Abstract
An 8.5-kb plasmid encoding genes (leuABCD) involved in leucine biosynthesis and a small plasmid of 1.74 kb of yet unknown function were found in the intracellular symbiont, Buchnera aphidicola, of two divergent aphid species, Thelaxes suberi and Tetraneura caerulescens, respectively. The leuABCD-carrying plasmid (pBTs1) was amplified from total aphid DNA by inverse long PCR, using outwardly oriented oligonucleotide primers specific to leuA. The resulting 8.2-kb PCR fragment as well as the 1.74-kb plasmid (pBTc1) were cloned and sequenced. pBTs1 differed from a previously described B. aphidicola plasmid (pRPE) of the aphid Rhopalosiphum padi by the presence of a small heat shock gene (ibp) and in the order of the leuABCD and repA genes. Comparison of both leucine plasmids to the small plasmid pBTc1 revealed extensive similarity with respect to putative replication functions as well as in the presence of a highly conserved open reading frame that was found to be homologous to Escherichia coli YqhA and Haemophilus influenzae HI0507 and which may encode an integral membrane protein. The three B. aphidicola plasmids most likely evolved from a common ancestral replicon, which in turn may be distantly related to IncFII plasmids. Phylogenetic affiliations of the B. aphidicola strains of the two aphid species were assessed by sequencing of their 16S rRNA genes. Evaluation of the distribution of the leuABCD-encoding plasmids within a phylogenetic framework suggests independent origins for pBTs1 and pRPE from an ancestral replicon resembling pBTc1. The implications for symbiotic essential amino acid biosynthesis and provisioning are discussed.
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- Allen S. P., Polazzi J. O., Gierse J. K., Easton A. M. Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J Bacteriol. 1992 Nov;174(21):6938–6947. doi: 10.1128/jb.174.21.6938-6947.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- Baumann L., Baumann P. Growth Kinetics of the Endosymbiont Buchnera aphidicola in the Aphid Schizaphis graminum. Appl Environ Microbiol. 1994 Sep;60(9):3440–3443. doi: 10.1128/aem.60.9.3440-3443.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baumann P., Baumann L., Lai C. Y., Rouhbakhsh D., Moran N. A., Clark M. A. Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol. 1995;49:55–94. doi: 10.1146/annurev.mi.49.100195.000415. [DOI] [PubMed] [Google Scholar]
- Bracho A. M., Martínez-Torres D., Moya A., Latorre A. Discovery and molecular characterization of a plasmid localized in Buchnera sp. bacterial endosymbiont of the aphid Rhopalosiphum padi. J Mol Evol. 1995 Jul;41(1):67–73. doi: 10.1007/BF00174042. [DOI] [PubMed] [Google Scholar]
- Caspers G. J., Leunissen J. A., de Jong W. W. The expanding small heat-shock protein family, and structure predictions of the conserved "alpha-crystallin domain". J Mol Evol. 1995 Mar;40(3):238–248. doi: 10.1007/BF00163229. [DOI] [PubMed] [Google Scholar]
- Chuang S. E., Burland V., Plunkett G., 3rd, Daniels D. L., Blattner F. R. Sequence analysis of four new heat-shock genes constituting the hslTS/ibpAB and hslVU operons in Escherichia coli. Gene. 1993 Nov 30;134(1):1–6. doi: 10.1016/0378-1119(93)90167-2. [DOI] [PubMed] [Google Scholar]
- Clark M. A., Baumann L., Baumann P. Sequence analysis of an aphid endosymbiont DNA fragment containing rpoB (beta-subunit of RNA polymerase) and portions of rplL and rpoC. Curr Microbiol. 1992 Nov;25(5):283–290. doi: 10.1007/BF01575863. [DOI] [PubMed] [Google Scholar]
- Cowing D. W., Bardwell J. C., Craig E. A., Woolford C., Hendrix R. W., Gross C. A. Consensus sequence for Escherichia coli heat shock gene promoters. Proc Natl Acad Sci U S A. 1985 May;82(9):2679–2683. doi: 10.1073/pnas.82.9.2679. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Douglas A. E. Mycetocyte symbiosis in insects. Biol Rev Camb Philos Soc. 1989 Nov;64(4):409–434. doi: 10.1111/j.1469-185x.1989.tb00682.x. [DOI] [PubMed] [Google Scholar]
- Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17(6):368–376. doi: 10.1007/BF01734359. [DOI] [PubMed] [Google Scholar]
- Fukatsu T., Ishikawa H. Occurrence of chaperonin 60 and chaperonin 10 in primary and secondary bacterial symbionts of aphids: implications for the evolution of an endosymbiotic system in aphids. J Mol Evol. 1993 Jun;36(6):568–577. doi: 10.1007/BF00556361. [DOI] [PubMed] [Google Scholar]
- Gemmill R. M., Wessler S. R., Keller E. B., Calvo J. M. leu operon of Salmonella typhimurium is controlled by an attenuation mechanism. Proc Natl Acad Sci U S A. 1979 Oct;76(10):4941–4945. doi: 10.1073/pnas.76.10.4941. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Godon J. J., Chopin M. C., Ehrlich S. D. Branched-chain amino acid biosynthesis genes in Lactococcus lactis subsp. lactis. J Bacteriol. 1992 Oct;174(20):6580–6589. doi: 10.1128/jb.174.20.6580-6589.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
- Lai C. Y., Baumann L., Baumann P. Amplification of trpEG: adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3819–3823. doi: 10.1073/pnas.91.9.3819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lai C. Y., Baumann P. Genetic analysis of an aphid endosymbiont DNA fragment homologous to the rnpA-rpmH-dnaA-dnaN-gyrB region of eubacteria. Gene. 1992 Apr 15;113(2):175–181. doi: 10.1016/0378-1119(92)90393-4. [DOI] [PubMed] [Google Scholar]
