• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jbacterPermissionsJournals.ASM.orgJournalJB ArticleJournal InfoAuthorsReviewers
J Bacteriol. Nov 1991; 173(22): 7313–7323.
PMCID: PMC209239

Evidence for two sets of structural genes coding for ribulose bisphosphate carboxylase in Thiobacillus ferrooxidans.

Abstract

Previously, we reported the cloning of the ribulose-1,5-bisphosphate carboxylase genes (rbcL1-rbcS1) of Thiobacillus ferrooxidans Fe1 (T. Kusano, K. Sugawara, C. Inoue, and N. Suzuki, Curr. Microbiol. 22:35-41, 1991). With these genes as probes, a second set of ribulose-1,5-bisphosphate carboxylase genes (rbcL2-rbcS2) was identified in the same strain and cloned. rbcL1 and rbcL2 encode the large subunits, and rbcS1 and rbcS2 encode the small subunits. Similar restriction patterns between these gene sets suggested a high level of sequence homology. In fact, sequence analysis showed that a 2.2-kb region, including the entire large and small subunit structural genes, was totally conserved in rbcL1-rbcS1 and rbcL2-rbcS2. The rbcL1 (rbcL2) and rbcS1 (rbcS2) genes were 1,422 and 333 bp in length and encoded 473- and 110-amino-acid proteins, respectively. The genes were separated by a 90-bp spacer sequence and were preceded by possible ribosome-binding sites. The N-terminal amino acid sequences of the subunit proteins, synthesized in Escherichia coli, were determined by Edman degradation and found to agree with the deduced amino acid sequences, except for the N-terminal methionine residue. The transcriptional start site of the rbc genes was determined by primer extension, and the size of the rbc transcript was estimated to be about 2.1 kb, suggestive of the cotranscription of rbcL1-rbcS1 and/or rbcL2-rbcS2 mRNAs. Comparisons of amino acid sequences of both subunits with those of other organisms revealed that the ribulose-1,5-bisphosphate carboxylase of T. ferrooxidans, a chemoautotrophic bacterium, is phylogenetically closer to the photosynthetic bacterium Chromatium vinosum than to another chemoautotrophic bacterium, Alcaligenes eutrophus.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.0M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Andersen K, Caton J. Sequence analysis of the Alcaligenes eutrophus chromosomally encoded ribulose bisphosphate carboxylase large and small subunit genes and their gene products. J Bacteriol. 1987 Oct;169(10):4547–4558. [PMC free article] [PubMed]
  • Andersen K, Wilke-Douglas M. Genetic and physical mapping and expression in Pseudomonas aeruginosa of the chromosomally encoded ribulose bisphosphate carboxylase genes of Alcaligenes eutrophus. J Bacteriol. 1987 May;169(5):1997–2004. [PMC free article] [PubMed]
  • Avni A, Edelman M, Rachailovich I, Aviv D, Fluhr R. A point mutation in the gene for the large subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase affects holoenzyme assembly in Nicotiana tabacum. EMBO J. 1989 Jul;8(7):1915–1918. [PMC free article] [PubMed]
  • Birnboim HC, Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. [PMC free article] [PubMed]
  • Boczar BA, Delaney TP, Cattolico RA. Gene for the ribulose-1,5-bisphosphate carboxylase small subunit protein of the marine chromophyte Olisthodiscus luteus is similar to that of a chemoautotrophic bacterium. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4996–4999. [PMC free article] [PubMed]
  • Chattoraj DK, Snyder KM, Abeles AL. P1 plasmid replication: multiple functions of RepA protein at the origin. Proc Natl Acad Sci U S A. 1985 May;82(9):2588–2592. [PMC free article] [PubMed]
  • Curtis SE, Haselkorn R. Isolation and sequence of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase from the cyanobacterium Anabaena 7120. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1835–1839. [PMC free article] [PubMed]
  • Dron M, Rahire M, Rochaix JD. Sequence of the chloroplast DNA region of Chlamydomonas reinhardii containing the gene of the large subunit of ribulose bisphosphate carboxylase and parts of its flanking genes. J Mol Biol. 1982 Dec 25;162(4):775–793. [PubMed]
