1887

Microbiology Society logo

Volume 143, Issue 8

Genomic rearrangements during evolution of the obligate intracellular parasite Rickettsia prowazekii as inferred from an analysis of 52015 bp nucleotide sequence Free

Abstract

Summary: In this study a description is given of the sequence and analysis of 52 kb from the 1.1 Mb genome of , a member of the α-Proteobacteria. An investigation was made of nucleotide frequencies and amino acid composition patterns of 41 coding sequences, distributed in 10 genomic contigs, of which 32 were found to have putative homologues in the public databases. Overall, the coding content of the individual contigs ranged from 59 to 97%, with a mean of 81%. The genes putatively identified included genes involved in the biosynthesis of nucleotides, macromolecules and cell wall structures as well as citric acid cycle component genes. In addition, a putative identification was made of a member of the regulatory response family of two-component signal transduction systems as well as a gene encoding haemolysin. For one gene, the homologue of , an internal stop codon was discovered within a region that is otherwise highly conserved. Comparisons with the genomic structures of and have revealed several atypical gene organization patterns in the genome. For example, was found to have a unique arrangement of genes upstream of in a region that is highly conserved among other microbial genomes and thought to represent the origin of replication of a primordial replicon. The results presented in this paper support the hypothesis that the genome is a highly derived genome and provide examples of gene order structures that are unique for the

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): genome sequencing and Rickettsia prowazekii
© Society for General Microbiology 1997
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-143-8-2783
1997-08-01
2024-05-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/143/8/mic-143-8-2783.html?itemId=/content/journal/micro/10.1099/00221287-143-8-2783&mimeType=html&fmt=ahah

