Nature 314:419–423 [CrossRef]
    [Google Scholar]
  16. Golden J. W., Mulligan M. E., Haselkorn R. 1987; Different recombination site specificity of two developmentally regulated genome rearrangements. Nature 327:526–529 [View Article][PubMed]
    [Google Scholar]
  17. Golden J. W., Carrasco C. D., Mulligan M. E., Schneider G. J., Haselkorn R. 1988; Deletion of a 55-kilobase-pair DNA element from the chromosome during heterocyst differentiation of Anabaena sp. strain PCC 7120. J Bacteriol 170:5034–5041[PubMed]
    [Google Scholar]
  18. Golden J. W., Whorff L. L., Wiest D. R. 1991; Independent regulation of nifHDK operon transcription and DNA rearrangement during heterocyst differentiation in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 173:7098–7105
    [Google Scholar]
  19. Hacker J., Carniel E. 2001; Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep 2:376–381[PubMed] [CrossRef]
    [Google Scholar]
  20. Hall B. G. 2004; Codon Align. Macintosh, Windows, Unix. Distributed by the author. Bellingham, WA. [View Article][PubMed]
    [Google Scholar]
  21. Happe T., Schütz K., Böhme H. 2000; Transcriptional and mutational analysis of the uptake hydrogenase of the filamentous cyanobacterium Anabaena variabilis ATCC 29413. J Bacteriol 182:1624–1631 [View Article][PubMed]
    [Google Scholar]
  22. Haraldsen J. D., Sonenshein A. L. 2003; Efficient sporulation in Clostridium difficile requires disruption of the sigmaK gene. Mol Microbiol 48:811–821 [View Article][PubMed]
    [Google Scholar]
  23. Haselkorn R. 1992; Developmentally regulated gene rearrangements in prokaryotes. Annu Rev Genet 26:113–130 [View Article][PubMed]
    [Google Scholar]
  24. Henson B. J., Watson L. E., Barnum S. R. 2002; Molecular differentiation of the heterocystous cyanobacteria, Nostoc and Anabaena, based on complete NifD sequences. Curr Microbiol 45:161–164 [View Article][PubMed]
    [Google Scholar]
  25. Henson B. J., Hesselbrock S. M., Watson L. E., Barnum S. R. 2004; Molecular phylogeny of the heterocystous cyanobacteria (subsections IV and V) based on nifD . Int J Syst Evol Microbiol 54:493–497 [View Article][PubMed]
    [Google Scholar]
  26. Henson B. J., Watson L. E., Barnum S. R. 2005; Characterization of a 4 kb variant of the nifD element in Anabaena sp. strain ATCC 33047. Curr Microbiol 50:129–132[PubMed]
    [Google Scholar]
  27. Herrero A., Muro-Pastor A. M., Valladares A., Flores E. 2004; Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria. FEMS Microbiol Rev 28:469–487 [View Article][PubMed]
    [Google Scholar]
  28. Huelsenbeck J. P., Hillis D. M., Jones R. 1995; Parametric bootstrapping in molecular phylogenetics: applications and performance. In Molecular Zoology: Advances, Strategies and Protocols pp. 19–46 Edited by Ferraris J. S., Palumbi S. R. NY: Wiley-Liss;
    [Google Scholar]
  29. Jiang F. Y., Wisén S., Widersten M., Bergman B., Mannervik B. 2000; Examination of the transcription factor NtcA-binding motif by in vitro selection of DNA sequences from a random library. J Mol Biol 301:783–793 [View Article][PubMed]
    [Google Scholar]
  30. Kallas T., Coursin T., Rippka R. 1985; Different organization of nif genes in nonheterocystous and heterocystous cyanobacteria. Plant Mol Biol 5:321–329 [View Article]
    [Google Scholar]
  31. Kaneko T., Nakamura Y., Wolk C. P., Kuritz T., Sasamoto S., Watanabe A., Iriguchi M., Ishikawa A., Kawashima K. et al. other authors 2001; Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8:205–213, 227–253 [View Article][PubMed]
