1887

Abstract

Formaldehyde is an intermediate formed during the metabolism of methanol or other methylated compounds. Many Gram-negative bacteria generate formaldehyde from methanol via a periplasmic pyrroloquinoline quinone (PQQ)-dependent dehydrogenase in which the subunit of an tetramer has catalytic activity. The genome of the facultative formaldehyde-oxidizing bacterium encodes XoxF, a homologue of the catalytic subunit of a proposed PQQ-containing dehydrogenase of . is part of a gene cluster that encodes periplasmic -type cytochromes, including CycI, isocytochrome and CycB (a cyt homologue), as well as , a glutathione-dependent formaldehyde dehydrogenase (GSH-FDH), and , a homologue of a glutathione–formaldehyde activating enzyme (Gfa). To test the roles of XoxF, CycB and Gfa in formaldehyde metabolism by , we monitored photosynthetic growth with methanol as a source of formaldehyde and whole-cell methanol-dependent oxygen uptake. Our data show that cells lacking XoxF or CycB do not exhibit methanol-dependent oxygen uptake and lack the capacity to utilize methanol as a sole photosynthetic carbon source. These results suggest that both proteins are required for formaldehyde metabolism. Gfa is not essential to activate formaldehyde, as cells lacking are capable of both methanol-dependent oxygen uptake and growth with methanol as a photosynthetic carbon source.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/011346-0
2008-01-01
2020-08-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/1/296.html?itemId=/content/journal/micro/10.1099/mic.0.2007/011346-0&mimeType=html&fmt=ahah

References

  1. Allen L. N., Hanson R. S.. 1985; Construction of broad-host-range cosmid cloning vectors: identification of genes necessary for growth of Methylobacterium organophilum on methanol. J Bacteriol161:955–962
    [Google Scholar]
  2. Anthony C.. 1982; The Biochemistry of Methylotrophs London: Academic Press;
  3. Anthony C.. 1992; The c type cytochromes of methylotrophic bacteria. Biochim Biophys Acta1099:1–15
    [Google Scholar]
  4. Anthony C., Williams P.. 2003; The structure and mechanism of methanol dehydrogenase. Biochim Biophys Acta1647:18–23
    [Google Scholar]
  5. Auerbach C., Moutschen-Dahmen M., Moutschen J.. 1977; Genetic and cytogenetical effects of formaldehyde and related compounds. Mutat Res39:317–361
    [Google Scholar]
  6. Barber R. D.. 1997; Formaldehyde sensing and metabolism in Rhodobacter sphaeroides PhD dissertation, University of Wisconsin-Madison;
  7. Barber R. D., Donohue T. J.. 1998; Pathways for transcriptional activation of a glutathione-dependent formaldehyde dehydrogenase gene. J Mol Biol280:775–784
    [Google Scholar]
  8. Barber R. D., Rott M. A., Donohue T. J.. 1996; Characterization of a glutathione-dependent formaldehyde dehydrogenase from Rhodobacter sphaeroides . J Bacteriol178:1386–1393
    [Google Scholar]
  9. Bethesda Laboratories Research 1986; BRL pUC host: E. coli DH5 α TM competent cells. Bethesda Res Lab Focus8:9–12
    [Google Scholar]
  10. Bockhorst J., Qiu Y., Glasner J., Liu M., Blattner F., Craven M.. 2003; Predicting bacterial transcription units using sequence and expression data. Bioinformatics19:i34–i43
    [Google Scholar]
  11. Bordo D., Bork P.. 2002; The rhodanese/Cdc25 phosphatase superfamily. Sequence–structure–function relations. EMBO Rep3:741–746
    [Google Scholar]
  12. Chen W. P., Kuo T. T.. 1993; A simple and rapid method for the preparation of Gram-negative bacterial genomic DNA. Nucleic Acids Res21:2260
    [Google Scholar]