References

  1. Aliabadi Z., Winkler H. H., Wood D. O. 1993; Isolation and characterization of the Rickettsia prowazekii gene encoding the flavoprotein subunit of succinate dehydrogenase. Gene 133:135–140
     [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
     [Google Scholar]
  3. Andersson S. G. E., Kurland C. G. 1995; Genomic evolution drives the evolution of the translation system. Biochem Cell Biol 73:775–787
     [Google Scholar]
  4. Andersson S. G. E., Sharp P. M. 1996; Codon usage and base composition in Rickettsia prowazekii. . J Mol Evol 42:525–536
     [Google Scholar]
  5. Andersson S. G. E., Zomorodipour A., Winkler H. H., Kurland C. G. 1995; Unusual organization of the rRNA genes in Rickettsia prowazekii. . J Bacteriol 177:4171–4175
     [Google Scholar]
  6. Andersson S. G. E., Eriksson A.-S., Näslund A. K., Andersen M. S., Kurland C. G. 1996; The Rickettsia prowazekii genome: a random sequence analysis. Microb Comp Genomics 4:293–315
     [Google Scholar]
  7. Blanchin-Roland S., Blanqurt S., Schmitter J.-M., Fayat G. 1986; The gene for Escherichia coli diadenosine tetraphosphate is located immediately clockwise to folA and forms an operon with ksgA. . Mol Gen Genet 205:515–522
     [Google Scholar]
  8. Buck D., Spencer M. E., Guest J. R. 1985; Primary structure of the succinyl-CoA synthetase of Escherichia coli. . Biochemistry 24:6245–6252
     [Google Scholar]
  9. van Buul C. P. J., J. & van Knippenberg P. H. 1985; Nucleotide sequence of the ksgA gene of Escherichia coli: comparison of methyltransferases effecting dimethylation of adenosine in ribosomal RNA. Gene 38:65–72
     [Google Scholar]
  10. Chen N.-Y., Jiang S.-Q., Klein D. A., Paulus H. 1993; Organization and nucleotide sequence of the Bacillus subtilis diaminopimelate operon, a cluster of genes encoding the first three enzymes of diaminopimelate synthesis and dipicolinate synthase. J Biol Chem 268:9448–9465
     [Google Scholar]
  11. Chistoserdova L. V., Lidstrom M. E. 1994; Genetics of the serine cycle in Methylobacterium extorquens AM1: cloning, sequence, mutation, and physiological effect of glyA, the gene for serine hydroxymethyltransferase. J Bacteriol 176:6759–6763
     [Google Scholar]
  12. Clarke D. H., Fox J. P. 1948; The phenomenon of in vitro hemolysis produced by the rickettsiae of typhus fever, with a note on the mechanism of rickettsial toxicity in mice. J Exp Med 88:24–41
     [Google Scholar]
  13. Dammel C. S., Noller H. F. 1995; Suppression of a cold-sensitive mutation in 16S rRNA by overexpression of a novel ribosome-binding factor, RbfA. Genes Dev 9:626–637
     [Google Scholar]
  14. Daniel R. A., Errington J. 1993; DNA sequence of the murE–murD region of Bacillus subtilis 168. J Gen Microbiol 139:361–370
     [Google Scholar]
  15. Eremeeva M. E., Roux V., Raoult D. 1993; Determination of genome size and restriction pattern polymorphism of Rickettsia prowazekii and Rickettsia typhi by pulsed field gel electrophoresis. FEMS Microbiol Lett 11:105–112
     [Google Scholar]
  16. Fleischmann R. D. and others 1995; Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512
     [Google Scholar]
  17. Fraser C. M. and others 1995; The minimal gene complement of Mycoplasma genitalium . Science 270:397–403
     [Google Scholar]
  18. Gray M. W. 1995; Mitochondrial evolution. . In Molecular Biology of Plant Mitochondria pp. 635–659 . Edited by Levings C. S. III, Vasil I. K. Dordrecht: Kluwer Academic Publishers;
     [Google Scholar]
  19. Gupta R. S. 1995; Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of the eukaryotic cells. Mol Microbiol 15:1–11
     [Google Scholar]
  20. Hempel J., Perozich J., Romovavek H., Hinich A., Kuo I., Feingold D. S. 1994; UDP-glucose dehydrogenase from bovine liver: primary structure and relationship to other dehydrogenases. Protein Sci 3:1074–1080
     [Google Scholar]
  21. Hendrix L. R., Mallavia L. P., Samuel J. E. 1993; Cloning and sequencing of Coxiella burnetii outer membrane protein gene com1. Infect Immun 61:470–477
     [Google Scholar]
  22. Higgins D. G., Bleasby A. J., Fuchs R. 1992; clustal v: improved software for multiple sequence alignment. CABIOS 8:189–191
     [Google Scholar]
  23. Hilbert H., Himmelreich R., Plagens H., Herrmann R. 1996; Sequence analysis of 56 kb from the genome of the bacterium Mycoplasma pneumoniae comprising the dnaA region, the atp operon and a cluster of ribosomal protein genes. Nucleic Acid Res 24:628–639
     [Google Scholar]
  24. Hui F. M., Morrison D. A. 1993; Identification of a purC gene from Streptococcus pneumoniae. . J Bacteriol 175:6364–6367
     [Google Scholar]
