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Volume 150, Issue 6

The transcription of the operon in Free

Abstract

is an aerobic ammonia-oxidizing bacterium that participates in the C and N cycles. utilizes CO as its predominant carbon source, and is an obligate chemolithotroph, deriving all the reductant required for energy and biosynthesis from the oxidation of ammonia (NH) to nitrite (). This bacterium fixes carbon via the Calvin–Benson–Bassham (CBB) cycle via a type I ribulose bisphosphate carboxylase/oxygenase (RubisCO). The RubisCO operon is composed of five genes, . This gene organization is similar to that of the operon for ‘green-like’ type I RubisCOs in other organisms. The gene encoding the putative regulatory protein for RubisCO transcription was identified upstream of . This study showed that transcription of genes was upregulated when the carbon source was limited, while , and other energy-harvesting-related genes were downregulated. responds to carbon limitation by prioritizing resources towards key components for carbon assimilation. Unlike the situation for genes, NH was not required for the transcription of the genes. All five genes were only transcribed when an external energy source was provided. In actively growing cells, mRNAs from the five genes in the RubisCO operon were present at different levels, probably due to premature termination of transcription, rapid mRNA processing and mRNA degradation.

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  • Accepted:
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  • Published Online:
Keyword(s): AMO, ammonia monooxygenase , HAO, hydroxylamine oxidoreductase , PRK, phosphoribulokinase and RubisCO, ribulose bisphosphate carboxylase/oxygenase
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2004-06-01
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References

  1. Arp D. J., Sayavedra-Soto L. A., Hommes N. G. 2002; Molecular biology and biochemistry of ammonia oxidation by Nitrosomonas europaea. Arch Microbiol 178:250–255 [CrossRef]
     [Google Scholar]
  2. Baxter N. J., Hirt R. P., Bodrossy L., Kovacs K. L., Embley T. M., Prosser J. I., Murrell J. C. 2002; The ribulose-1,5-bisphosphate carboxylase/oxygenase gene cluster of Methylococcus capsulatus (Bath). Arch Microbiol 177:279–289 [CrossRef]
     [Google Scholar]
  3. Beudeker R. F., Cannon D. C., Kuenen J. G., Shively J. M. 1980; Relations between d-ribulose-1,5-bisphosphate carboxylase, carboxysomes and CO2 fixing capacity in the obligate chemolithoautotroph Thiobacillus neapolitanus grown under different limitations in the chemostat. Arch Microbiol 124:185–189
     [Google Scholar]
  4. Bock E., Koops H.-P., Harms H. 1986; Cell biology of nitrifying bacteria. In Nitrification pp. 17–38Edited by Prosser J. I. Oxford: IRL Press;
     [Google Scholar]
  5. Bock E., Koops H. P., Harms H., Ahlers B. 1991; The biochemistry of nitrifying organisms. In Variations in Autotrophic Life pp. 171–200Edited by Shively J. M., Barton L. L. San Diego, CA: Academic Press;
     [Google Scholar]
  6. Calin-Jageman I., Nicholson A. W. 2003; RNA structure-dependent uncoupling of substrate recognition and cleavage by Escherichia coli ribonuclease III. Nucleic Acids Res 31:2381–2392 [CrossRef]
     [Google Scholar]
  7. Chain P., Lamerdin J., Larimer F.12 other authors 2003; Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol 185:2759–2773 [CrossRef]
     [Google Scholar]
  8. Clark C., Schmidt E. L. 1966; Effect of mixed culture on Nitrosomonas europaea simulated by uptake and utilization of pyruvate. J Bacteriol 91:367–373
     [Google Scholar]
  9. Clark C., Schmidt E. L. 1967; Uptake and utilization of amino acids by resting cells of Nitrosomonas europaea. J Bacteriol 91:1309–1315