    [Google Scholar]
  32. Kunkel B., Losick R., Stragier P. 1990; The Bacillus subtilis gene for the development transcription factor sigma K is generated by excision of a dispensable DNA element containing a sporulation recombinase gene. Genes Dev 4:525–535 [View Article][PubMed]
    [Google Scholar]
  33. Lammers P. J., Golden J. W., Haselkorn R. 1986; Identification and sequence of a gene required for a developmentally regulated DNA excision in anabaena. Cell 44:905–911 [CrossRef]
    [Google Scholar]
  34. Lammers P. J., McLaughlin S., Papin S., Trujillo-Provencio C., Ryncarz A. J. II 1990; Developmental rearrangement of cyanobacterial nif genes: nucleotide sequence, open reading frames, and cytochrome P-450 homology of the Anabaena sp. strain PCC 7120 nifD element. J Bacteriol 172:6981–6990[PubMed]
    [Google Scholar]
  35. Lilley A., Young P., Bailey M. 2000; Bacterial population genetics: do plasmids maintain bacterial diversity and adaptation?. In The Horizontal Gene Pool pp. 287–300 Edited by Thomas C. M. Amsterdam: Harwood Academic Publishers; [View Article]
    [Google Scholar]
  36. López-Gomollón S., Hernández J. A., Pellicer S., Angarica V. E., Peleato M. L., Fillat M. F. 2007; Cross-talk between iron and nitrogen regulatory networks in Anabaena (Nostoc) sp. PCC 7120: identification of overlapping genes in FurA and NtcA regulons. J Mol Biol 374:267–281 [View Article][PubMed]
    [Google Scholar]
  37. Lynn M. E., Bantle J. A., Ownby J. D. 1986; Estimation of gene expression in heterocysts of Anabaena variabilis by using DNA-RNA hybridization. J Bacteriol 167:940–946[PubMed]
    [Google Scholar]
  38. Maruyama K., Sato N., Ohta N. 1999; Conservation of structure and cold-regulation of RNA-binding proteins in cyanobacteria: probable convergent evolution with eukaryotic glycine-rich RNA-binding proteins. Nucleic Acids Res 27:2029–2036 [View Article][PubMed]
    [Google Scholar]
  39. Mazur B. J., Chui C. F. 1982; Sequence of the gene coding for the beta-subunit of dinitrogenase from the blue-green alga Anabaena . Proc Natl Acad Sci U S A 79:6782–6786 [View Article][PubMed]
    [Google Scholar]
  40. Meeks J. C., Joseph C. M., Haselkorn R. 1988; Organization of the nif genes in cyanobacteria in symbiotic association with Azolla and Anthoceros . Arch Microbiol 150:61–71 [View Article][PubMed]
    [Google Scholar]
  41. Meeks J. C., Campbell E. L., Bisen P. S. 1994; Elements interrupting nitrogen-fixation genes in cyanobacteria – presence and absence of a nifD in clones of Nostoc sp. strain Mac. Microbiology 140:3225–3232 [View Article]
    [Google Scholar]
  42. Meeks J. C., Elhai J., Thiel T., Potts M., Larimer F., Lamerdin J., Predki P., Atlas R. 2001; An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 70:85–106 [View Article][PubMed]
    [Google Scholar]
  43. Mulligan M. E., Buikema W. J., Haselkorn R. 1988; Bacterial-type ferredoxin genes in the nitrogen fixation regions of the cyanobacterium Anabaena sp. strain PCC 7120 and Rhizobium meliloti . J Bacteriol 170:4406–4410[PubMed]
    [Google Scholar]
  44. Muro-Pastor M. I., Reyes J. C., Florencio F. J. 2001; Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels. J Biol Chem 276:38320–38328[PubMed]
    [Google Scholar]
  45. Nunes-Düby S. E., Kwon H. J., Tirumalai R. S., Ellenberger T., Landy A. 1998; Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res 26:391–406 [View Article][PubMed]
    [Google Scholar]
