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Cloning and characterization of an ftsZ homologue from a bacterial symbiont of Drosophila melanogaster

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Abstract

A 1194 by open reading frame that codes for a 398 amino acid peptide was cloned from a λgt11 library of Drosophila melanogaster genomic DNA. The predicted peptide sequence is very similar to three previously characterized protein sequences that are encoded by the ftsZ genes in Escherichia coli, Bacillus subtilis and Rhizobium meliloti. The FtsZ protein has a major role in the initiation of cell division in prokaryotic cells. Using a tetracycline treatment that eradicates bacterial parasites from insects, the ftsZ homologue has been found to be derived from a bacterium that lives within the strain. However, polymerase chain reaction (PCR) amplification of the gene from treated embryos suggests that it is not derived from a gut bacterium. Nevertheless, by amplifying and characterizing part of the 16S rRNA from this bacterium we have been able to demonstrate that it is a member of the genus Wolbachia, a parasitic organism that infects, and disturbs the sexual cycle of various strains of Drosophila simulans. We suggest that this ftsZ homologue is implicated in the cell division of Wolbachia, an organism that fails to grow outside the host organism. Sequence and alignment analysis of this ftsZ homologue show the presence of a potential GTP-binding motif indicating that it may function as a GTPase. The consequences of this function particularly with respect to its role in cell division are discussed.

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References

  • Ashburner M (1989) Drosophila: a laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Beall B, Lowe M, Lutkenhaus JF (1988) Cloning and characterization of Bacillus subtilis homologs of Escherichia coli cell division genes ftsZ and ftsA. J Bacteriol 170:4855–4864

    Google Scholar 

  • Begg K, Donachie WD (1985) Cell shape and division in Escherichia coli: experiments with shape and division mutations. J Bacteriol 174:63–70

    Google Scholar 

  • Bi E, Lutkenhaus JF (1990) FtsZ regulates frequency of cell division in Escherichia coli. J Bacteriol 172:2765–2768

    Google Scholar 

  • Bi E, Lutkenhaus JF (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354:161–164

    Google Scholar 

  • Bourne HR, Sanders DA, McCormick F (1991) The GTPase superfamily: conserved structure and molecular mechanism. Nature 349:117–127

    Google Scholar 

  • Campbell BC, Bragg TS, Turner C (1992) Phylogeny of symbiotic bacteria of four weevil species (Curculionidae: Coleoptera) based on analysis of ribosomal DNA. Insect Biochem 22:415–421

    Google Scholar 

  • Corton JC, Ward JJE, Lutkenhaus JF (1987) Analysis of the cell division gene ftsZ (sulB) from gram-negative and gram-positive bacteria. J Bacteriol 169:1–7

    Google Scholar 

  • Dai K, Lutkenhaus JF (1991) ftsZ Is an essential cell division gene in Escherichia coli. J Bacteriol 173:3500–3506

    Google Scholar 

  • de Boer PAJ, Cook WR, Rothfield LI (1990) Bacterial cell division. Annu Rev Genet 24:249–274

    Google Scholar 

  • de Boer PAJ, Crossley R, Rothfield LI (1992) The essential bacterial cell-division protein FtsZ is a GTPase. Nature 359:254–256

    Google Scholar 

  • Devereux J, Haebert M, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395

    Google Scholar 

  • Feinberg A, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13

    Google Scholar 

  • Glover DM, Raff J, Karr T, O'Neill SL, Lin H, Wolfner MF (1990) Parasites in Drosophila embryos. Nature 348:117

    Google Scholar 

  • Hertig M (1936) The rickettsia Wolbachia pipientis (gen et sp n) and associated inclusions of the mosquito, Culex pipiens. Parisitology 28:453–486

    Google Scholar 

  • Higgins DG, Sharp PM (1989) Fast and sensitive multiple sequence alignments on the microcomputer. CABIOS 5:151–153

    Google Scholar 

  • Hoffmann AA (1988) Partial cytoplasmic incompatibility between two Australian populations of Drosophila melanogaster. Entomologia Experimentalis et Applicata 48:61–67

    Google Scholar 

  • Hoffmann AA, Turelli M, Simmons GM (1986) Unidirectional incompatibility between populations of Drosophila simulans. Evolution 40:692–701

    Google Scholar 

  • Holden PR, Jones P, Brookfield JFY (1993) Evidence for a Wolbachia Symbiont in Drosophila melanogaster which does not cause cytoplasmic incompatability. Genetical Research (in press)

  • Lipmann DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227:1435–1441

    Google Scholar 

  • Lutkenhaus JF (1990) Regulation of cell division in E. coli. Trends Genet 6:22–25

    Google Scholar 

  • Lutkenhaus JF, Wolf-Watz H, Donachie WD (1980) Organisation of genes in the ftsA-envA region of Escherichia coli genomic map and identification of a new fts locus (ftsZ). J Bacteriol 142:615–620

    Google Scholar 

  • Margolin W, Corbo JC, Long SR (1991) Cloning and characterization of a Rhizobium meliloti homolog of the Escherichia coli cell division gene ftsZ. J Bacteriol 173:5822–5830

    Google Scholar 

  • Mukherjee A, Kang D, Lutkenhans J (1993) Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc Natl Acad Sci USA 90:1053–1057

    Google Scholar 

  • Ochman H, Wilson AC (1987) Evolutionary history of enteric bacteria. In: Neidhardt FC (ed) Escherichia coli and Salmonella typhimurium: cellular and molecular biology. American Society for Microbiology, Washington DC, pp 1649–1654

    Google Scholar 

  • O'Neill SL, Karr TL (1990) Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348:178–180

    Google Scholar 

  • O'Neill SL, Giordano R, Colbert AME, Karr TL, Robertson HM (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA 89:2699–2702

    Google Scholar 

  • RayChaudhuri D, Park JT (1992) Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature 359:251–254

    Google Scholar 

  • Ridley AJ, Hall A (1992) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389–399

    Google Scholar 

  • Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A (1992) The small GTP-binding protein rac regulates growth factor-induced ruffling. Cell 70:401–410

    Google Scholar 

  • Rousset F, Vautrin D, Solignac M (1992) Molecular identification of Wolbachia, the agent of cytoplasmic incompatibility in Drosophila simulans, and variability in relation with host mitochondrial types. Proc R Soc Lond [Biol] 247:163–168

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor New York

    Google Scholar 

  • Stevens L, Wade MJ (1990) Cytoplasmically inherited reproductive incompatibility in Tribolium flour beetles: the rate of spread and effect on population size. Genetics 124:367–372

    Google Scholar 

  • Turelli M, Hoffmann AA (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353:440–442

    Google Scholar 

  • Yi QM, Lutkenhaus J (1985) The nucleotide sequence of the essential cell division gene ftsZ of Escherichia coli. Gene 36:241–247

    Google Scholar 

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Communicated by D. Finnegan

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Holden, P.R., Brookfield, J.F. & Jones, P. Cloning and characterization of an ftsZ homologue from a bacterial symbiont of Drosophila melanogaster . Molec. Gen. Genet. 240, 213–220 (1993). https://doi.org/10.1007/BF00277059

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  • DOI: https://doi.org/10.1007/BF00277059

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