  • Estelle M, Hanks J, McIntosh L, Somerville C. Site-specific mutagenesis of ribulose-1,5-bisphosphate carboxylase/oxygenase. Evidence that carbamate formation at Lys 191 is required for catalytic activity. J Biol Chem. 1985 Aug 15;260(17):9523–9526. [PubMed]
  • Gibson JL, Tabita FR. Localization and mapping of CO2 fixation genes within two gene clusters in Rhodobacter sphaeroides. J Bacteriol. 1988 May;170(5):2153–2158. [PMC free article] [PubMed]
  • Goldschmidt-Clermont M, Rahire M. Sequence, evolution and differential expression of the two genes encoding variant small subunits of ribulose bisphosphate carboxylase/oxygenase in Chlamydomonas reinhardtii. J Mol Biol. 1986 Oct 5;191(3):421–432. [PubMed]
  • Gutteridge S, Sigal I, Thomas B, Arentzen R, Cordova A, Lorimer G. A site-specific mutation within the active site of ribulose-1,5-bisphosphate carboxylase of Rhodospirillum rubrum. EMBO J. 1984 Dec 1;3(12):2737–2743. [PMC free article] [PubMed]
  • Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983 Jun 5;166(4):557–580. [PubMed]
  • Deaton MA, Bock SE, Zwick H, Freeman JA. Common properties shared by growth-associated proteins of the regenerating optic nerve of goldfish (C. auratus). Neurosci Lett. 1988 Feb 29;85(2):267–271. [PubMed]
  • Hartman FC, Larimer FW, Mural RJ, Machanoff R, Soper TS. Essentiality of Glu-48 of ribulose bisphosphate carboxylase/oxygenase as demonstrated by site-directed mutagenesis. Biochem Biophys Res Commun. 1987 Jun 30;145(3):1158–1163. [PubMed]
  • Hartman FC, Soper TS, Niyogi SK, Mural RJ, Foote RS, Mitra S, Lee EH, Machanoff R, Larimer FW. Function of Lys-166 of Rhodospirillum rubrum ribulosebisphosphate carboxylase/oxygenase as examined by site-directed mutagenesis. J Biol Chem. 1987 Mar 15;262(8):3496–3501. [PubMed]
  • Hattori M, Sakaki Y. Dideoxy sequencing method using denatured plasmid templates. Anal Biochem. 1986 Feb 1;152(2):232–238. [PubMed]
  • Igarashi Y, McFadden BA, el-Gul T. Active site histidine in spinach ribulosebisphosphate carboxylase/oxygenase modified by diethyl pyrocarbonate. Biochemistry. 1985 Jul 16;24(15):3957–3962. [PubMed]
  • Ingledew WJ. Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph. Biochim Biophys Acta. 1982 Nov 30;683(2):89–117. [PubMed]
  • Kado CI, Liu ST. Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol. 1981 Mar;145(3):1365–1373. [PMC free article] [PubMed]
  • Klintworth R, Husemann M, Salnikow J, Bowien B. Chromosomal and plasmid locations for phosphoribulokinase genes in Alcaligenes eutrophus. J Bacteriol. 1985 Nov;164(2):954–956. [PMC free article] [PubMed]
  • Kobayashi H, Viale AM, Takabe T, Akazawa T, Wada K, Shinozaki K, Kobayashi K, Sugiura M. Sequence and expression of genes encoding the large and small subunits of ribulose 1,5-bisphosphate carboxylase/oxygenase from Chromatium vinosum. Gene. 1991 Jan 2;97(1):55–62. [PubMed]
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. [PubMed]
  • Lane DJ, Stahl DA, Olsen GJ, Heller DJ, Pace NR. Phylogenetic analysis of the genera Thiobacillus and Thiomicrospira by 5S rRNA sequences. J Bacteriol. 1985 Jul;163(1):75–81. [PMC free article] [PubMed]
  • Lorimer GH. Ribulosebisphosphate carboxylase: amino acid sequence of a peptide bearing the activator carbon dioxide. Biochemistry. 1981 Mar 3;20(5):1236–1240. [PubMed]
  • Mazur BJ, Chui CF. Sequence of a genomic DNA clone for the small subunit of ribulose bis-phosphate carboxylase-oxygenase from tobacco. Nucleic Acids Res. 1985 Apr 11;13(7):2373–2386. [PMC free article] [PubMed]
  • Miziorko HM, Lorimer GH. Ribulose-1,5-bisphosphate carboxylase-oxygenase. Annu Rev Biochem. 1983;52:507–535. [PubMed]
  • Nierzwicki-Bauer SA, Curtis SE, Haselkorn R. Cotranscription of genes encoding the small and large subunits of ribulose-1,5-bisphosphate carboxylase in the cyanobacterium Anabaena 7120. Proc Natl Acad Sci U S A. 1984 Oct;81(19):5961–5965. [PMC free article] [PubMed]
