JXB Advance Access published online on February 16, 2008
Journal of Experimental Botany, doi:10.1093/jxb/erm361
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SPECIAL ISSUE REVIEW PAPER |
Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships
1Department of Microbiology, The Ohio State University, 484 West 12th Avenue, Columbus, Ohio 43210–1292, USA
2The Plant Molecular Biology Biology/Biotechnology Program, The Ohio State University, 484 West 12th Avenue, Columbus, Ohio 43210–1292, USA
3The OSU Biochemistry Program, The Ohio State University, 484 West 12th Avenue, Columbus, Ohio 43210–1292, USA
4College of Marine and Earth Studies, Delaware Biotechnology Institute, University of Delaware, 127 DBI, 15 Innovation Way, Newark, DE 19711, USA
* To whom correspondence should be addressed at the Department of Microbiology, The Ohio State University. E-mail: Tabita.1{at}osu.edu
Received 22 October 2007; Revised 29 November 2007 Accepted 18 December 2007
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Abstract |
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 Top Abstract IntroductionThe different forms of...Phylogenetic relationships in...The diversity and evolution...Recent structure/function...ConclusionsReferences |
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There are four forms of ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) found in nature. Forms I, II, and III catalyse the carboxylation and oxygenation of ribulose 1,5-bisphosphate, while form IV, also called the Rubisco-like protein (RLP), does not catalyse either of these reactions. There appear to be six different clades of RLP. Although related to bona fide Rubisco proteins at the primary sequence and tertiary structure levels, RLP from two of these clades is known to perform other functions in the cell. Forms I, II, and III Rubisco, along with form IV (RLP), are thought to have evolved from a primordial archaeal Rubisco. Structure/function studies with both archaeal form III (methanogen) and form I (cyanobacterial) Rubisco have identified residues that appear to be specifically involved with interactions with molecular oxygen. A specific region of all form I, II, and III Rubisco was identified as being important for these interactions.
Key words: CBB cycle, different forms, evolution, Rubisco, structure/function
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Introduction |
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TopAbstractIntroductionThe different forms of...Phylogenetic relationships in...The diversity and evolution...Recent structure/function...ConclusionsReferences |
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There are four known metabolic routes by which micro-organisms and plants reduce and assimilate carbon dioxide into organic matter (Fuchs et al., 1987; Yoon et al., 2000). Paramount among these on a global scale is the Calvin–Benson–Bassham (CBB) reductive pentose phosphate pathway. In this scheme, the enediol form of the sugar bisphosphate ribulose 1,5-bisphosphate (RuBP) accepts a molecule of CO2, with the enzyme RuBP carboxylase/oxygenase (Rubisco) catalysing the actual primary CO2 fixation reaction. Rubisco is found in most autotrophic organisms, ranging from diverse prokaryotes, including photosynthetic and chemolithoautotrophic bacteria and archaea, to eukaryotic algae and higher plants. All bona fide Rubisco proteins must first be activated or carbamylated at the
-amino group of a specific lysine residue (e.g. Lys-201 of the plant enzyme), with divalent cations bound to adjacent acidic residues serving to stabilize the carbamate. This carbamylated lysine or E-CO2-Me2+ ternary complex catalyses proton abstraction from the substrate RuBP, thus initiating the catalytic cycle. While the basic mechanistic details underlying catalysis are well understood (Cleland et al., 1998), there still remain many perplexing issues about Rubisco. Not the least of which are the fundamental reasons why structurally superimposable proteins from different sources, with up to 90% sequence identity, often show vastly different catalytic properties and distinct kinetic behaviour (Tabita, 1999).
The active site of all Rubisco proteins is formed by the interaction of two monomeric catalytic subunits, with the C-terminus of one monomer binding to the N-terminus of a second monomer in a specific manner to form two active sites per dimer. Distinct residues from both monomeric units thus comprise the active site required for both carboxylation of CO2 and the fixation of molecular oxygen (Fig. 1), with the two gaseous substrates clearly competing for the same active site. The relative rate of carboxylation and oxygenation of RuBP (vc/vo) thus defines the protein's catalytic efficiency or ability to provide the cell with needed carbon. The latter ratio may be determined after specific isolation of the reaction products, 3- phosphoglyceric acid (3-PGA) and 2-phosphoglycolate (2-PG) (Fig. 1), which may be easily distinguished after performing the enzymatic reaction with [1-3H]-RuBP. Quantitation of [3H]-PGA or [3H]-2-PG from [1-3H]-RuBP, in the presence of both CO2 and O2, is a measure of the relative activity of the carboxylase and oxygenase reactions, respectively, under conditions where both reactions may be measured simultaneously. From the foregoing, it is apparent that efficient Rubisco catalysis is dependent on the inherent ability of the enzyme to discriminate between CO2 and O2 (the 
or 
value) at the relative concentration of CO2 and O2 employed in a particular reaction. The rates of the two reactions are defined by vc/vo=[CO2]/[O2]. Thus, =vc [O2]/vo [CO2] and =VcKo/VoKc with Vc and Vo representing maximum velocities for carboxylation and oxygenation, respectively, and Kc and Ko the relative Michaelis constants for CO2 and O2, respectively.