  46. Okada K., Kamiya Y., Zhu X. F., Suzuki K., Tanaka K., Nakagawa T., Matsuda H., Kawamukai M. 1997; Cloning of the sdsA gene encoding solanesyl diphosphate synthase from Rhodobacter capsulatus and its functional expression in Escherichia coli and Saccharomyces cerevisiae . J Bacteriol 179:5992–5998[PubMed]
    [Google Scholar]
  47. Oxelfelt F., Tamagnini P., Salema R., Lindblad P. 1995; Hydrogen uptake in Nostoc strain PCC-73102 – effects of nickel, hydrogen, carbon, and nitrogen. Plant Physiol Biochem 33:617–623
    [Google Scholar]
  48. Posada D., Crandall K. A. 1998; MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818 [View Article][PubMed]
    [Google Scholar]
  49. Prasanna R., Kaushik B. D. 1995; Nitrogen fixation and nif gene organization in branched heterocystous cyanobacteria: variation in the presence of xisA. Folia Microbiol (Praha) 40:176–180 [View Article]
    [Google Scholar]
  50. Ramasubramanian T. S., Wei T. F., Golden J. W. 1994; Two Anabaena sp. strain PCC 7120 DNA-binding factors interact with vegetative cell- and heterocyst-specific genes. J Bacteriol 176:1214–1223[PubMed]
    [Google Scholar]
  51. Ramasubramanian T. S., Wei T. F., Oldham A. K., Golden J. W. 1996; Transcription of the Anabaena sp. strain PCC 7120 ntcA gene: multiple transcripts and NtcA binding. J Bacteriol 178:922–926[PubMed]
    [Google Scholar]
  52. Ramaswamy K. S., Carrasco C. D., Fatma T., Golden J. W. 1997; Cell-type specificity of the Anabaena fdxN-element rearrangement requires xisH and xisI. Mol Microbiol 23:1241–1249 [View Article][PubMed]
    [Google Scholar]
  53. Rice D., Mazur B. J., Haselkorn R. 1982; Isolation and physical mapping of nitrogen fixation genes from the cyanobacterium Anabaena 7120. J Biol Chem 257:13157–13163[PubMed]
    [Google Scholar]
  54. Saville B., Straus N., Coleman J. R. 1987; Contiguous organization of nitrogenase genes in a heterocystous cyanobacterium. Plant Physiol 85:26–29 [View Article][PubMed]
    [Google Scholar]
  55. Sazuka T. 2003; Proteomic analysis of the cyanobacterium Anabaena sp. strain PCC 7120 with two-dimensional gel electrophoresis and amino-terminal sequencing. Photosynth Res 78:279–291 [View Article][PubMed]
    [Google Scholar]
  56. Smith M. C. M., Thorpe H. M. 2002; Diversity in the serine recombinases. Mol Microbiol 44:299–307 [View Article][PubMed]
    [Google Scholar]
  57. Tamagnini P., Costa J. L., Almeida L., Oliveira M. J., Salema R., Lindblad P. 2000; Diversity of cyanobacterial hydrogenases, a molecular approach. Curr Microbiol 40:356–361 [View Article][PubMed]
    [Google Scholar]
  58. Tanigawa R., Shirokane M., Maeda Si S., Omata T., Tanaka K., Takahashi H. 2002; Transcriptional activation of NtcA-dependent promoters of Synechococcus sp. PCC 7942 by 2-oxoglutarate in vitro . Proc Natl Acad Sci U S A 99:4251–4255 [View Article][PubMed]
    [Google Scholar]
  59. 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 22:4673–4680 [View Article][PubMed]
    [Google Scholar]
  60. Voziyanov Y., Pathania S., Jayaram M. 1999; A general model for site-specific recombination by the integrase family recombinases. Nucleic Acids Res 27:930–941 [View Article][PubMed]
    [Google Scholar]
  61. Wolk P. C., Anneliese E., Elhai J. 1994; Heterocyst metabolism and development. In The Molecular Biology of Cyanobacteria pp. 769–823 Edited by Bryant D. A. The Netherlands: Kluwer Academic Publishers;
    [Google Scholar]
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