  13. Chistoserdova L.. 1996; Metabolism of formaldehyde in M. extorquens AM1. In Microbial Growth on C1 Compounds pp16–24 Edited by Lidstrom M. E.. Tabita F. R.. Dordrecht: Kluwer Academic Publishers;
    [Google Scholar]
  14. Chistoserdova L., Lidstrom M. E.. 1997; Molecular and mutational analysis of a DNA region separating two methylotrophy gene clusters in Methylobacterium extorquens AM1. Microbiology143:1729–1736
    [Google Scholar]
  15. Cox R. L., Patterson C., Donohue T. J.. 2001; Roles for the Rhodobacter sphaeroides CcmA and CcmG proteins. J Bacteriol183:4643–4647
    [Google Scholar]
  16. Davis J., Donohue T. J., Kaplan S.. 1988; Construction, characterization, and complementation of a Puf mutant of Rhodobacter sphaeroides . J Bacteriol170:320–329
    [Google Scholar]
  17. Dennis J. J., Zylstra G. J.. 1998; Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of Gram-negative bacterial genomes. Appl Environ Microbiol64:2710–2715
    [Google Scholar]
  18. Ghosh M., Anthony C., Harlos K., Goodwin M. G., Blake C.. 1995; The refined structure of the quinoprotein methanol dehydrogenase from Methylobacterium extorquens at 1.94 A. Structure3:177–187
    [Google Scholar]
  19. Goenrich M., Bartoschek S., Hagemeier C. H., Griesinger C., Vorholt J. A.. 2002; A glutathione-dependent formaldehyde activating enzyme (Gfa) from Paracoccus denitrificans detected and purified via 2D proton exchange NMR spectroscopy. J Biol Chem277:3069–3072
    [Google Scholar]
  20. Goodwin P. M., Anthony C.. 1998; The biochemistry, physiology and genetics of PQQ and PQQ-containing enzymes. Adv Microb Physiol40:1–80
    [Google Scholar]
  21. Harms N., van Spanning R. J.. 1991; C1 metabolism in Paracoccus denitrificans : genetics of Paracoccus denitrificans . J Bioenerg Biomembr23:187–210
    [Google Scholar]
  22. Harms N., Ras J., Koning S., Reijnders W. N. M., Stouthamer A. H., van Spanning R. J. M.. 1996; Genetics of C1 metabolism regulation in Paracoccus denitrificans . In Microbial Growth on C1 Compounds pp126–132 Edited by Lidstrom M. E., Tabita F. R. Dordrecht: Kluwer Academic Publishers;
    [Google Scholar]
  23. Hickman J.. 2003; Physiology and regulation of glutathione-dependent formaldehyde metabolism PhD dissertation, University of Wisconsin-Madison;
  24. Hickman J. W., Barber R. D., Skaar E. P., Donohue T. J.. 2002; Link between the membrane-bound pyridine nucleotide transhydrogenase and glutathione-dependent processes in Rhodobacter sphaeroides . J Bacteriol184:400–409
    [Google Scholar]
  25. Hickman J. W., Witthuhn V. C. Jr, Dominguez M., Donohue T. J.. 2004; Positive and negative transcriptional regulators of glutathione-dependent formaldehyde metabolism. J Bacteriol186:7914–7925
    [Google Scholar]
  26. Kumar S., Tamura K., Nei M.. 2004; mega3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform5:150–163
    [Google Scholar]
  27. Levy H.. 1971; Normal atmosphere: large radical and formaldehyde concentrations predicted. Science173:141–143
    [Google Scholar]
  28. Long A. R., Anthony C.. 1991; Characterization of the periplasmic cytochromes c of Paracoccus denitrificans : identification of the electron acceptor for methanol dehydrogenase, and description of a novel cytochrome c heterodimer. J Gen Microbiol137:415–425
    [Google Scholar]
  29. Mackenzie C., Choudhary M., Larimer F. W., Predki P. F., Stilwagen S., Armitage J. P., Barber R. D., Donohue T. J., Hosler J. P.. other authors 2001; The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1. Photosynth Res70:19–41
    [Google Scholar]
  30. Messing J.. 1979; A multipurpose cloning system based on the single-standed DNA bacteriophage, M13. Recomb DNA Tech Bull2:43–48