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The different forms of Rubisco |
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TopAbstractIntroductionThe different forms of...Phylogenetic relationships in...The diversity and evolution...Recent structure/function...ConclusionsReferences |
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There are four known forms or types of Rubisco found in nature, forms I, II, III, and IV (Tabita, 1999; Tabita et al., 2007), each of which is placed in a separate category based on differences in primary sequence of the constituent
50 kDa polypeptide. In addition, these four different holoenzyme forms are often structurally unique, yet the fundamental unit common to all forms is the large (catalytic) subunit dimer. Of the four forms, form I is the most abundant. It is found in eukaryotes and bacteria, and is composed of eight large subunits and eight small subunits (L8S8) with 422 symmetry (Schneider et al., 1992). Many form I Rubisco structures from different organisms have been determined and show high similarity (Andersson and Taylor, 2003). In form I, the basic structural motif, the dimer of L, is repeated four times to form a catalytic (L8) core of 8 L subunits, with small subunits on top and bottom of this core (Fig. 2).
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The first Rubisco structure to be solved was that from the bacterium Rhodospirillum rubrum (Andersson et al., 1989; Schneider et al., 1990). This enzyme is a simple dimer of L subunits (Tabita and McFadden, 1974) that shares only 25–30% identity to L subunits from type I Rubisco. It has served for many years as the paradigm for structure–function studies of Rubisco (Hartman and Harpel, 1994) and has provided the base-line information required to determine the structure of the more complex form I enzyme. Thus, the structure of this type II or form II Rubisco closely resembles the structure of the basic dimer of the form I Rubisco despite some differences in catalytic properties. Further work in several laboratories (see Portis, 1992; Hartman and Harpel, 1994; Cleland et al., 1998; Spreitzer, 1999; Tabita, 1999; Spreitzer and Salvucci, 2002, for recent reviews), including our own studies, has led to: (i) the demonstration that L is definitely the catalytic subunit of the L8S8 enzyme and undergoes catalysis in the absence of S (Andrews, 1988; Lee and Tabita, 1990); (ii) the identification of residues that participate in various aspects of the catalytic mechanism including CO2/O2 specificity (Hartman and Harpel, 1994; Cleland et al., 1998; Tabita, 1999; Spreitzer and Salvucci, 2002); (iii) the finding that effector sites are also found on L (Lee et al., 1991b); (iv) the finding that S affects activity by influencing the correct conformation of the catalytic core of L (Andrews, 1988; Lee and Tabita, 1990; Lee et al., 1991a); (v) verification of the prediction from X-ray models that the subtle conformational change elicited by S can influence important kinetic parameters including CO2/O2 specificity (Read and Tabita, 1992a, b; Spreitzer et al., 2005). These latter studies demonstrate that residues far from the active site can influence important catalytic parameters. Finally, as indicated, it should be stressed that X-ray structural work established that the active site is formed from the interface between the N-terminal domain of one subunit and the
/β barrel of the C-terminal domain of the second subunit of a dimer, with at least two subunits required to form the complete active site. |
Phylogenetic relationships in the Rubisco superfamily |
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TopAbstractIntroductionThe different forms of...Phylogenetic relationships in...The diversity and evolution...Recent structure/function...ConclusionsReferences |
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The division of Rubisco into phylogenetically and catalytically distinct structural form I and form II proteins lasted for about 20 years. However, the recent explosion of completed genomic sequencing projects, from diverse organisms, has led to the finding of additional phylogenetically distinct Rubisco forms, including those from organisms that use alternatives to the CBB pathway to fix CO2. Indeed, in some instances, micro-organisms that do not use CO2 as a major carbon source were shown to contain some form of Rubisco (Tabita et al., 2007). Thus, by the end of the twentieth century, the long-standing classification of Rubisco into only forms I and II was clearly outdated. In particular, many archaea were shown to contain a separate class of Rubisco, termed form III (Tabita, 1999; Watson et al., 1999). In addition, at about this time, it was noted (Tabita, 1999) that that the green sulphur phototrophic bacterium Chlorobium tepidum and the heterotroph Bacillus subtilis contained putative Rubisco genes that were clearly not of the form I and form II types, and shown to be distinct from form III as well. These new sequences were found to be in a class of their own, and classified as form IV Rubisco (Hanson and Tabita, 2001). Because the form IV proteins were incapable of catalysing RuBP-dependent CO2 fixation, the form IV proteins were further distinguished and termed Rubisco-like-proteins (RLPs), to set them apart from bona fide forms I, II, and III Rubisco. The RLPs are unable to catalyse CO2 fixation because of key substitutions of many essential active-site residues (Hanson and Tabita, 2001). The basic properties of Rubiscos and RLPs are described in Table 1.