     [Google Scholar]
  10. Dijkhuizen L., Harder W. 1979; Regulation of autotrophic and heterotrophic metabolism in Pseudomonas oxalaticus OX1. Growth on mixtures of acetate and formate in continuous culture. Arch Microbiol 123:47–53 [CrossRef]
     [Google Scholar]
  11. Ehretsmann C. P., Carpousis A. J., Krisch H. M. 1992; Specificity of Escherichia coli endoribonuclease RNase E: in vivo and in vitro analysis of mutants in a bacteriophage T4 mRNA processing site. Genes Dev 6:149–159 [CrossRef]
     [Google Scholar]
  12. English R. S., Williams C. A., Lorbach S. C., Shively J. M. 1992; Two forms of ribulose-1,5-bisphosphate carboxylase/oxygenase from Thiobacillus denitrificans. FEMS Microbiol Lett 73:111–119
     [Google Scholar]
  13. Ensign S. A., Hyman M. R., Arp D. J. 1993; In vitro activation of ammonia monooxygenase from Nitrosomonas europaea by copper. J Bacteriol 175:1971–1980
     [Google Scholar]
  14. Friedrich C. G. 1982; Depression of hydrogenase during limitation of electron donors and derepression of ribulosebisphosphate carboxylase during carbon limitation of Alcaligenes eutrophus. J Bacteriol 149:203–210
     [Google Scholar]
  15. Gibson J. L., Tabita F. R. 1997; Analysis of the cbbXYZ operon in Rhodobacter sphaeroides. J Bacteriol 179:663–669
     [Google Scholar]
  16. Goethals K., Van Montagu M., Holsters M. 1992; Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 reveal a common structure in promoters regulated by LysR-type proteins. Proc Natl Acad Sci U S A 89:1646–1650 [CrossRef]
     [Google Scholar]
  17. Gornall A. G., Bardawill C. J., David M. M. 1949; Determination of serum proteins by means of the Biuret reaction. J Biol Chem 177:751–766
     [Google Scholar]
  18. Grunberg-Manago M. 1999; Messenger RNA stability and its role in control of gene expression in bacteria and phages. Annu Rev Genet 33:193–227 [CrossRef]
     [Google Scholar]
  19. Hageman R. H., Hucklesby D. P. 1971; Nitrate reductase in higher plants. Methods Enzymol 23:491–503
     [Google Scholar]
  20. Hayashi N. R., Igarashi Y. 2002; ATP binding and hydrolysis and autophosphorylation of CbbQ encoded by the gene located downstream of RubisCO genes. Biochem Biophys Res Commun 290:1434–1440 [CrossRef]
     [Google Scholar]
  21. Hayashi N. R., Arai H., Kodama T., Igarashi Y. 1997; The novel genes, cbbQ and cbbO, located downstream from the RubisCO genes of Pseudomonas hydrogenothermophila, affect the conformational states and activity of RubisCO. Biochem Biophys Res Commun 241:565–569 [CrossRef]
     [Google Scholar]
  22. Hayashi N. R., Arai H., Kodama T., Igarashi Y. 1999; The cbbQ genes, located downstream of the form I and form II RubisCO genes, affect the activity of both RubisCOs. Biochem Biophys Res Commun 265:177–183 [CrossRef]
     [Google Scholar]
  23. Hayashi N. R., Terazono K., Kodama T., Igarashi Y. 2000; Structure of ribulose 1,5-bisphosphate carboxylase/oxygenase gene cluster from a thermophilic hydrogen-oxidizing bacterium, Hydrogenophilus thermoluteolus, and phylogeny of the fructose 1,6-bisphosphate aldolase encoded by cbbA in the cluster. Biosci Biotechnol Biochem 64:61–71 [CrossRef]
     [Google Scholar]
  24. Heinhorst S., Baker S. H., Johnson D. R., Davies P. S., Cannon G. C., Shively J. M. 2002; Two copies of form I RuBisCO genes in Acidithiobacillus ferrooxidans ATCC 23270. Curr Microbiol 45:115–117 [CrossRef]
     [Google Scholar]
  25. Hernandez J. M., Baker S. H., Lorbach S. C., Shively J. M., Tabita F. R. 1996; Deduced amino acid sequence, functional expression, and unique enzymatic properties of the form I and form II ribulose bisphosphate carboxylase/oxygenase from the chemoautotrophic bacterium Thiobacillus denitrificans. J Bacteriol 178:347–356
     [Google Scholar]