  25. ter Huurne A. A. H., M., Muir S., van Houten M., van der Zeijst B. A. M., Gaastra W., Kusters J. G. 1994; Characterization of three putative Serpulina hyodysenteriae hemolysins. Microb Pathog 16:269–282
     [Google Scholar]
  26. Jennings M. P., Bisercic M., Dunn K. L. R., Virji M., Martin A., Wilks K. E., Richards J. C., Moxon E. R. 1995; Cloning and molecular analysis of the lsi1 (rfaF) gene of Neisseria meningitidis which encodes a heptosyl-2-transferase involved in LPS biosynthesis: evaluation of surface exposed carbohydrates in LPS mediated toxicity for human endothelial cells. Microb Pathog 19:391–407
     [Google Scholar]
  27. Kaneko T., Tanaka A., Sato S., Kotani H., Sazuka T., Miyajima N., Sugiura M., Tabata S. 1995; Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. I. Sequence features in the 1 Mb region from map position 64% to 92% of the genome. DNA Res 2:153–166
     [Google Scholar]
  28. Kaneko T. and others 1996; Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136
     [Google Scholar]
  29. Kündig C., Hennecke H., Gӧttfert M. 1993; Correlated physical and genetic map of the Bradyrhizobium japonicum 110 genome. J Bacteriol 175:613–622
     [Google Scholar]
  30. Kuramitsu S., Ogawa T., Ogawa H., Kagamiyama H. 1985; Branched-chain amino acid aminotransferase of Escherichia coli: nucleotide sequence of the ilvE gene and the deduced amino acid sequence. J Biochem 97:993–999
     [Google Scholar]
  31. Lancy E. D., Lifsics M. R., Munson P., Maurer R. 1989; Nucleotide sequence of dnaE, the gene for the polymerase subunit of DNA polymerase III in Salmonella typhimurium, and a variant that facilitates growth in the absence of another polymerase subunit. J Bacteriol 171:5581–5586
     [Google Scholar]
  32. Lawther R. P., Nichols B., Zurawski X., Hafield G. W. 1979; The nucleotide sequence preceeding and including the beginning of the ilvE gene of the ilvGEDA operon of Escherichia coli K12. Nucleic Acids Res 7:2289–2301
     [Google Scholar]
  33. Lloyd A. T., Sharp P. M. 1992; codons: a microcomputer program for codon usage analysis. J Hered 83:239–240
     [Google Scholar]
  34. Malakhov M. P., Los D. A., Wada H., Semenenko V. E., Murata N. 1995; Characterization of the murF gene of the cyanobacterium Synechocystis sp. PCC6803. Microbiology 141:163–169
     [Google Scholar]
  35. Miczak A., Chauhan A. K., Apirion D. 1991; Two new genes located between 2758 and 2761 kilobase pairs on the Escherichia coli genome. J Bacteriol 173:3271–3272
     [Google Scholar]
  36. Moshiri F., Chawla A., Maier R. 1991; Cloning, characterisation, and expression in Escherichia coli of the genes encoding the cytochrome d oxidase complex from Azotobacter vinelandii. . J Bacteriol 173:6230–6241
     [Google Scholar]
  37. Muto A., Osawa S. 1987; The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84:166–169
     [Google Scholar]
  38. Myers E., Miller W. 1988; Optimal alignments in linear space. CABIOS 4:11–17
     [Google Scholar]
  39. Nishiyama M., Horinouchi S., Beppu T. 1991; Characterization of an operon encoding succinyl-CoA synthetase and malate dehydrogenase from Thermus flavus AT-62 and its expression in Escherichia coli. . Mol Gen Genet 226:1–9
     [Google Scholar]
  40. Ogasawara N., Moriya S., von Meyerbur K., Hansen F. G., Yoshikawa H. 1985; Conservation of genes and their organization in the chromosomal replication origins of Bacillus subtilis and Escherichia coli. . EMBO J 4:3345–3350
     [Google Scholar]
  41. Oguro A., Kakeshita H., Honda K., Takamatsu H., Nakamura K., Yamane K. 1995; srb: a Bacillus subtilis gene encoding a homologue of the alpha-subunit of the mammalian signal recognition particle receptor. DNA Res 2:95–100
     [Google Scholar]
  42. Olsen G. J., Woese C. R., Overbeek R. 1994; The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol 176:1–6
     [Google Scholar]
  43. Oppermann F. B., Steinbüchel A. 1994; Identification and molecular characterization of the aco genes encoding the Pelobacter carbinolicus acetoin dehydrogenase enzyme system. J Bacteriol 176:469–485
     [Google Scholar]
  44. Pang H., Winkler H. H. 1993; Copy number of the 16S rRNA gene in Rickettsia prowazekii. . J Bacteriol 175:3893–3896
     [Google Scholar]
  45. Parquet C., Flouret B., Mengin-Lecreulx D., van Heijenoort J. 1989; Nucleotide sequence of the murF gene encoding the UDP-MurNAc-pentapeptide synthetase of Escherichia coli. . Nucleic Acids Res 17:5379
     [Google Scholar]
  46. Ramm L. E., Winkler H. H. 1973a; Rickettsial hemolysis: adsorption of rickettsiae to erythrocytes. Infect Immun 7:93–99
     [Google Scholar]
  47. Ramm L. E., Winkler H. H. 1973b; Rickettsial hemolysis: effect of metabolic inhibitors upon hemolysis and adsorption. Infect Immun 7:550–555
