1887

Abstract

The Calvin–Benson–Bassham (CBB) cycle has been extensively studied in proteobacteria, cyanobacteria, algae and plants, but hardly at all in Gram-positive bacteria. Some characteristics of ribulose bisphosphate carboxylase/oxygenase (RuBisCO) and a cluster of potential CBB cycle genes in a Gram-positive bacterium are described in this study with two species of (Gram-positive, facultatively autotrophic, mineral sulfide-oxidizing acidophiles). In contrast to the Gram-negative, iron-oxidizing acidophile , grew poorly autotrophically unless the CO concentration was enhanced over that in air. However, the RuBisCO of each organism showed similar affinities for CO and for ribulose 1,5-bisphosphate, and similar apparent derepression of activity under CO limitation. The red-type, form I RuBisCO of was confirmed as closely related to that of the anoxygenic phototroph . Eight genes potentially involved in the CBB cycle in were clustered in the order , , , , , , and .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/006262-0
2007-07-01
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/7/2231.html?itemId=/content/journal/micro/10.1099/mic.0.2007/006262-0&mimeType=html&fmt=ahah

References

  1. Ashida, H., Danchin, A. & Yokota, A. ( 2005; ). Was photosynthetic RuBisCO recruited by acquisitive evolution from RuBisCO-like proteins involved in sulfur metabolism?. Res Microbiol 156, 611–618.[CrossRef]
    [Google Scholar]
  2. Beudeker, R. F., Cannon, G. C., Kuenen, J. G. & Shively, J. M. ( 1980; ). Relations between d-ribulose-1,5-bisphosphate carboxylase, carboxysomes and CO2 fixing capacity in the obligate chemolithotroph Thiobacillus neapolitanus grown under different limitations in the chemostat. Arch Microbiol 124, 185–189.
    [Google Scholar]
  3. Bowien, B. ( 1977; ). RuBisCO from Paracoccus denitrificans. FEMS Microbiol Lett 2, 263–266.[CrossRef]
    [Google Scholar]
  4. Bowien, B. & Kusian, B. ( 2002; ). Genetics and control of CO2 assimilation in the chemoautotroph Ralstonia eutropha. Arch Microbiol 178, 85–93.[CrossRef]
    [Google Scholar]
  5. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T. J., Higgins, D. G. & Thompson, J. D. ( 2003; ). Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res 31, 3497–3500.[CrossRef]
    [Google Scholar]
  6. Clark, D. A. ( 1995; ). The study of acidophilic, moderately thermophilic iron-oxidizing bacteria. PhD Thesis, University of Warwick.
  7. Clark, D. A. & Norris, P. R. ( 1996; ). Acidimicrobium ferrooxidans gen. nov., sp. nov.: mixed culture ferrous iron oxidation with Sulfobacillus species. Microbiology 142, 785–790.[CrossRef]
    [Google Scholar]
  8. Cook, C. M., Lanaras, T., Wood, A. P., Codd, G. A. & Kelly, D. P. ( 1991; ). Kinetic properties of ribulose bisphosphate carboxylase/oxygenase from Thiobacillus thyasiris, the putative symbiont of Thyasira flexuosa (Montagu), a bivalve mussel. J Gen Microbiol 137, 1491–1496.[CrossRef]
    [Google Scholar]
  9. Delwiche, C. F. & Palmer, J. D. ( 1996; ). Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol Biol Evol 13, 873–882.[CrossRef]
    [Google Scholar]
  10. Dew, D. W., van Buuren, C., McEwan, K. & Bowker, C. ( 1999; ). Bioleaching of base metal sulphide concentrates: a comparison of mesophile and thermophile bacterial cultures. In Biohydrometallurgy and the Environment toward the Mining of the 21st Century, part A, pp. 229–238. Edited by R. Amils & A. Ballester. Amsterdam: Elsevier.
  11. Dubbs, J. M. & Tabita, F. R. ( 2004; ). Regulators of nonsulfur purple phototrophic bacteria and the interactive control of CO2 assimilation, nitrogen fixation, hydrogen metabolism and energy metabolism. FEMS Microbiol Rev 28, 353–376.[CrossRef]
    [Google Scholar]
  12. Felsenstein, J. ( 2002; ). phylip (Phylogeny Inference Package), version 3.6a3. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, USA.
