1887

Abstract

Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) plays an important role in glucose catabolism, converting glyceraldehyde 3-phosphates to 1,3-bisphosphoglycerates. Open reading frame (ORF) in the genome of pv. () strain 8004 is the only ORF in this strain annotated to encode a GAPDH. In this work, we have demonstrated genetically that this ORF encodes a unique GAPDH in strain 8004, which seems to be constitutively expressed. A GAPDH-deficient mutant could still grow in medium with glucose or other sugars as the sole carbon source, and no phosphofructokinase activity was detectable in strain 8004. These facts suggest that may employ the Entner–Doudoroff pathway, but not glycolysis, to utilize glucose. The mutant could not utilize pyruvate as sole carbon source, whereas the wild-type could, implying that the GAPDH of is involved in gluconeogenesis. Furthermore, inactivation of the GAPDH resulted in impairment of bacterial growth and virulence in the host plant, and reduction of intracellular ATP and extracellular polysaccharide (EPS). This reveals that GAPDH is required for EPS production and full pathogenicity of .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.023762-0
2009-05-01
2020-07-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/5/1602.html?itemId=/content/journal/micro/10.1099/mic.0.023762-0&mimeType=html&fmt=ahah

References

  1. Alvarez A. M.. 2000; Black rot of crucifers.. In Mechanisms of Resistance to Plant Diseases pp21–52 Edited by Slusarenko A. J., Fraser R. S. S., C L.. van Loon. Dordrecht: Kluwer Academic Publications;
  2. Becker A., Katzen F., Pühler A., Ielpi L.. 1998; Xanthan gum biosynthesis and application: a biochemical/genetic perspective. Appl Microbiol Biotechnol50:145–152
    [Google Scholar]
  3. Blanvillain S., Meyer D., Boulanger A., Lautier M., Guynet C., Denance N., Vasse J., Lauber E., Arlat M.. 2007; Plant carbohydrate scavenging through TonB-dependent receptors: a feature shared by phytopathogenic and aquatic bacteria. PLoS One2:e224
    [Google Scholar]
  4. Charpentier B., Bardey V., Robas N., Branlant C.. 1998; The EIIGlc protein is involved in glucose-mediated activation of Escherichia coli gapA and gapB-pgk transcription. J Bacteriol180:6476–6483
    [Google Scholar]
  5. Daniels M. J., Barber C. E., Turner P. C., Sawczyc M. K., Byrde R. J., Fielding A. H.. 1984; Cloning of genes involved in pathogenicity of Xanthomonas campestris pv. campestris using the broad host range cosmid pLAFR1. EMBO J3:3323–3328
    [Google Scholar]
  6. de Crécy-Lagard V., Bouvet O. M., Lejeune P., Danchin A.. 1991; Fructose catabolism in Xanthomonas campestris pv. campestris . Sequence of the PTS operon, characterization of the fructose-specific enzymes. J Biol Chem266:18154–18161
    [Google Scholar]
  7. Denny T. P.. 1995; Involvement of bacterial polysaccharides in plant pathogenesis. Annu Rev Phytopathol33:173–197
    [Google Scholar]
  8. Doan T., Aymerich S.. 2003; Regulation of the central glycolytic genes in Bacillus subtilis : binding of the repressor CggR to its single DNA target sequence is modulated by fructose-1,6-bisphosphate. Mol Microbiol47:1709–1721
    [Google Scholar]
  9. Dow J. M., Crossman L., Findlay K., He Y.-Q., Feng J.-X., Tang J.-L.. 2003; Biofilm dispersal in Xanthomonas campestris is controlled by cell–cell signaling and is required for full virulence to plants. Proc Natl Acad Sci U S A100:10995–11000
    [Google Scholar]
  10. Fillinger S., Boschi-Muller S., Azza S., Dervyn E., Branlant G., Aymerich S.. 2000; Two glyceraldehyde 3-phosphate dehydrogenases with opposite physiological roles in a nonphotosynthetic bacterium. J Biol Chem275:14031–14037
    [Google Scholar]
  11. Ganter C., Plückthun A.. 1990; Glycine to alanine substitutions in helices of glyceraldehyde-3-phosphate dehydrogenase: effects on stability. Biochemistry29:9395–9402