    [Google Scholar]
  31. Mouncey N. J., Gak E., Choudhary M., Oh J., Kaplan S.. 2000; Respiratory pathways of Rhodobacter sphaeroides 2.4.1T: identification and characterization of genes encoding quinol oxidases. FEMS Microbiol Lett192:205–210
    [Google Scholar]
  32. Neculai A. M., Neculai D., Griesinger C., Vorholt J. A., Becker S.. 2005; A dynamic zinc redox switch. J Biol Chem280:2826–2830
    [Google Scholar]
  33. Ozcan S.. 1996; Pyrroloquinoline quinone (PQQ) synthesis is required for butanol metabolism MS thesis, University of Wisconsin-La Crosse;
  34. Price M. N., Huang K. H., Alm E. J., Arkin A. P.. 2005; A novel method for accurate operon predictions in all sequenced prokaryotes. Nucleic Acids Res33:880–892
    [Google Scholar]
  35. Quayle J. R., Pfennig N.. 1975; Utilization of methanol by Rhodospirillaceae . Arch Microbiol102:193–198
    [Google Scholar]
  36. Ras J., Reijnders W. N., van Spanning R. J., Harms N., Oltmann L. F., Stouthamer A. H.. 1991; Isolation, sequencing, and mutagenesis of the gene encoding cytochrome c 553i of Paracoccus denitrificans and characterization of the mutant strain. J Bacteriol173:6971–6979
    [Google Scholar]
  37. Rott M. A., Fitch J., Meyer T. E., Donohue T. J.. 1992; Regulation of a cytochrome c 2 isoform in wild-type and cytochrome c 2 mutant strains of Rhodobacter sphaeroides . Arch Biochem Biophys292:576–582
    [Google Scholar]
  38. Rott M. A., Witthuhn V. C., Schilke B. A., Soranno M., Ali A., Donohue T. J.. 1993; Genetic evidence for the role of isocytochrome c 2 in photosynthetic growth of Rhodobacter sphaeroides Spd mutants. J Bacteriol175:358–366
    [Google Scholar]
  39. Sahm H., Cox R. B., Quayle J. R.. 1976; Metabolism of methanol by Rhodopseudomonas acidophila . J Gen Microbiol94:313–322
    [Google Scholar]
  40. Saier M. H. Jr. 1994; Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, and evolution. Microbiol Rev58:71–93
    [Google Scholar]
  41. Saier M. H. Jr. 2000; A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol Mol Biol Rev64:354–411
    [Google Scholar]
  42. Simon R., Priefer U., Pühler A.. 1983; A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Bio/Technology1:784–791
    [Google Scholar]
  43. Sistrom W. R.. 1960; A requirement for sodium in the growth of Rhodopseudomonas sphaeroides . J Gen Microbiol22:778–785
    [Google Scholar]
  44. Spallarossa A., Forlani F., Pagani S., Salvati L., Visca P., Ascenzi P., Bolognesi M., Bordo D.. 2003; Inhibition of Azotobacter vinelandii rhodanese by NO-donors. Biochem Biophys Res Commun306:1002–1007
    [Google Scholar]
  45. Spallarossa A., Forlani F., Carpen A., Armirotti A., Pagani S., Bolognesi M., Bordo D.. 2004; The “rhodanese” fold and catalytic mechanism of 3-mercaptopyruvate sulfurtransferases: crystal structure of SseA from Escherichia coli . J Mol Biol335:583–593
    [Google Scholar]
  46. Vorholt J. A., Marx C. J., Lidstrom M. E., Thauer R. K.. 2000; Novel formaldehyde-activating enzyme in Methylobacterium extorquens AM1 required for growth on methanol. J Bacteriol182:6645–6650
    [Google Scholar]
  47. Zannoni D., Melandri B. A., Baccarini-Melandri A.. 1976; Energy transduction in photosynthetic bacteria. X. Composition and function of the branched oxidase system in wild type and respiration deficient mutants of Rhodopseudomonas capsulata . Biochim Biophys Acta423:413–430
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/011346-0
Loading
/content/journal/micro/10.1099/mic.0.2007/011346-0
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