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With respect to the function of the RLP, an RLP gene knockout strain of C. tepidum was shown to exhibit a pleiotropic phenotype, including the deposition of elemental sulphur into the surrounding media, as well as distinct effects on autotrophic growth (Hanson and Tabita, 2001). This was shown to be due to a specific effect on thiosulphate (and not sulphide) oxidation, leading to a general stress response. The stress response in C. tepidum was manifested by synthesis of stress-related proteins, including a thiol-specific hydroperoxidase and superoxide dismutase, resulting in resistance to high levels of hydrogen peroxide (Hanson and Tabita, 2003). In B. subtilis, the specific function of its RLP (or YkrW/MtnW) was identified where it was shown to participate in a methionine salvage pathway. In this and related organisms, RLP catalyses the enolization of the RuBP analogue, 2,3-diketo-5-methylthiopentyl-1-P (Ashida et al., 2003). Additional structure/function studies by Imker et al. (2007), with a related protein from Geobacillus kaustophilus, clearly illustrated the similarities of the enolase reactions catalysed by this RLP and Rubisco. Moreover, these authors determined the structure of the activated enolase and identified the base that catalyses proton abstraction.
In summary, phylogenetic analyses of Rubisco and RLP amino acid sequences indicate that there are at least three distinct lineages of bona fide Rubisco (forms I, II, and III) and six distinct clades of RLP molecules (form IV) (Fig. 3). Beyond studies with the YkrW group or ‘enolase’ RLPs from B. subtilis and G. kaustophilus, and physiological indications that the C. tepidum RLP is involved in some way with thiosulphate oxidation, representative RLPs from other clades have yet to be assigned a function. Furthermore, many of the RLP genes that encode proteins of unknown function were unable genetically to complement strains with knockouts in genes that encode RLP proteins of known function (J Singh, FR Tabita, unpublished results), suggesting that these unknown or undefined RLP proteins catalyse different reaction(s).
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The diversity and evolution of Rubisco and its homologue, the Rubisco-like protein |
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It is our contention that different molecular forms of Rubisco, from organisms that fix CO2 under highly divergent conditions in many distinct environments, may provide clues relative to the molecular basis for Rubisco substrate specificity and other kinetic properties, while also shedding light as to how the active site of this protein may have evolved from primordial ancestors. Certainly in light of efforts to improve the catalytic properties of Rubisco, studying its evolution ensures that one does not repeat experiments that nature has already performed. In a comprehensive analysis of all available microbial and plant Rubisco and RLP sequences, the different lineages were evaluated by various methods including phylogenetic reconstruction with multiple models on a more extensive sequence set, structural homology searches, gene conservation (both local and genome wide), concerted variation in active site substitution patterns, and others (Tabita et al., 2007). In all instances, it was concluded that the most likely scenario was that a form III Rubisco, arising within the Methanomicrobia, was the ultimate source of all Rubisco and RLP lineages (Fig. 4). Indeed, from these analyses, the euryarchaea appear to harbour the deepest branching Rubisco and RLP sequences and therefore are the most likely candidates for the evolutionary root of the Rubisco and RLP superfamily. We have thus proposed that a single transfer of RLP from a methanogenic euryarchaeon into an ancestor of the Firmicutes, Proteobacteria, and Chlorobia, with subsequent lateral transfer to the Chloroflexi, followed by gene losses could account for the distribution of most of the RLP lineages (Fig. 4). Likewise, lateral transfer of a form III Rubisco from a euryarchaeon to a common ancestor of Cyanobacteria and Proteobacteria, with eukaryote Rubiscos being acquired via subsequent endosymbiotic events, could account for the currently observed distribution of bona fide Rubisco lineages. From these considerations, the likely evolutionary development of the large subunit of Rubisco and RLP probably follows the model illustrated (Fig. 4). The scenario presented here is largely an extension of prior work by Delwiche and Palmer (1996) and Tabita (1999), but incorporates form III and form IV sequences that were not known at the time. In addition, a significant number of Rubisco and RLP sequences were recently reported from the global ocean sampling (GOS) expedition (Yooseph et al., 2007) and the authors purport to have discovered a number of new sub-families of Rubisco and RLP. However, our own examination of the same data suggests that this claim is overstated as will be detailed elsewhere.
