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Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UK
Correspondence
Paul R. Norris
P.R.Norris{at}warwick.ac.uk
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ABSTRACT |
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Present address: Mathys and Squire, Patent Attorneys, 120, Holborn, London EC1N 2SQ, UK.
The GenBank accession number of the S. acidophilus genomic DNA sequence containing putative cbb genes and flanking sequences is U75301.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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) and in the development of base metal extraction processes with various mineral sulfides (Dew et al., 1999). Their ribulose bisphosphate carboxylase/oxygenase (RuBisCO) activity has indicated that the Calvin–Benson–Bassham (CBB) cycle is likely to be the primary route of CO2 fixation when these nutritionally versatile acidophiles grow autotrophically (Wood & Kelly, 1984). However, there has been no characterization of the CBB cycle's enzymes, encoding genes or regulation in these organisms. Form I RuBisCOs have been divided into red or green types with reference to their presence in red algae or chlorophytes respectively (Delwiche & Palmer, 1996). Both types, and the two major subgroups of each, contain examples from prokaryotes (Watson & Tabita, 1997). The partial sequences of RuBisCO large subunits predicted from cbbL gene fragments of Sulfobacillus strain NMW-6 (Holden & Brown, 1993) and Sulfobacillus acidophilus (Clark, 1995) were reported as most similar to sequences of those proteobacteria, such as Ralstonia eutropha, that have red-type RuBisCOs. Analysis of a larger fragment of the S. acidophilus RuBisCO inferred from a partial cbbL gene PCR product confirmed this affiliation but showed a close relationship only to RuBisCO of the anoxygenic phototroph Oscillochloris trichoides (Tourova et al., 2006).
Sulfobacillus thermosulfidooxidans grows strongly on mineral sulfides and S. acidophilus grows well on sulfur (Norris et al., 1996), but both grow poorly autotrophically unless the CO2 concentration in culture aeration is enhanced (Clark & Norris, 1996). S. thermosulfidooxidans has been used here to investigate some aspects of its CO2 assimilation, including some relevant enzyme activities in comparison to those of the well-studied Gram-negative, mineral sulfide-oxidizing acidophile, Acidithiobacillus ferrooxidans. The genes encoding RuBisCO and other enzymes potentially involved in the CBB cycle in S. acidophilus are described.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Acidithiobacillus ferrooxidans (DSMZ 583) was grown in the same medium but at 30 °C. Cultures (0.5 l) were grown in stirred reactors (1 l capacity) gassed with air or with 1 % (v/v) CO2 in air (0.25 l min–1). S. thermosulfidooxidans was also grown mixotrophically with ferrous iron in the presence of glucose (1 mM) and 1 % (v/v) CO2 in air. S. acidophilus was grown lithoheterotrophically with ferrous iron and yeast extract (0.02 %, w/v) to provide biomass for DNA extraction. Rhodobacter sphaeroides (NCIMB 8253) was kindly provided by N. H. Mann (University of Warwick). It was harvested from an illuminated, continuous culture operated with a dilution rate of 0.05 h–1 under CO2 limitation in butyrate/bicarbonate medium (Gibson & Tabita, 1977). The culture was grown at 30 °C and degassed with O2-free N2.
Preparation of cell suspensions and cell-free extracts.
Autotrophic cultures of S. thermosulfidooxidans (grown with CO2 supplementation) and A. ferrooxidans were harvested from the exponential growth phase by centrifugation for 10 min at 15 000 g. Cell pellets were washed with 50 mM Tris/HCl (pH 8) and 10 mM EDTA. Permeabilized cells were prepared by incubation with Triton X-100 or cetyl trimethylammonium bromide (CTAB) at selected concentrations (see Results) for 15 min at 45 °C (S. thermosulfidooxidans) or 30 °C (A. ferrooxidans). Cell-free extracts were prepared at 4 °C by four passes through a French pressure cell at 138 MPa (S. thermosulfidooxidans) or 276 MPa (A. ferrooxidans) followed by centrifugation (15 000 g for 15 min) to remove cell debris. A stromal extract of pea (Pisum sativum) chloroplasts was prepared by hypertonic lysis.
Partial purification of bacterial RuBisCO.