  • Norrander J, Kempe T, Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. [PubMed]
  • Reed KC, Mann DA. Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res. 1985 Oct 25;13(20):7207–7221. [PMC free article] [PubMed]
  • Robison PD, Tabita FR. Modification of ribulose bisphosphate carboxylase from Rhodospirillum rubrum with tetranitromethane. Biochem Biophys Res Commun. 1979 May 14;88(1):85–91. [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Schloss JV, Stringer CD, Hartman FC. Identification of essential lysyl and cysteinyl residues in spinach ribulosebisphosphate carboxylase/oxygenase modified by the affinity label N-bromoacetylethanolamine phosphate. J Biol Chem. 1978 Aug 25;253(16):5707–5711. [PubMed]
  • Shinozaki K, Sugiura M. The nucleotide sequence of the tobacco chloroplast gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Gene. 1982 Nov;20(1):91–102. [PubMed]
  • Shinozaki K, Sugiura M. The gene for the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is located close to the gene for the large subunit in the cyanobacterium Anacystis nidulans 6301. Nucleic Acids Res. 1983 Oct 25;11(20):6957–6964. [PMC free article] [PubMed]
  • Shinozaki K, Yamada C, Takahata N, Sugiura M. Molecular cloning and sequence analysis of the cyanobacterial gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci U S A. 1983 Jul;80(13):4050–4054. [PMC free article] [PubMed]
  • Shiratori T, Inoue C, Sugawara K, Kusano T, Kitagawa Y. Cloning and expression of Thiobacillus ferrooxidans mercury ion resistance genes in Escherichia coli. J Bacteriol. 1989 Jun;171(6):3458–3464. [PMC free article] [PubMed]
  • SILVERMAN MP, LUNDGREN DG. Studies on the chemoautotrophic iron bacterium Ferrobacillus ferrooxidans. I. An improved medium and a harvesting procedure for securing high cell yields. J Bacteriol. 1959 May;77(5):642–647. [PMC free article] [PubMed]
  • Stringer CD, Hartman FC. Sequences of two active-site peptides from spinach ribulosebisphosphate carboxylase/oxygenase. Biochem Biophys Res Commun. 1978 Feb 28;80(4):1043–1048. [PubMed]
  • Tabita FR. Molecular and cellular regulation of autotrophic carbon dioxide fixation in microorganisms. Microbiol Rev. 1988 Jun;52(2):155–189. [PMC free article] [PubMed]
  • Tabita FR, McFadden BA. D-ribulose 1,5-diphosphate carboxylase from Rhodospirillum rubrum. II. Quaternary structure, composition, catalytic, and immunological properties. J Biol Chem. 1974 Jun 10;249(11):3459–3464. [PubMed]
  • Valle E, Kobayashi H, Akazawa T. Transcriptional regulation of genes for plant-type ribulose-1,5-bisphosphate carboxylase/oxygenase in the photosynthetic bacterium, Chromatium vinosum. Eur J Biochem. 1988 May 2;173(3):483–489. [PubMed]
  • Viale AM, Kobayashi H, Akazawa T. 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. 1989 May;171(5):2391–2400. [PMC free article] [PubMed]
  • Viale AM, Kobayashi H, Akazawa T. Distinct properties of Escherichia coli products of plant-type ribulose-1,5-bisphosphate carboxylase/oxygenase directed by two sets of genes from the photosynthetic bacterium Chromatium vinosum. J Biol Chem. 1990 Oct 25;265(30):18386–18392. [PubMed]
  • Wasmann CC, Ramage RT, Bohnert HJ, Ostrem JA. Identification of an assembly domain in the small subunit of ribulose-1,5-bisphosphate carboxylase. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1198–1202. [PMC free article] [PubMed]
  • Yanisch-Perron C, Vieira J, Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. [PubMed]
  • Yates JR, Cunningham RP, Holmes DS. IST2: an insertion sequence from Thiobacillus ferrooxidans. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7284–7287. [PMC free article] [PubMed]
  • Yates JR, Holmes DS. Two families of repeated DNA sequences in Thiobacillus ferrooxidans. J Bacteriol. 1987 May;169(5):1861–1870. [PMC free article] [PubMed]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

Formats:

Related citations in PubMed

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...