    [Google Scholar]
  12. Gottschalk G.. 1986; Bacterial Metabolism New York: Springer-Verlag;
  13. Harris J. I., Hocking J. D., Runswick M. J., Suzuki K., Walker J. E.. 1980; d-Glyceraldehyde-3-phosphate dehydrogenase. The purification and characterisation of the enzyme from the thermophiles Bacillus stearothermophilus and Thermus aquaticus . Eur J Biochem108:535–547
    [Google Scholar]
  14. Hayward A. C.. 1993; The host of Xanthomonas . In Xanthomonas , pp51–54 Edited by Swings J. G., Civerolo E. L.. London: Chapman & Hall;
    [Google Scholar]
  15. Henderson R. F., Benson J. M., Hahn F. F., Hobbs C. H., Jones R. K., Mauderly J. L., McClellan R. O., Pickrell J. A.. 1985; New approaches for the evaluation of pulmonary toxicity: bronchoalveolar lavage fluid analysis. Fundam Appl Toxicol5:451–458
    [Google Scholar]
  16. Hsu C.-H., Lo Y.-M.. 2003; Characterization of xanthan gum biosynthesis in a centrifugal, packed-bed reactor using metabolic flux analysis. Process Biochem38:1617–1625
    [Google Scholar]
  17. Jarman T. R., Pace G. W.. 1984; Energy requirements for microbial exopolysaccharide synthesis. Arch Microbiol137:231–235
    [Google Scholar]
  18. Kennedy J. F., Bradshaw I. J.. 1984; Production, properties and applications of xanthan. Prog Ind Microbiol19:319–371
    [Google Scholar]
  19. Kimmich G. A., Randles J., Brand J. S.. 1975; Assay of picomole amounts of ATP, ADP, and AMP using the luciferase enzyme system. Anal Biochem69:187–206
    [Google Scholar]
  20. Koksharova O., Schubert M., Shestakov S., Cerff R.. 1998; Genetic and biochemical evidence for distinct key functions of two highly divergent GAPDH genes in catabolic and anabolic carbon flow of the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol36:183–194
    [Google Scholar]
  21. Kormanec J., Lempel'ová A., Nováková R., Rezuchová B., Homérová D.. 1997; Expression of the Streptomyces aureofaciens glyceraldehyde-3-phosphate dehydrogenase gene ( gap ) is developmentally regulated and induced by glucose. Microbiology143:3555–3561
    [Google Scholar]
  22. Lambeir A. M., Loiseau A. M., Kuntz D. A., Vellieux F. M., Michels P. A., Opperdoes F. R.. 1991; The cytosolic and glycosomal glyceraldehyde-3-phosphate dehydrogenase from Trypanosoma brucei . Kinetic properties and comparison with homologous enzymes. Eur J Biochem198:429–435
    [Google Scholar]
  23. Leong S. A., Ditta G. S., Helinski D. R.. 1982; Heme biosynthesis in Rhizobium : identification of a cloned gene coding for δ -aminolevulinic acid synthetase from Rhizobium meliloti . J Biol Chem257:8724–8730
    [Google Scholar]
  24. Letisse F., Chevallereau P., Simon J. L., Lindley N. D.. 2001; Kinetic analysis of growth and xanthan gum production with Xanthomonas campestris on sucrose, using sequentially consumed nitrogen sources. Appl Microbiol Biotechnol55:417–422
    [Google Scholar]
  25. Lu G.-T., Ma Z.-F., Hu J.-R., Tang D.-J., He Y.-Q., Feng J.-X., Tang J.-L.. 2007a; A novel locus involved in extracellular polysaccharide production and virulence of Xanthomonas campestris pathovar campestris . Microbiology153:737–746
    [Google Scholar]
  26. Lu G.-T., Yang Z.-J., Peng F.-Y., Tan Y.-N., Tang Y.-Q., Feng J.-X., Tang D.-J., He Y.-Q., Tang J.-L.. 2007b; The role of glucose kinase in carbohydrate utilization and extracellular polysaccharide production in Xanthomonas campestris pathovar campestris . Microbiology153:4284–4294
    [Google Scholar]
  27. Maurer K. H., Pfeiffer F., Zehender H., Mecke D.. 1983; Characterization of two glyceraldehyde-3-phosphate dehydrogenase isoenzymes from the pentalenolactone producer Streptomyces arenae . J Bacteriol153:930–936
    [Google Scholar]