The procedure was based on those of Bowien (1977) and Cook et al. (1991). Membrane-free fractions of S. thermosulfidooxidans and A. ferrooxidans were prepared from cell-free extracts by centrifugation at 40 000 g for 2 h. Fractions precipitated with 30–55 % (w/v) ammonium sulfate were the most active fractions after resuspension and dialysis. These were concentrated by ultrafiltration (10 kDa cut-off) and fractionated on 0.2–0.8 M sucrose gradients. Active fractions were again pooled and subjected to FPLC with a Green-A dye-ligand column (Amicon). Proteins were eluted with a 0–2 M KCl gradient.
Enzyme assays.
RuBisCO, phosphoribulokinase (PRK) and phosphoenolpyruvate (PEP) carboxylase were assayed with minor modifications to procedures described by Smith et al. (1980). An assay buffer (0.9 ml) was added to cell-free extracts or permeabilized cells (0.3 ml aliquots containing approximately 0.5 mg cell protein). The buffer contained Tris/HCl, pH 8 (78 mM), MgCl2 (25 mM), reduced glutathione (2.1 mM) and NaH14CO3 (44 mM; 6.9x106 Bq mmol–1). PEP carboxylase activity was assayed with addition of sodium glutamate (8 mM) and acetyl-CoA (0.32 mM) and replacement of Tris/HCl and MgCl2 by Tris/H2SO4 and MgSO4 as described by Smith et al. (1980). PRK was assayed in the presence of ATP (4.6 mM), NADH (0.85 mM) and RuBisCO (4.5 mg spinach enzyme, Sigma). Enzymes were activated by 10 min incubation of assay mixtures at 45 °C (S. thermosulfidooxidans) or 30 °C (A. ferrooxidans) before addition (0.3 ml) of the appropriate substrates. These were ribulose 1,5-bisphosphate (RuBP) (10 mM), PEP (60 mM) or ribose 5-phosphate (10 mM). Samples (200 µl) were taken and added to 6 M phosphoric acid (200 µl) in glass scintillation vials that were heated for 1 h at 40 °C to release unfixed CO2 before addition of 10 ml Optiphase Safe scintillation fluid (LKB) for counting. The substrate affinities of RuBisCOs were determined essentially as described by Pierce et al. (1982) and Cook et al. (1991). Partially purified enzymes from S. thermosulfidooxidans and A. ferrooxidans and pea enzyme in a stromal extract were used. A range of RuBP concentrations (0.025–0.4 mM) in the presence of 30 mM NaHCO3 and a range of NaH14CO3 concentrations (0.4–6.6 mM) in the presence of 1 mM RuBP were used in a buffer of Bicine (100 mM), dithiothreitol (0.5 mM), EDTA (0.2 mM) and MgCl2 (20 mM). Protein concentrations were approximately 0.1 mg ml–1. Reactions were terminated with HCl before release of unfixed CO2 and counting as above. Reported enzyme activities are the means of five independent experiments with permeabilized cells and three independent experiments with cell-free extracts.
Electrophoresis and Western blotting.
Whole-cell lysates were prepared by incubation with lysozyme (1 mg ml–1) for 15 min at 37 °C and subjected to standard slab gel SDS-PAGE using 10 % (w/v) acrylamide gels. Electrophoresed proteins were stained with Coomassie blue R250 or transferred to Hybond C nitrocellulose paper (Amersham) and probed with anti-R. sphaeroides form I RuBisCO antibodies kindly provided by G. A. Codd (University of Dundee) and J. C. Murrell (University of Warwick). Native PAGE used 3–40 % (w/v) acrylamide gradients and 5 % (w/v) acrylamide tube gels. RuBisCO activity was assayed in tube gels after electrophoresis of sucrose gradient-fractionated cell-free extracts. These fractions were prepared as described above in buffer containing Tris/HCl (20 mM), MgCl2 . 6H2O (10 mM), NaHCO3 (50 mM), EDTA (1 mM) and β-mercaptoethanol (5 mM). Following native PAGE of fractions that showed RuBisCO activity, tube gels were frozen at –20 °C and sliced into 1 mm discs. These were incubated in RuBisCO assay mix (200 µl) with shaking at 4 °C for 3 h to facilitate enzyme activation. After pre-incubation for 10 min at 30 °C (A. ferrooxidans and R. sphaeroides) or 45 °C (S. thermosulfidooxidans), RuBisCO activity was determined during 30 min further incubation after addition of 20 µl RuBP (10 mM).