  26. Hirota R., Kato J., Morita H., Kuroda A., Ikeda T., Takiguchi N., Ohtake H. 2002; Isolation and characterization of cbbL and cbbS genes encoding form I ribulose-1,5-bisphosphate carboxylase/oxygenase large and small subunits in Nitrosomonas sp. strain ENI-11. Biosci Biotechnol Biochem 66:632–635 [CrossRef]
     [Google Scholar]
  27. Hommes N. G., Sayavedra-Soto L. A., Arp D. J. 1996; Mutagenesis of hydroxylamine oxidoreductase in Nitrosomonas europaea by transformation and recombination. J Bacteriol 178:3710–3714
     [Google Scholar]
  28. Hommes N. G., Sayavedra-Soto L. A., Arp D. J. 1998; Mutagenesis and expression of amo, which codes for ammonia monooxygenase in Nitrosomonas europaea. J Bacteriol 180:3353–3359
     [Google Scholar]
  29. Hommes N. G., Sayavedra-Soto L. A., Arp D. J. 2001; Transcript analysis of multiple copies of amo(encoding ammonia monooxygenase) and hao (encoding hydroxylamine oxidoreductase) in Nitrosomonas europaea. J Bacteriol 183:1096–1100 [CrossRef]
     [Google Scholar]
  30. Hommes N. G., Sayavedra-Soto L. A., Arp D. J. 2002; The roles of the three gene copies encoding hydroxylamine oxidoreductase in Nitrosomonas europaea. Arch Microbiol 178:471–476 [CrossRef]
     [Google Scholar]
  31. Hommes N. G., Sayavedra-Soto L. A., Arp D. J. 2003; Chemolithoorganotrophic growth of Nitrosomonas europaea on fructose. J Bacteriol 185:6809–6814 [CrossRef]
     [Google Scholar]
  32. Hyman M. R., Arp D. J. 1993; An electrophoretic study of the thermal-dependent and reductant-dependent aggregation of the 27 kDa component of ammonia monooxygenase from Nitrosomonas europaea. Electrophoresis 14:619–627 [CrossRef]
     [Google Scholar]
  33. Hyman M. R., Arp D. J. 1995; Effects of ammonia on the de novo synthesis of polypeptides in cells of Nitrosomonas europaea denied ammonia as an energy source. J Bacteriol 177:4974–4979
     [Google Scholar]
  34. Klotz M. G., Norton J. M. 1995; Sequence of an ammonia monooxygenase subunit A-encoding gene from Nitrosospira sp. NpAV. Gene 163:159–160 [CrossRef]
     [Google Scholar]
  35. Klotz M. G., Norton J. M. 1998; Multiple copies of ammonia monooxygenase (amo) operons have evolved under biased AT/GC mutational pressure in ammonia-oxidizing autotrophic bacteria. FEMS Microbiol Lett 168:303–311 [CrossRef]
     [Google Scholar]
  36. Kusano T., Sugawara K. 1993; Specific binding of Thiobacillus ferrooxidans RbcR to the intergenic sequence between the rbc operon and the rbcR gene. J Bacteriol 175:1019–1025
     [Google Scholar]
  37. Kusano T., Takeshima T., Inoue C., Sugawara K. 1991; Evidence for two sets of structural genes coding for ribulose bisphosphate carboxylase in Thiobacillus ferrooxidans. J Bacteriol 173:7313–7323
     [Google Scholar]
  38. Kusian B., Bowien B. 1995; Operator binding of the CbbR protein, which activates the duplicate cbb CO2 assimilation operons of Alcaligenes eutrophus. J Bacteriol 177:6568–6574
     [Google Scholar]
  39. Kusian B., Bednarski R., Husemann M., Bowien B. 1995; Characterization of the duplicate ribulose-1,5-bisphosphate carboxylase genes and cbb promoters of Alcaligenes eutrophus. J Bacteriol 177:4442–4450
     [Google Scholar]
  40. Kusian B., Sultemeyer D., Bowien B. 2002; Carbonic anhydrase is essential for growth of Ralstonia eutropha at ambient CO2 concentrations. J Bacteriol 184:5018–5026 [CrossRef]
     [Google Scholar]
  41. Lee S. N., Kim Y. M. 1998; Cloning and characterization of ribulose bisphosphate carboxylase gene of a carboxydobacterium, Hydrogenophagea pseudoflava DSM 1084. Mol Cells 8:524–529
     [Google Scholar]
  42. Martiny H., Koops H.-P. 1982; Incorporation of organic compounds into cell protein by lithotrophic, ammonia-oxidizing bacteria. Antonie van Leeuwenhoek 48:327–336 [CrossRef]
     [Google Scholar]