  13. Figge, R. M., Schubert, M., Brinkmann, H. & Cerff, R. ( 1999; ). Glyceraldehyde-3-phosphate dehydrogenase gene diversity in eubacteria and eukaryotes: evidence for intra- and inter-kingdom gene transfer. Mol Biol Evol 16, 429–440.[CrossRef]
    [Google Scholar]
  14. Gibson, J. L. & Tabita, F. R. ( 1977; ). Different molecular forms of RuBisCO from Rhodobacter sphaeroides. J Biol Chem 252, 943–949.
    [Google Scholar]
  15. Gibson, J. L. & Tabita, F. R. ( 1996; ). The molecular regulation of the reductive pentose phosphate pathway in Proteobacteria and Cyanobacteria. Arch Microbiol 166, 141–150.[CrossRef]
    [Google Scholar]
  16. Gibson, J. L. & Tabita, F. R. ( 1997; ). Analysis of the cbbXYZ operon in Rhodobacter sphaeroides. J Bacteriol 179, 663–669.
    [Google Scholar]
  17. Hansen, S., Vollan, V. B., Hough, E. & Andersen, K. ( 1999; ). The crystal structure of rubisco from Alcaligenes eutrophus reveals a novel central eight-stranded β-barrel formed by β-strands from four subunits. J Mol Biol 288, 609–621.[CrossRef]
    [Google Scholar]
  18. Hanson, T. E. & Tabita, F. R. ( 2001; ). A ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc Natl Acad Sci U S A 98, 4397–4402.[CrossRef]
    [Google Scholar]
  19. Harrison, D. H. T., Runquist, J. A., Holub, A. & Miziorko, H. M. ( 1998; ). The crystal structure of phosphoribulokinase from Rhodobacter sphaeroides reveals a fold similar to that of adenylate kinase. Biochemistry 37, 5074–5085.[CrossRef]
    [Google Scholar]
  20. Holden, P. J. & Brown, R. W. ( 1993; ). Amplification of ribulose bisphosphate carboxylase/oxygenase large subunit (RuBisCO LSU) gene fragments from Thiobacillus ferrooxidans and a moderate thermophile using polymerase chain reaction. FEMS Microbiol Rev 11, 19–30.[CrossRef]
    [Google Scholar]
  21. Holuigue, L., Herrera, L., Phillips, O. M., Young, M. & Allende, J. E. ( 1987; ). CO2 fixation by mineral-leaching bacteria: characteristics of the ribulose bisphosphate carboxylase-oxygenase of Thiobacillus ferrooxidans. Biotechnol Appl Biochem 9, 497–505.[CrossRef]
    [Google Scholar]
  22. Horken, K. M. & Tabita, F. R. ( 1999; ). Closely related form I ribulose bisphosphate carboxylase/oxygenase molecules that possess different CO2/O2 substrate specificities. Arch Biochem Biophys 361, 183–194.[CrossRef]
    [Google Scholar]
  23. Jordan, D. B. & Ogren, W. L. ( 1981; ). Species variation in the specificity of ribulose-bisphosphate carboxylase-oxygenase. Nature 291, 513–515.[CrossRef]
    [Google Scholar]
  24. Kusian, B. & Bowien, B. ( 1997; ). Organization and regulation of cbb CO2 assimilation genes in autotrophic bacteria. FEMS Microbiol Rev 21, 135–155.[CrossRef]
    [Google Scholar]
  25. Maier, U.-G., Fraunholz, M., Zauner, S., Penny, S. & Douglas, S. ( 2000; ). A nucleomorph-encoded CbbX and the phylogeny of RuBisCo regulators. Mol Biol Evol 17, 576–583.[CrossRef]
    [Google Scholar]
  26. Martin, W. & Schnarrenberger, C. ( 1997; ). The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr Genet 32, 1–18.[CrossRef]
    [Google Scholar]
  27. Miller, P. C. ( 1997; ). The design and operating practice of bacterial oxidation plant using moderate thermophiles (the Bactech process). In Biomining, pp. 81–102. Edited by D. E. Rawlings. Berlin: Springer.
  28. Miziorko, H. M. ( 1998; ). Phosphoribulokinase: current perspectives on the structure/function basis for regulation and catalysis. In Advances in Enzymology and Related Areas of Molecular Biology, vol. 74, Mechanisms of Enzyme Action, part B, pp. 95–127. Edited by D. L. Purich. New York: Wiley.
  29. Norris, P. R., Clark, D. A., Owen, J. P. & Waterhouse, S. ( 1996; ). Characteristics of Sulfobacillus acidophilus sp. nov. and other moderately thermophilic mineral-sulphide-oxidizing bacteria. Microbiology 142, 775–783.[CrossRef]