Identification of Calvin–Benson–Bassham cycle genes.
Routine DNA manipulations were performed by standard methods. N-Hybond membrane (Amersham), digoxigenin (DIG) nucleic acid labelling and chemiluminescence detection systems (Boehringer Mannheim) were used in Southern blotting. Genomic DNA from S. acidophilus was digested with several endonucleases, electrophoresed and blotted. Two probes, each of 80 oligonucleotides, were based on sequence positions 1–80 and 221–300 of a 387 nucleotide fragment of the gene (cbbL) predicted to encode the RuBisCO large subunit of S. acidophilus (Clark, 1995). The DNA fragments labelled most strongly with each probe were the same size for any single enzyme digest, with the exception of EcoRI-digested DNA because of an EcoRI site between the regions specific for each probe. A BamHI-digested fragment of approximately 9 kb was eluted and cloned in pUC18 with an Escherichia coli host (Invitrogen). Inverse PCR (Ochman et al., 1993) was used to allow sequencing upstream of the cloned region after initial sequencing indicated that the gene encoding the RuBisCO large subunit (cbbL) was close to the 5' end of the cloned fragment. Genomic DNA was digested with restriction endonucleases (SalI, SacI and BamHI) and recircularized at a concentration of 5 ng µl–1. Inverse PCR used the religated DNA as template to amplify approximately 6 kb upstream of the cbbL gene. The GenBank accession number of the S. acidophilus genomic DNA sequence containing putative cbb genes and flanking sequences is U75301.
Sequence alignments and phylogenetic analysis.
Alignments of translated gene sequences produced with CLUSTAL_X (Chenna et al., 2003) were manually adjusted as required and gaps were removed before analysis with PHYLIP programs (Phylogeny Inference Package version 3.6a3; Felsenstein, 2002). Preliminary trees were constructed using distance and maximum-likelihood programs generally with 25–35 appropriate sequences. Maximum-likelihood trees with a limited number of sequences that were representative of the larger trees are presented.
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RESULTS |
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). The organisms showed similar RuBisCO activity and an increase of between 2.2- and 2.7-fold in this activity when grown under air. PRK and PEP carboxylase activities were not clearly influenced by the CO2 concentration during growth.
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). Further SDS-PAGE coupled to densitometry of Coomassie-stained bands with correction for protein loading differences indicated they were about threefold more abundant in CO2-limited cells of S. thermosulfidooxidans compared to cells grown with 1 % (v/v) CO2 in air. The increase was between twofold and threefold for the putative RuBisCO in similarly treated A. ferrooxidans. Whole-cell extract fractions of S. thermosulfidooxidans, A. ferrooxidans and R. sphaeroides that showed RuBisCO activity after sucrose gradient centrifugation were pooled and analysed by native PAGE. The activity in native gel slices resided in two peaks with R. sphaeroides, indicating form I and form II enzyme activities, and in single peaks with S. thermosulfidooxidans and A. ferrooxidans which corresponded to the activity of the R. sphaeroides form I enzyme (data not shown).
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; Kusian & Bowien, 1997). The upstream genes encoded a putative RNA polymerase factor sigma70 (orf1) and PEP carboxylase (ppc) and those downstream of the cluster encoded a putative acetyltransferase (orf2), a sensor histidine kinase (orf3) and response regulator receiver (orf4), and a transcription terminator factor Rho (orf5). The gene arrangement is shown in Fig. 2 and the proteins inferred from translations of the putative cbb genes are listed in Table 3. The translational start sites were predicted from similarity searches in protein databases and putative Shine–Dalgarno (SD) regions. The mol% G+C contents of the eight putative cbb genes were between 54.6 and 59.5, with most close to the 55–56 mol% G+C value for S. acidophilus genomic DNA.