  43. Meijer W. G., Arnberg A. C., Enequist H. G., Terpstra P., Lidstrom M. E., Dijkhuizen L. 1991; Identification and organization of carbon dioxide fixation genes in Xanthobacter flavus H4-14. Mol Gen Genet 225:320–330 [CrossRef]
     [Google Scholar]
  44. Norton J. M., Low J. M., Klotz M. G. 1996; The gene encoding ammonia monooxygenase subunit A exists in three nearly identical copies in Nitrosospira sp. NpAV. FEMS Microbiol Lett 139:181–188 [CrossRef]
     [Google Scholar]
  45. Onizuka T., Akiyama H., Endo S., Kanai S., Hirano M., Tanaka S., Miyasaka H. 2002; CO2 response element and corresponding trans-acting factor of the promoter for ribulose-1,5-bisphosphate carboxylase/oxygenase genes in Synechococcus sp. PCC7002 found by an improved electrophoretic mobility shift assay. Plant Cell Physiol 43:660–667 [CrossRef]
     [Google Scholar]
  46. Otsuka Y., Ueno H., Yonesaki T. 2003; Escherichia coli endoribonucleases involved in cleavage of bacteriophage T4 mRNAs. J Bacteriol 185:983–990 [CrossRef]
     [Google Scholar]
  47. Paoli G. C., Soyer F., Shively J., Tabita F. R. 1998; Rhodobacter capsulatus genes encoding form I ribulose-1,5-bisphosphate carboxylase/oxygenase (cbbLS) and neighbouring genes were acquired by a horizontal gene transfer. Microbiology 144:219–227 [CrossRef]
     [Google Scholar]
  48. Pulgar V., Gaete L., Allende J., Orellana O., Jordana X., Jedlicki E. 1991; Isolation and nucleotide sequence of the Thiobacillus ferrooxidans genes for the small and large subunits of ribulose 1,5-bisphosphate carboxylase/oxygenase. FEBS Lett 292:85–89 [CrossRef]
     [Google Scholar]
  49. Reddy K., Gilman M. 1993; Preparation of bacterial RNA. In Current Protocols in Molecular Biology pp 4.41–44.44.47 Edited by Ausubel F. M. and others New York: Wiley;
     [Google Scholar]
  50. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  51. Sayavedra-Soto L. A., Hommes N. G., Russell S. A., Arp D. J. 1996; Induction of ammonia monooxygenase and hydroxylamine oxidoreductase mRNAs by ammonium in Nitrosomonas europaea. Mol Microbiol 20:541–548 [CrossRef]
     [Google Scholar]
  52. Sayavedra-Soto L. A., Hommes N. G., Alzerreca J. J., Arp D. J., Norton J. M., Klotz M. G. 1998; Transcription of the amoC, amoA, and amoB genes in Nitrosomonas europaea and Nitrosospira sp. NpAV. FEMS Microbiol Lett 167:81–88 [CrossRef]
     [Google Scholar]
  53. Schäferjohann J., Yoo J. G., Bowien B. 1995; Analysis of the genes forming the distal parts of the two cbb CO2 fixation operons from Alcaligenes eutrophus. Arch Microbiol 163:291–299 [CrossRef]
     [Google Scholar]
  54. Schäferjohann J., Bednarski R., Bowien B. 1996; Regulation of CO2 assimilation in Ralstonia eutropha: premature transcription termination within the cbb operon. J Bacteriol 178:6714–6719
     [Google Scholar]
  55. Schell M. A. 1993; Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47:597–626 [CrossRef]
     [Google Scholar]
  56. Shibata M., Ohkawa H., Kaneko T., Fukuzawa H., Tabata S., Kaplan A., Ogawa T. 2001; Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci U S A 98:11789–11794 [CrossRef]
     [Google Scholar]
  57. 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]
  58. Stein L. Y., Arp D. J. 1998; Loss of ammonia monooxygenase activity in Nitrosomonas europaea upon exposure to nitrite. Appl Environ Microbiol 64:4098–4102
     [Google Scholar]
  59. Stein L. Y., Sayavedra-Soto L. A., Hommes N. G., Arp D. J. 2000; Differential regulation of amoA and amoB gene copies in Nitrosomonas europaea. FEMS Microbiol Lett 192:163–168 [CrossRef]
     [Google Scholar]
  60. Terazono K., Hayashi N. R., Igarashi Y. 2001; CbbR, a LysR-type transcriptional regulator from Hydrogenophilus thermoluteolus, binds two cbb promoter regions. FEMS Microbiol Lett 198:151–157 [CrossRef]
     [Google Scholar]
