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Aspects of energy-yielding metabolism in the aphid,Schizaphis graminum, and its endosymbiont: Detection of gene fragments potentially coding for the ATP synthaseβ-subunit and glyceraldehyde-3-phosphate dehydrogenase

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Abstract

Specialized cells within the aphid,Schizaphis graminum, contain intracellular, vesicleenclosed eubacterial endosymbionts (Buchnera aphidicola). Using oligonucleotide probes derived from conserved sequences of the ATP synthase β-subunit and glyceraldehyde-3-phosphate dehydrogenase, and the polymerase chain reaction (PCR), we have amplified, cloned, and sequenced three DNA fragments. Amino acid sequence similarity indicated that two of these fragments corresponded to endosymbiont and host genes potentially coding for the β-subunit of ATP synthase. The host gene fragment contained two putative introns. The third DNA fragment corresponded to a portion of a gene coding for a glyceraldehyde-3-phosphate dehydrogenase that was highly related to one of the enzymes fromEscherichia coli (GapA). These results indicate thatB. aphidicola may have an ATP synthase and consequently could synthesize ATP from a proton motive force generated within the intracellular vesicles of host cells containing the endosymbionts. The detection of a gene fragment coding for a protein similar to glyceraldehyde-3-phosphate dehydrogenase suggests the presence of this glycolytic enzyme in the endosymbiont and its involvement in energy-yielding metabolism.

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Literature Cited

  1. Alefounder PR, Perham RN (1989) Identification, molecular cloning and sequence analysis of a gene cluster encoding the class II fructose 1,6-biphosphate aldolase, 3-phosphoglycerate kinase and a putative second glyceraldehyde 3-phosphate dehydrogenase ofEscherichia coli. Mol Microbiol 3:723–732

    Google Scholar 

  2. Amann R, Ludwig W, Schleifer KH (1988) β-subunit of ATP-synthase: a useful marker for studying the phylogenetic relationships of eubacteria. J Gen Microbiol 134:2815–2821

    Google Scholar 

  3. Breen GAM, Holmans PL, Garnett KE (1988) Isolation and characterization of a complementary DNA for the nuclearcoded precursor of the β-subunit of bovine mitochondrial F1-ATPase. Biochemistry 27:3955–3961

    Google Scholar 

  4. Branlant G, Branlant C (1985) Nucleotide sequence of theEscherichia coli gap gene. Different evolutionary behavior or the NAD+-binding domain and of the catalytic domain ofd-glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 150:61–66

    Google Scholar 

  5. Campbell BC (1990) On the role of microbial symbiotes in herbivorous insects. In: Bernays EA (ed) Insect-plant interactions, vol I. Boca Raton, Florida: CRC Press, Inc., pp 1–44

    Google Scholar 

  6. Clark MA, Baumann L, Baumann P (1992) Sequence analysis of an aphid endosymbiont DNA fragment containingrpoB (β-subunit of RNA polymerase) and portions ofrplL andrpoC. Curr Microbiol 25:283–290

    Google Scholar 

  7. Clark MA, Baumann L, Munson MA, Baumann P, Campbell BC, Duffus JE, Osborne LS, Moran NA (1992) The eubacterial endosymbionts of whitefies (Homoptera: Aleyrodoidea) constitute a lineage distinct from the endosymbionts of aphids and mealybugs. Curr Microbiol 25:119–123

    Google Scholar 

  8. Conway T, Sewell GW, Ingram LO (1987) Glyceraldehyde-3-phosphate dehydrogenase gene fromZymomonas mobilis: cloning, sequencing, and identification of promoter region. J Bacteriol 169:5653–5662

    Google Scholar 

  9. Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev 64:409–434

    Google Scholar 

  10. Hensel R, Zwickl P, Fabry S, Lang J, Palm P (1989) Sequence comparison of glyceraldehyde-3-phosphate dehydrogenases from the three urkingdoms: evolutionary implication. Can J Microbiol 35:81–85

    Google Scholar 

  11. Houk EJ (1987) Symbionts. In: Minks AK, Harrewijn P (eds) Aphids; their biology, natural enemies, and control, vol 2A. Amsterdam: Elsevier Biomedical Press, pp 123–129

    Google Scholar 

  12. Ishikawa H (1989) Biochemical and molecular aspects of endosymbiosis in insects. Int Rev Cytol 116:1–45

    Google Scholar 

  13. Lai C-Y, Baumann P (1992) Genetic analysis of an aphid endosymbiont DNA fragment homologous to thernpA-rpmH-dnaA-dnaN-gyrB region of eubacteria. Gene 113:175–181

    Google Scholar 

  14. Lai C-Y, Baumann P (1992) Sequence analysis of a DNA fragment ofBuchnera aphidicola (endosymbiont of aphids) containing genes homologous todnaG, rpoD, cysE, andsecB. Gene 119:113–118

    Google Scholar 

  15. Lawrence JG, Ochman H, Hartl DL (1991) Molecular and evolutionary relationships among enteric bacteria. J Gen Microbiol 137:1911–1921

    Google Scholar 

  16. Lewin B (1990) Genes IV. Oxford: Oxford University Press, pp 595–600

    Google Scholar 

  17. Michels PAM, Marchand M, Kohl L. Allert S, Wierenga RK, Opperdoes FR (1991) The cytosolic and glycosomal isoenzymes of glyceraldehyde-3-phosphate dehydrogenase inTrypanosoma brucei have a distant evolutionary relationship. Eur J Biochem 198:421–428

    Google Scholar 

  18. Munson MA, Baumann P, Kinsey MG (1991a)Buchneara gen. nov. andBuchnera aphidicola sp. nov., a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. Int J Syst Bacteriol 41:566–568

    Google Scholar 

  19. Munson MA, Baumann P, Clark MA, Baumann L, Moran NA, Voegtlin DJ, Campbell BC (1991b) Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol 173:6321–6324

    Google Scholar 

  20. Munson MA, Baumann L, Baumann P (1992)Buchnera aphidicola, the endosymbiont of aphids, contains genes for four ribosomal RNA proteins, initiation factor-3, and the α-subunit of RNA polymerase. Curr Microbiol 24:23–29

    Google Scholar 

  21. Padget RA, Grabowski PJ, Konarska MM, Seiler S, Shart PA (1986) Splicing of messenger RNA precursors. Annu Rev Biochem 55:1119–1150

    Google Scholar 

  22. Sharp PA (1987) Splicing of messenger RNA precursors. Science 235:766–771

    Google Scholar 

  23. Sharp PA (1987) Nutritional physiology. In: Minks AK, Harrewijn P (eds) Aphids; their biology, natural enemies, and control, vol 2A. Amsterdam: Elsevier Biomedical Press, pp 99–121

    Google Scholar 

  24. Walker JE, Saraste M, Gay NJ (1984) Theunc operon. Nucleotide sequence, regulation and structure of ATP-synthase. Biochim Biophys Acta 768:164–200

    Google Scholar 

  25. Williamson LR, Plano GV, Winkler HH, Krause DC, Wood DO (1989) Nucleotide sequence of theRickettsia prowazekii ATP/ADP translocase-encoding gene. Gene 80:269–278

    Google Scholar 

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Clark, M.A., Baumann, P. Aspects of energy-yielding metabolism in the aphid,Schizaphis graminum, and its endosymbiont: Detection of gene fragments potentially coding for the ATP synthaseβ-subunit and glyceraldehyde-3-phosphate dehydrogenase. Current Microbiology 26, 233–237 (1993). https://doi.org/10.1007/BF01577382

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