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) are present in the inferred S. acidophilus protein sequence. This was placed on a phylogenetic tree close to red-type enzyme sequences, but before these subdivided into groups C and D (Fig. 3a). Ten amino acids were conserved in 95 % of the examples in a comparison of green- and red-type RuBisCO small-subunit sequences (Spreitzer, 2003) and these were all present in the S. acidophilus sequence. The S. acidophilus small subunit was phylogenetically most closely related to those from organisms with red-type algal and bacterial small subunits (Fig. 3b) and, like those, it has an extended C-terminal region that could augment interaction with the large subunit (Hansen et al., 1999; Sugawara et al., 1999). The cbbX-encoded protein, which might be required for synthesis of active red-type RuBisCOs (Gibson & Tabita, 1997; Bowien & Kusian, 2002), differed in only one sequence position of those described as invariant when similar sequences were first compared (Gibson & Tabita, 1997). Its phylogenetic relationship appears closer to proteobacterial than red algal proteins (Fig. 3c) in an analysis with an outgroup that reflects the relationship of these sequences to those of stage-specific Bacillus sporulation factors and a group of mycobacterial hypothetical proteins (Maier et al., 2000). Two similar sequences from cyanobacteria with green-type RuBisCOs were grouped separately from those of the proteobacteria: the cbbX genes in these cyanobacteria are among a cluster of RuBisCO and carboxysome genes rather than adjacent to cbbS.
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). The partial sequence was 49–53 % identical to these cyanobacterial PRK sequences and 40–46 % to a second group of related sequences in the cyanobacteria (Fig. 3d).
Other cbb genes.
The putative cbb genes in the S. acidophilus cluster that could encode carbohydrate-transforming enzymes that are not unique to the CBB pathway have inferred products that appear most closely related to similar proteins of some other Gram-positive bacteria, particularly species of Carboxydothermus, Geobacillus and Bacillus (Table 3). Amino acid sequence analysis has shown no homology between class I and class II fructose-1,6-bisphosphate (FBP) aldolases, and a division of class II types into A and B groups (Plaumann et al., 1997). The S. acidophilus cbbA sequence encodes a putative class IIB enzyme that appears most closely affiliated with those of Gram-positive bacteria (Fig. 3e). Ribulose-5-phosphate-3-epimerase (RPE) catalyses the interconversion of ribulose 5-phosphate and xylulose 5-phosphate in reductive and oxidative pentose phosphate pathways. RPE is encoded by genes termed cbbE if they are associated with the CBB pathway or rpe if they are not. In E. coli, the rpe gene is one of three ORFs that share conserved motifs (Sprenger, 1995): the sequence of the inferred product of one of the two genes of unknown function that are less closely related to confirmed rpe/cbbE genes was used as an outgroup in analysis of the S. acidophilus sequence. Its placement closest to those of low G+C Gram-positive bacteria was only supported by low bootstrap values (Fig. 3f) with identities of about 60 % to sequences from species of Bacillus and Synechococcus and 50 % to the cbbE-encoded sequences from the proteobacteria Bradyrhizobium japonicum and Rhodobacter capsulatus. The inferred transketolase of S. acidophilus encoded by the putative cbbT contains the conserved thiamine diphosphate-binding motif and all of the residues described as invariant when similar sequences were previously compared (Schenk et al., 1997). Using a yeast enzyme sequence outgroup, there was poor bootstrap support for the branching order close to the S. acidophilus sequence, which was among those from a varied collection of mostly Gram-positive bacteria, and separate from most sequences previously described as cbbT-encoded (data not shown). In relation to three groups of divergent, class I glyceraldehyde-3-phosphate dehydrogenases (GAP) (Figge et al., 1999), the S. acidophilus cbbG gene product sequence was placed with those of the GAP II subgroup (Fig. 3g).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Partially purified RuBisCOs from S. thermosulfidooxidans and A. ferrooxidans showed similar affinities for CO2 and for RuBP (Table 2). The apparent affinities of the A. ferrooxidans enzyme for CO2 and RuBP were slightly lower and similar respectively to the 28 µM CO2 and 80 µM RuBP reported for A. ferrooxidans by Holuigue et al. (1987). Values in control assays with pea were close to published values (Yeoh et al., 1981). The apparent affinity of the S. thermosulfidooxidans enzyme for CO2 was in the range (25–100 µM) reported (Horken & Tabita, 1999) for bacteria (e.g. Bradyrhizobium japonicum and Xanthobacter flavus) with enzymes that are phylogenetically close to that of S. acidophilus (Fig. 3a) and its affinity for RuBP was slightly lower than those found in the Bradyrhizobium–Xanthobacter group (17–55 µM RuBP). The apparent derepression of RuBisCO with CO2 limitation of A. ferrooxidans and S. thermosulfidooxidans was similar to that with CO2 limitation of other sulfur-oxidizing bacteria such as Thiobacillus (now Halothiobacillus) neapolitanus (Beudeker et al., 1980). In summary, the different growth responses of the Sulfobacillus and Acidithiobacillus species to CO2 limitation appeared unrelated to characteristics of the key enzymes directly involved in CO2 fixation. The responses were more likely related to differences in CO2-uptake capacities and the presence of carboxysomes in A. ferrooxidans but not in S. thermosulfidooxidans (data not shown).