  28. Miller J. H.. 1972; Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  29. Onsando J. M.. 1992; Black rot of crucifers. . In Plant Diseases of International Importance II: Diseases of Vegetable and Oil Seed Crops pp243–252 Edited by Chaube H. S., Kumar J., Mukhopadhyay A. N., Singh U. S. Englewood Cliffs, NJ: Prentice Hall;
  30. Pielken P., Schmiz K. L., Eggeling L., Sahm H.. 1988; Glucose metabolism in Xanthomonas campestris and influence of methionine on the carbon flow. Can J Microbiol34:1333–1337
    [Google Scholar]
  31. Qian W., Jia Y., Ren S.-X., He Y.-Q., Feng J.-X., Lu L.-F., Sun Q., Ying G., Tang D.-J.. other authors 2005; Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris . Genome Res15:757–767
    [Google Scholar]
  32. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  33. Schäfer A., Tauch A., Jäger W., Kalinowski J., Thierbach G., Pühler A.. 1994; Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum . Gene145:69–73
    [Google Scholar]
  34. Schneider D. A., Gourse R. L.. 2004; Relationship between growth rate and ATP concentration in Escherichia coli : a bioassay for available cellular ATP. J Biol Chem279:8262–8268
    [Google Scholar]
  35. Seta F. D., Boschi-Muller S., Vignails M. L., Branlant G.. 1997; Characterization of Esherichia coli strains with gapA and gapB genes deleted. J Bacteriol179:5218–5221
    [Google Scholar]
  36. Staskawicz B., Dahlbeck D., Keen N., Napoli C.. 1987; Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea . J Bacteriol169:5789–5794
    [Google Scholar]
  37. Suzuki K., Imahori K.. 1973; Glyceraldehyde 3-phosphate dehydrogenase of Bacillus stearothermophilus . Kinetics and physicochemical studies. J Biochem74:955–970
    [Google Scholar]
  38. Tang J.-L., Liu Y.-N., Barber C. E., Dow J. M., Wootton J. C., Daniels M. J.. 1991; Genetic and molecular analysis of a cluster of rpf genes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris. Mol Gen Genet226:409–417
    [Google Scholar]
  39. Tang D.-J., He Y.-Q., Feng J.-X., He B.-R., Jiang B.-L., Lu G.-T., Chen B., Tang J.-L.. 2005; Xanthomonas campestris pv. campestris possesses a single gluconeogenic pathway that is required for virulence. J Bacteriol187:6231–6237
    [Google Scholar]
  40. Tarze A., Deniaud A., Le Bras M., Maillier E., Molle D., Larochette N., Zamzami N., Jan G., Kroemer G., Brenner C.. 2007; GAPDH, a novel regulator of the pro-apoptotic mitochondrial membrane permeabilization. Oncogene26:2606–2620
    [Google Scholar]
  41. Tobisch S., Zuhlke D., Bernhardt J., Stulke J., Hecker M.. 1999; Role of CcpA in regulation of the central pathways of carbon catabolism in Bacillus subtilis . J Bacteriol181:6996–7004
    [Google Scholar]
  42. Turner P., Barber C., Daniels M. J.. 1984; Behavior of the transposons Tn 5 and Tn 7 in Xanthomonas campestris pv. campestris . Mol Gen Genet195:101–107
    [Google Scholar]
  43. Whitfield C., Sutherland I. W., Cripps R. E.. 1982; Glucose metabolism in Xanthomonas campestris . J Gen Microbiol128:981–985
    [Google Scholar]
  44. Windgassen M., Urban A., Jaeger K. E.. 2000; Rapid gene inactivation in Pseudomonas aeruginosa . FEMS Microbiol Lett193:201–205
    [Google Scholar]
  45. Yanisch-Perron C., Vieira J., Messing J.. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene33:103–119
    [Google Scholar]
  46. Yun M. H., Torres P. S., El Oirdi M., Rigano L. A., Gonzalez-Lamothe R., Marano M. R., Castagnaro A. P., Dankert M. A., Bouarab K., Vojnov A. A.. 2006; Xanthan induces plant susceptibility by suppressing callose deposition. Plant Physiol141:178–187
    [Google Scholar]
  47. Zheng L., Roeder R. G., Luo Y.. 2003; S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell114:255–266
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.023762-0
Loading
/content/journal/micro/10.1099/mic.0.023762-0
Loading

Data & Media loading...

Most cited this month 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