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Recent structure/function studies |
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The archaeal form III Rubisco
It is clear from the discussion above that many distinct forms of Rubisco are found in nature and are available for structure–function studies. In many instances, these diverse proteins exhibit distinctive catalytic properties such that their study provides useful insights as to how all Rubisco eenzymes function (Tabita, 1999). For example, the discovery of the form III enzymes, obtained from organisms that never see molecular oxygen, offer tantalizing possibilities to learn more about how the active site of Rubisco might have evolved. This is especially relevant since it was found that several archaeal enzymes are highly sensitive to molecular oxygen and have extremely poor capabilities to discriminate between CO2 and O2 (Watson et al., 1999; Finn and Tabita, 2003; Kreel and Tabita, 2007), due in part to an extremely high affinity of these enzymes for O2 (Kreel and Tabita, 2007). In this recent study, the basis for the high affinity to O2 was sought, with the enzyme from Archaeoglobus fulgidus used as a model system. Bioinformatic and structural comparisons of all sequenced archaeal form III Rubiscos pointed towards unique residues that were positioned to interact with the active site. One of these residues, Met-295, was changed by site-directed mutagenesis and the resultant M295D protein was shown to recover from oxygen exposure much more effectively than the wild-type A. fulgidus enzyme. This was consistent with an increase in the Ko for oxygen from 5 µM in the wild-type enzyme to about 24 µM for the M295D enzyme. In addition, there was an unprecedented 3-fold increase in the substrate specificity factor (
) of the M295D enzyme compared with the wild-type protein. Structural analyses indicated that Met-295 was situated in a hydrophobic pocket created by residues along the active site and in close proximity to a highly conserved active-site residue, Arg-279 found in all other forms of Rubisco and shown to be necessary for substrate (RuBP) binding (Knight et al., 1990). In the wild-type A. fulgidus enzyme (RbcL2), there is no hydrogen bond to the Arg-279 residue (Fig. 5A). However, the model structure suggests that a mutation to an aspartate residue at the Met-295 position would allow for an ionic interaction between one of the hydroxyl side chains of the aspartate residue with one of the side chain nitrogen atoms of Arg-279 (Fig. 5B). Interestingly, there is definite hydrogen bonding to the equivalent Arg residue in all other form I and form II Rubisco structures; for example, originating from the oxygen atom of the carbonyl group of His-324 from the peptide backbone of the Synechococcus PCC 6301 enzyme (Kreel and Tabita, 2007).
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Further investigation into the above localized structural change led us to another amino acid, Ser-363, which was predicted to have similar effects on oxygen sensitivity of the A. fulgidus enzyme. Ser-363 is situated in what appears to be a hydrophobic pocket that surrounds one side of the active site (Fig. 5C). In addition, the model structure shows an interaction of the side chain of Ser-363 with two highly conserved and catalytically important residues, Gly-313 and Thr-314. Gly-313 and Thr-314, found in all forms of Rubisco, show no interactions with the amino acid residue equivalent to Ser-363 of RbcL2 in form I and form II enzymes. Thus, this unique interaction and positioning of Ser-363 in a key hydrophobic pocket of RbcL2, similar to Met-295, suggested that Ser-363 of RbcL2 might be a likely candidate for further investigation by site-directed mutagenesis. Ser-363 was thus changed to residues found in equivalent positions in form I and form II enzymes (alanine and isoleucine, respectively, and valine). Much like the M295D enzymes, the S363I and S363V enzymes retained much higher levels of activity (about 45–50%) when exposed to oxygen compared to the wild-type enzyme (about 10–15% activity) (Kreel and Tabita, 2007). Moreover, double mutants (M295DS363I or M295DS363V) exhibited an apparent additive effect and recovered nearly 90% activity after being exposed to oxygen. Recent studies further indicate that the Ko for the M295DS363I double mutant has been raised to over 400 µM, very close to values obtained for form I and form II Rubisco proteins (KE Kreel and FR Tabita, unpublished results). Clearly, the above studies point to the importance of hydrophobic regions for interactions with oxygen, with the oxygen-sensitive A. fulgidus form III enzyme providing a potential template for examining other forms of Rubisco.