The number and order of genes in CBB cycle operons in bacteria vary considerably (Gibson & Tabita, 1996; Kusian & Bowien, 1997). The inferred products of eight potential cbb genes found in a cluster in S. acidophilus have the key residues required for activity. Further work is required to link directly the observed RuBisCO, PRK and PEP carboxylase activities to expression of potential cbbL, cbbS and cbbP genes, and so far the activities and genes have been described for different, although closely related, species. The relationship of the S. acidophilus RuBisCO to red-type enzymes was indicated by analysis of the predicted large- and small-subunit sequences and by the presence of a cbbX gene immediately following cbbL and cbbS. The identity of the inferred sequence of the S. acidophilus CbbL to the most closely related full sequences available for comparison is high (Table 3) but a closer relationship exists to the RuBisCO of Oscillochloris trichoides. Over the 224 amino acid sequence positions described for O. trichoides (GenBank accession no. DQ139403), S. acidophilus shared 89 % identity compared to 76–78 % with the D-subgroup enzyme sequences used in the phylogenetic analysis (Fig. 3). In contrast to its RuBisCO, the predicted S. acidophilus PRK sequence did not show a close evolutionary relationship to the respective protein of proteobacteria with red-type RuBisCO (Fig. 3c). While PRKs from prokaryotes and eukaryotes share key features of the active site for RuBP synthesis, there are major differences in primary sequence, quaternary structure and regulation of the enzymes (Miziorko, 1998). Over the region of sequence comparison between spinach and R. sphaeroides, one relative insertion (of 15 residues) in the plant sequence and three (of 10, 11 and 3 residues) in the proteobacterial sequence were all absent in cyanobacteria and S. acidophilus. The inferred protein of S. acidophilus has the key residues that have been implicated in catalysis in R. sphaeroides (R49, H45 and K165 involved in Ru5P binding, key catalytic sites D42, E131, R168, D169 and R173, and R187, which may influence cooperativity of substrate binding). Those involved in Ru5P binding and R187 are changed in the uridine kinase of B. subtilis while the others are conserved. The closeness of the conserved Y98 and H100 to the active site in R. sphaeroides was noted (Harrison et al., 1998) and H100 significantly influences catalytic efficiency (Runquist & Miziorko, 2006). Y98, but not H100, is present in the B. subtilis kinase while both are in the S. acidophilus putative PRK sequence. A uridine kinase-like enzyme in a Sulfobacillus ancestor could have evolved to RuBP binding and enzymes of carbohydrate central metabolism could have adapted to fulfil CBB cycle functions, in keeping with the consideration that it is the reactions of the cycle that are conserved rather than the origins of the enzymes that carry them out (Martin & Schnarrenberger, 1997). The potential CBB cycle enzymes CbbA, CbbE, CbbG and CbbT of S. acidophilus, in contrast to those described in other bacteria, appear affiliated with proteins of low mol% G+C Gram-positive bacteria, although with some low bootstrap values (Fig. 3). A suggestion of a Gram-positive bacterium as a possible origin of a CBB-active enzyme of some proteobacteria arose previously from the apparent relatedness of their CbbA to the class II FBP aldolase of B. subtilis (van den Bergh et al., 1996). However, the RuBisCO of S. acidophilus shows no closer relationship than other red-type RuBisCOs to the distantly related RuBisCO-like proteins (including examples in several Bacillus species) which could be closer to a common ancestor of CBB cycle-active RuBisCOs (Ashida et al., 2005), giving no support for particularly early evolution of a bacterial CBB cycle in Sulfobacillus-like species. Acquisition of CBB cycle genes by Sulfobacillus (or an ancestor) from an unknown organism could also have led to their autotrophy. It is not yet known if the close relationship of the Sulfobacillus and Oscillochloris CbbL sequences might extend to those of other CBB cycle proteins in these bacteria. Neither genus has other closely related genera with organisms that use the CBB cycle.