    [Google Scholar]
  30. Ochman, H., Ayala, F. J. & Hartl, D. L. ( 1993; ). Use of polymerase chain reaction to amplify segments outside boundaries of known sequences. Methods Enzymol 218, 309–321.
    [Google Scholar]
  31. Pierce, J. W., McCurry, S. D., Mulligan, R. M. & Tolbert, N. E. ( 1982; ). Activation and assay of RuBisCO. Methods Enzymol 89, 47–55.
    [Google Scholar]
  32. Plaumann, M., Pelzer-Reith, B., Martin, W. F. & Schnarrenberger, C. ( 1997; ). Multiple recruitment of class-I aldolase to chloroplasts and eubacterial origin of eukaryotic class-II aldolases revealed by cDNAs from Euglena gracilis. Curr Genet 31, 430–438.[CrossRef]
    [Google Scholar]
  33. Runquist, J. A. & Miziorko, H. M. ( 2006; ). Functional contribution of a conserved, mobile loop histidine of phosphoribulokinase. Protein Sci 15, 837–842.[CrossRef]
    [Google Scholar]
  34. Schenk, G., Layfield, R., Candy, J. M., Duggleby, R. G. & Nixon, P. F. ( 1997; ). Molecular evolutionary analysis of the thiamine-diphosphate-dependent enzyme, transketolase. J Mol Evol 44, 552–572.[CrossRef]
    [Google Scholar]
  35. Shively, J. M., van Keulen, G. & Meijer, W. G. ( 1998; ). Something from almost nothing: carbon dioxide fixation in chemoautotrophs. Annu Rev Microbiol 52, 191–230.[CrossRef]
    [Google Scholar]
  36. Smith, A. L., Kelly, D. P. & Wood, A. P. ( 1980; ). Metabolism of Thiobacillus A2 grown under autotrophic, mixotrophic and heterotrophic conditions in chemostat culture. J Gen Microbiol 121, 127–138.
    [Google Scholar]
  37. Spreitzer, R. J. ( 2003; ). Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase. Arch Biochem Biophys 414, 141–149.[CrossRef]
    [Google Scholar]
  38. Sprenger, G. A. ( 1995; ). Genetics of pentose-phosphate pathway enzymes of Escherichia coli K-12. Arch Microbiol 164, 324–330.[CrossRef]
    [Google Scholar]
  39. Sugawara, H., Yamamoto, H., Shibata, N., Inoue, T., Okada, S., Miyake, C., Yokota, A. & Kai, Y. ( 1999; ). Crystal structure of carboxylase reaction-oriented ribulose 1,5-bisphosphate carboxylase oxygenase from a thermophilic red alga, Galdieria partita. J Biol Chem 274, 15655–15661.[CrossRef]
    [Google Scholar]
  40. Tourova, T. P., Spiridonova, E. M., Slobodova, N. V., Boulygina, E. S., Keppen, O. I., Kuznetsov, B. B. & Ivanovsky, R. N. ( 2006; ). Phylogeny of anoxygenic filamentous phototrophic bacteria of the family Oscillochloridaceae as inferred from comparative analyses of the rrs, cbbL, and nifH genes. Microbiology (English translation of Mikrobiologiya) 75, 192–200.[CrossRef]
    [Google Scholar]
  41. van den Bergh, E. R. E., Baker, S. C., Raggers, R. J., Terpstra, P., Woudstra, E. C., Dijkhuizen, L. & Meijer, W. G. ( 1996; ). Primary structure and phylogeny of the Calvin Cycle enzymes transketolase and fructosebisphosphate aldolase of Xanthobacter flavus. J Bacteriol 178, 888–893.
    [Google Scholar]
  42. Watson, G. M. F. & Tabita, F. R. ( 1997; ). Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a molecule for phylogenetic and enzymological investigation. FEMS Microbiol Lett 146, 13–22.[CrossRef]
    [Google Scholar]
  43. Wood, A. P. & Kelly, D. P. ( 1984; ). Autotrophic and mixotrophic growth and metabolism of some moderately thermoacidophilic iron-oxidizing bacteria. In Planetary Ecology, pp. 251–262. Edited by D. E. Caldwell, J. A. Brierley & C. L. Brierley. New York: Van Nostrand Reinhold.
  44. Yeoh, H.-H., Badger, M. R. & Watson, L. ( 1981; ). Variations in kinetic properties of RuBisCO among plants. Plant Physiol 67, 1151–1155.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/006262-0
Loading
/content/journal/micro/10.1099/mic.0.2007/006262-0
Loading

Data & Media loading...

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