     [Google Scholar]
  48. Roux V., Raoult D. 1993; Genotypic identification and phylogenetic analysis of the spotted fever group rickettsiae by pulsed-field gel electrophoresis. J Bacteriol 175:4895–4909
     [Google Scholar]
  49. Salvi S., Trinei M., Lanfaloni L., Pon C. L. 1994; Cloning and characterization of the gene encoding an esterase from Spirulina platensis. . Mol Gen Genet 243:124–126
     [Google Scholar]
  50. Schramek S. 1972; Deoxyribonucleic acid base composition of members of the typhus group of rickettsiae. Acta Virol 16:447
     [Google Scholar]
  51. Seki T., Yoshikawa H., Takahashi H., Saitou H. 1987; Cloning and nucleotide sequence of phoP, the regulatory gene for alkaline phosphatase and phosphodiesterase in Bacillus subtilis. . J Bacteriol 169:2913–2916
     [Google Scholar]
  52. Shazand K., Tucker J., Grunberg-Manago M., Rabinowitz J. C., Leighton T. 1993; Similar organization of the nusA–infB operon in Bacillus subtilis and Escherichia coli. . J Bacteriol 175:2880–2887
     [Google Scholar]
  53. Shibata C., Ehara T., Tomura K., Igarashi K., Kobayashi H. 1992; Gene structure of the Enterococcus hirae (Streptococcus faecalis) F1F0-ATPase, which functions as a regulator of cytoplasmic pH. J Bacteriol 174:6117–6124
     [Google Scholar]
  54. Stock J. B., Ninfa A. J., Stock A. M. 1989; Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev 52:450–490
     [Google Scholar]
  55. Syvänen A.-C., Amiri H., Jamal A., Andersson S. G. E., Kurland C. G. 1996; A chimeric disposition of elongation factor genes in Rickettsia prowazekii. . J Bacteriol 178:6192–6199
     [Google Scholar]
  56. 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
     [Google Scholar]
  57. Tokito M. K., Daldal F. 1992; petR, located upstream of the fbcFBC operon encoding the cytochrome bc 1 complex, is homologous to bacterial response regulators and necessary for photosynthetic and respiratory growth of Rhodobacter capsulatus. . Mol Microbiol 6:1645–1654
     [Google Scholar]
  58. Tyeryar F. J., Weiss E., Millar D. B., Bozeman F. M., Ormsbee R. A. 1973; DNA base composition of rickettsiae. Science 180:415–417
     [Google Scholar]
  59. Uemori T., Ishino Y., Fujita K., Asada K., Kato I. 1993; Cloning of the DNA polymerase gene of Bacillus caldotenax and characterization of the gene product. J Biochem 113:401–410
     [Google Scholar]
  60. Viale A., Arakaki A. K. 1994; The chaperone connection to the origins of the eukaryotic organelles. FEBS Lett 341:146–151
     [Google Scholar]
  61. Williamson L. R., Plano G. V., Winkler H. H., Krause D. C., Wood D. O. 1989; Nucleotide sequence of the Rickettsia prowazekii ATP/ADP translocase gene. Gene 80:269–278
     [Google Scholar]
  62. Winkler H. H. 1974; Inhibitory and restorative effects of adenine nucleotides on rickettsial adsorption and hemolysis. Infect Immun 9:119–126
     [Google Scholar]
  63. Winkler H. H. 1976; Rickettsial permeability: an ATP/ADP transport system. J Biol Chem 251:389–396
     [Google Scholar]
  64. Winkler H. H., Daughtery R. M. 1984; Regulatory role of phosphate and other anions in transport of ADP and ATP by Rickettsia prowazekii. . J Bacteriol 160:76–79
     [Google Scholar]
  65. Winkler H. H., Miller E. T. 1980; Phospholipase A activity in the hemolysis of sheep and human erythrocytes by Rickettsia prowazekii. . Infect Immun 29:316–321
     [Google Scholar]
  66. Winkler H. H., Miller E. T. 1982; Phospholipase A and the interaction of Rickettsia prowazekii and mouse fibroblasts (L-292 cells). Infect Immun 38:109–113
     [Google Scholar]
  67. Winkler H. H., Miller E. T. 1989; Phospholipase A activity associated with the growth of Rickettsia prowazekii in L929 cells. Infect Immun 57:36–40
     [Google Scholar]
  68. Wood D. O., Williamson L. R., Winkler H. H., Krause D. C. 1987; Nucleotide sequence of the Rickettsia prowazekii citrate synthase gene. J Bacteriol 169:3564–3572
     [Google Scholar]
  69. Yura T., Mori H., Nagai H., Nagata T., Ishihama A., Fujita N., Isono K., Mizobuchi K., Nakata A. 1992; Systematic sequencing of the Escherichia coli genome: analysis of the 02.4 min region. Nucleic Acids Res 20:3305–3308
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-143-8-2783
Loading
Genomic rearrangements during evolution of the obligate intracellular parasite Rickettsia prowazekii as inferred from an analysis of 52015 bp nucleotide sequence
Microbiology 143, 2783 (1997); https://doi.org/10.1099/00221287-143-8-2783
/content/journal/micro/10.1099/00221287-143-8-2783
/content/journal/micro/10.1099/00221287-143-8-2783
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error