Any significance to the location of the ppc gene in the opposite orientation adjacent to the genes presumably encoding the major CO2 assimilation pathway is unknown but PEP has been discussed as a signal metabolite with regard to the carbon status of cells and therefore to cbb gene expression (Shively et al., 1998). The redox state of the cell, and therefore the availability of reduced inorganic substrates in chemoautotrophs, is also related to expression of the CBB cycle, which could act as an electron sink (Shively et al., 1998; Dubbs & Tabita, 2004). A ferrous iron oxidation-minus mutant of S. acidophilus, grown in the presence of iron and yeast extract, did not produce RuBisCO until reversion to iron oxidation after several serial cultures with the same substrates (N. P. Burton & P. R. Norris, unpublished work). This first description of a cbb gene cluster in the nutritionally versatile Sulfobacillus species could facilitate investigation of possible interaction between the CBB cycle and iron oxidation.
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ACKNOWLEDGEMENTS |
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Edited by: R. van Spanning
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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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.[CrossRef]
Bowien, B. (1977). RuBisCO from Paracoccus denitrificans. FEMS Microbiol Lett 2, 263–266.[CrossRef]
Bowien, B. & Kusian, B. (2002). Genetics and control of CO2 assimilation in the chemoautotroph Ralstonia eutropha. Arch Microbiol 178, 85–93.[CrossRef][Medline]
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.
Clark, D. A. (1995). The study of acidophilic, moderately thermophilic iron-oxidizing bacteria. PhD Thesis, University of Warwick.
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.
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.
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.[Abstract]
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.
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][Medline]
Felsenstein, J. (2002). PHYLIP (Phylogeny Inference Package), version 3.6a3. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, USA.
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.[Abstract]
Gibson, J. L. & Tabita, F. R. (1977). Different molecular forms of RuBisCO from Rhodobacter sphaeroides. J Biol Chem 252, 943–949.
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][Medline]
Gibson, J. L. & Tabita, F. R. (1997). Analysis of the cbbXYZ operon in Rhodobacter sphaeroides. J Bacteriol 179, 663–669.
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][Medline]
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.
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][Medline]
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.[Medline]
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.
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][Medline]
Jordan, D. B. & Ogren, W. L. (1981). Species variation in the specificity of ribulose-bisphosphate carboxylase-oxygenase. Nature 291, 513–515.[CrossRef]
Kusian, B. & Bowien, B. (1997). Organization and regulation of cbb CO2 assimilation genes in autotrophic bacteria. FEMS Microbiol Rev 21, 135–155.[CrossRef][Medline]
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.
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][Medline]
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.
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.
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.[Abstract]
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.[Medline]
Pierce, J. W., McCurry, S. D., Mulligan, R. M. & Tolbert, N. E. (1982). Activation and assay of RuBisCO. Methods Enzymol 89, 47–55.[Medline]
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][Medline]
Runquist, J. A. & Miziorko, H. M. (2006). Functional contribution of a conserved, mobile loop histidine of phosphoribulokinase. Protein Sci 15, 837–842.
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][Medline]
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][Medline]
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.
Spreitzer, R. J. (2003). Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase. Arch Biochem Biophys 414, 141–149.[CrossRef][Medline]
Sprenger, G. A. (1995). Genetics of pentose-phosphate pathway enzymes of Escherichia coli K-12. Arch Microbiol 164, 324–330.[CrossRef][Medline]
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.
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]
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.
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][Medline]
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.
Yeoh, H.-H., Badger, M. R. & Watson, L. (1981). Variations in kinetic properties of RuBisCO among plants. Plant Physiol 67, 1151–1155.
Received 21 January 2007;
revised 1 April 2007;
accepted 10 April 2007.
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