  61. Tichi M. A., Tabita F. R. 2002; Metabolic signals that lead to control of CBB gene expression in Rhodobacter capsulatus. J Bacteriol 184:1905–1915 [CrossRef]
     [Google Scholar]
  62. Utåker J. B., Andersen K., Aakra A., Moen B., Nes I. F. 2002; Phylogeny and functional expression of ribulose 1,5-bisphosphate carboxylase/oxygenase from the autotrophic ammonia-oxidizing bacterium Nitrosospira sp. isolate 40KI. J Bacteriol 184:468–478 [CrossRef]
     [Google Scholar]
  63. Valle E., Kobayashi H., Akazawa T. 1988; Transcriptional regulation of genes for plant-type ribulose-1,5-bisphosphate carboxylase/oxygenase in the photosynthetic bacterium, Chromatium vinosum. Eur J Biochem 173:483–489 [CrossRef]
     [Google Scholar]
  64. Vangnai A. S., Arp D. J., Sayavedra-Soto L. A. 2002; Two distinct alcohol dehydrogenases participate in butane metabolism in Pseudomonas butanovora. J Bacteriol 184:1916–1924 [CrossRef]
     [Google Scholar]
  65. van Keulen G., Ridder A. N., Dijkhuizen L., Meijer W. G. 2003; Analysis of DNA binding and transcriptional activation by the LysR-type transcriptional regulator CbbR of Xanthobacter flavus. J Bacteriol 185:1245–1252 [CrossRef]
     [Google Scholar]
  66. Viale A. M., Kobayashi H., Akazawa T. 1989; Expressed genes for plant-type ribulose 1,5-bisphosphate carboxylase/oxygenase in the photosynthetic bacterium Chromatium vinosum, which possesses two complete sets of the genes. J Bacteriol 171:2391–2400
     [Google Scholar]
  67. Viale A. M., Kobayashi H., Akazawa T., Henikoff S. 1991; rbcR [correction of rcbR], a gene coding for a member of the LysR family of transcriptional regulators, is located upstream of the expressed set of ribulose 1,5-bisphosphate carboxylase/oxygenase genes in the photosynthetic bacterium Chromatium vinosum. J Bacteriol 173:5224–5229
     [Google Scholar]
  68. Vichivanives P., Bird T. H., Bauer C. E., Robert Tabita F. 2000; Multiple regulators and their interactions in vivo and in vitro with the cbb regulons of Rhodobacter capsulatus. J Mol Biol 300:1079–1099 [CrossRef]
     [Google Scholar]
  69. Wallace W., Knowles S. E., Nicholas D. J. 1970; Intermediary metabolism of carbon compounds by nitrifying bacteria. Arch Mikrobiol 70:26–42 [CrossRef]
     [Google Scholar]
  70. Windhovel U., Bowien B. 1990; On the operon structure of the cfx gene clusters in Alcaligenes eutrophus. Arch Microbiol 154:85–91
     [Google Scholar]
  71. Winogradsky S. 1931; The bacterial agents of nitrification – new investigations. Compt Rend Acad Agr France 17:591–599
     [Google Scholar]
  72. Xiang Y., Zhang J., Weeks D. P. 2001; The Cia5 gene controls formation of the carbon concentrating mechanism in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 98:5341–5346 [CrossRef]
     [Google Scholar]
  73. Xu H. H., Tabita F. R. 1994; Positive and negative regulation of sequences upstream of the form II cbb CO2 fixation operon of Rhodobacter sphaeroides. J Bacteriol 176:7299–7308
     [Google Scholar]
  74. Yokoyama K., Hayashi N. R., Arai H., Chung S. Y., Igarashi Y., Kodama T. 1995; Genes encoding RubisCO in Pseudomonas hydrogenothermophilaare followed by a novel cbbQ gene similar to nirQ of the denitrification gene cluster from Pseudomonas species. Gene 153:75–79 [CrossRef]
     [Google Scholar]
  75. Yoo J. G., Bowien B. 1995; Analysis of the cbbF genes from Alcaligenes eutrophus that encode fructose-1,6-sedoheptulose-1,7-bisphosphatase. Curr Microbiol 31:55–61 [CrossRef]
     [Google Scholar]
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The transcription of the cbb operon in Nitrosomonas europaea
Microbiology 150, 1869 (2004); https://doi.org/10.1099/mic.0.26785-0
/content/journal/micro/10.1099/mic.0.26785-0
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