- Lai C. Y., Baumann P., Moran N. A. Genetics of the tryptophan biosynthetic pathway of the prokaryotic endosymbiont (Buchnera) of the aphid Schlechtendalia chinensis. Insect Mol Biol. 1995 Feb;4(1):47–59. doi: 10.1111/j.1365-2583.1995.tb00007.x. [DOI] [PubMed] [Google Scholar]
- Latorre A., Moya A., Ayala F. J. Evolution of mitochondrial DNA in Drosophila subobscura. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8649–8653. doi: 10.1073/pnas.83.22.8649. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lisser S., Margalit H. Compilation of E. coli mRNA promoter sequences. Nucleic Acids Res. 1993 Apr 11;21(7):1507–1516. doi: 10.1093/nar/21.7.1507. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ludwig W., Schleifer K. H. Bacterial phylogeny based on 16S and 23S rRNA sequence analysis. FEMS Microbiol Rev. 1994 Oct;15(2-3):155–173. doi: 10.1111/j.1574-6976.1994.tb00132.x. [DOI] [PubMed] [Google Scholar]
- Maidak B. L., Olsen G. J., Larsen N., Overbeek R., McCaughey M. J., Woese C. R. The Ribosomal Database Project (RDP). Nucleic Acids Res. 1996 Jan 1;24(1):82–85. doi: 10.1093/nar/24.1.82. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marchuk D., Drumm M., Saulino A., Collins F. S. Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nucleic Acids Res. 1991 Mar 11;19(5):1154–1154. doi: 10.1093/nar/19.5.1154. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moran N. A. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2873–2878. doi: 10.1073/pnas.93.7.2873. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morioka M., Ishikawa H. Mutualism based on stress: selective synthesis and phosphorylation of a stress protein by an intracellular symbiont. J Biochem. 1992 Apr;111(4):431–435. doi: 10.1093/oxfordjournals.jbchem.a123774. [DOI] [PubMed] [Google Scholar]
- Munson M. A., Baumann L., Baumann P. Buchnera aphidicola (a prokaryotic endosymbiont of aphids) contains a putative 16S rRNA operon unlinked to the 23S rRNA-encoding gene: sequence determination, and promoter and terminator analysis. Gene. 1993 Dec 31;137(2):171–178. doi: 10.1016/0378-1119(93)90003-l. [DOI] [PubMed] [Google Scholar]
- Munson M. A., Baumann P., Clark M. A., Baumann L., Moran N. A., Voegtlin D. J., Campbell B. C. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol. 1991 Oct;173(20):6321–6324. doi: 10.1128/jb.173.20.6321-6324.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Munson M. A., Baumann P. Molecular cloning and nucleotide sequence of a putative trpDC(F)BA operon in Buchnera aphidicola (endosymbiont of the aphid Schizaphis graminum). J Bacteriol. 1993 Oct;175(20):6426–6432. doi: 10.1128/jb.175.20.6426-6432.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Narberhaus F., Weiglhofer W., Fischer H. M., Hennecke H. The Bradyrhizobium japonicum rpoH1 gene encoding a sigma 32-like protein is part of a unique heat shock gene cluster together with groESL1 and three small heat shock genes. J Bacteriol. 1996 Sep;178(18):5337–5346. doi: 10.1128/jb.178.18.5337-5346.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohtaka C., Nakamura H., Ishikawa H. Structures of chaperonins from an intracellular symbiont and their functional expression in Escherichia coli groE mutants. J Bacteriol. 1992 Mar;174(6):1869–1874. doi: 10.1128/jb.174.6.1869-1874.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olsen G. J., Matsuda H., Hagstrom R., Overbeek R. fastDNAmL: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput Appl Biosci. 1994 Feb;10(1):41–48. doi: 10.1093/bioinformatics/10.1.41. [DOI] [PubMed] [Google Scholar]
- Rouhbakhsh D., Baumann P. Characterization of a putative 23S-5S rRNA operon of Buchnera aphidicola (endosymbiont of aphids) unlinked to the 16S rRNA-encoding gene. Gene. 1995 Mar 21;155(1):107–112. doi: 10.1016/0378-1119(94)00910-k. [DOI] [PubMed] [Google Scholar]
- Rzhetsky A. Estimating substitution rates in ribosomal RNA genes. Genetics. 1995 Oct;141(2):771–783. doi: 10.1093/genetics/141.2.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sauer U., Dürre P. Sequence and molecular characterization of a DNA region encoding a small heat shock protein of Clostridium acetobutylicum. J Bacteriol. 1993 Jun;175(11):3394–3400. doi: 10.1128/jb.175.11.3394-3400.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tisa L. S., Rosen B. P. Transport systems encoded by bacterial plasmids. J Bioenerg Biomembr. 1990 Aug;22(4):493–507. doi: 10.1007/BF00762959. [DOI] [PubMed] [Google Scholar]
- Unterman B. M., Baumann P., McLean D. L. Pea aphid symbiont relationships established by analysis of 16S rRNAs. J Bacteriol. 1989 Jun;171(6):2970–2974. doi: 10.1128/jb.171.6.2970-2974.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wessler S. R., Calvo J. M. Control of leu operon expression in Escherichia coli by a transcription attenuation mechanism. J Mol Biol. 1981 Jul 15;149(4):579–597. doi: 10.1016/0022-2836(81)90348-x. [DOI] [PubMed] [Google Scholar]
- Womble D. D., Rownd R. H. Genetic and physical map of plasmid NR1: comparison with other IncFII antibiotic resistance plasmids. Microbiol Rev. 1988 Dec;52(4):433–451. doi: 10.1128/mr.52.4.433-451.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]