Random mutagenesis and bioselection of mutant cyanobacterial form I Rubisco
Prokaryotic bioselection after random mutagenesis has now become feasible and adapted for the isolation of mutant forms of Rubisco (Smith and Tabita, 2003; Green et al., 2007). It is convenient to use Rhodobacter capsulatus, with its endogenous form I and form II Rubisco genes deleted, as a host strain for whatever prokaryotic Rubisco we wish to study (Finn and Tabita, 2003; Smith and Tabita, 2003, 2004). Both R. sphaeroides (Falcone and Tabita, 1991), but particularly R. capsulatus (Paoli et al., 1998) with its more rapid growth, especially under aerobic chemolithoautotrophic conditions, offers a host system with a built-in reductive pentose phosphate pathway for easy complementation under a variety of growth conditions, including conditions where CO2 may be used as the sole carbon source in both aerobic and anaerobic atmospheres. Recovery of mutants is also made simple by the fact that CO2 fixation is dispensable in these organisms and strains may be grown under aerobic heterotrophic conditions as with Escherichia coli. Clearly, growth at various levels and ratios of CO2 and O2 provides intriguing selective pressures to isolate potentially useful mutant forms of Rubisco, in an intracellular environment where Rubisco normally functions. This system thus far appears inherently more stable than artificial systems recently developed (Parikh et al., 2006), however, the potential for all such systems is great. Moreover, the R. capsulatus system offers a simple way to isolate specific mutations in either the large (RbcL/CbbL) or small subunit (RbcS/CbbS). This may be accomplished by using a two-plasmid system whereby specific mutations in either subunit may be obtained after mating mutated rbcL/cbbL or rbcS/cbbS genes into the Rubisco negative host containing the opposite, unmutagenized gene carried on a separate plasmid (Fig. 6). As illustrated for cyanobacterial Rubisco (Fig. 6), it was found that expression of rbcL or rbcS on separate plasmids results in the reconstitution of an active form I L8S8 holoenzyme in vivo from newly synthesized large and small subunits. Thus, specific alterations on each subunit may be assessed after normal protein assembly in E.coli, followed by purification of the recombinant protein as with the one-plasmid system.
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An important hyrophobic pocket identified upon random mutagenesis and bioselection
Several interesting mutant cyanobacterial (Synechococcus sp. strain PCC 6301) rbcL and rbcS genes have been isolated upon error-prone random mutagenesis using the R. capsulatus system (Smith and Tabita, 2003, 2004; SS Scott and FR Tabita, unpublished results). Of particular interest were residues that were distal to the active site that were localized at monomer–monomer or dimer–dimer interfaces and appeared to influence important kinetic constants, particularly the Kc. One of these mutant proteins, D103V, was shown not to be able to support growth in R. capsulatus SBI/II–, presumably by virtue of causing a rise in the Kc value (Smith and Tabita, 2003). Asp-103 is localized on the surface of one monomer of a dimeric pair, where it contacts Ser-367 of a monomer from a second dimeric pair of large subunits. To gain an understanding as to how Asp-103, which is far from the active site, might influence catalysis, an attempt was made to isolate specific internal suppressor mutations which, it was surmised, would overcome the effect of D103V, provide insights into residues that might interact with Asp-103, and subsequently allow growth in the R. capsulatus SBI/II– background. Over several years, multiple investigators in our laboratory were all able to isolate a single suppressor mutation that allowed growth in the R. capsulatus system. This suppressor or compensatory protein, a D103VA375V double mutant, was found to possess an improved Kc. Furthermore, it appears that both Asp-103 and Ala-375 exert their influence on Ser-376, an important active-site residue required for binding the P2 phosphate of the substrate ribulose 1,5-bisphospate (S Satagopan et al., unpublished results). Most importantly, however, Ala-375 was subsequently shown to be localized in an interesting hydrophobic region near the active site. Indeed, all forms of Rubisco, including form I (Andersson, 1996, form II (Schneider et al., 1990), and form III Rubisco (Kitano et al., 2001) contain this hydrophobic pocket (Fig. 7).
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Why might this hydrophobic region be important? Ala-375 of the Synechococcus form I Rubisco is equivalent to Ser-363 of the A. fulgidus enzyme. As discussed above, Ser-363 of the archaeal A. fulgidus enzyme appears to play some role in the ability of this enzyme to interact with oxygen (Kreel and Tabita, 2007), and this residue, along with Met-295, appears able to influence the Ko. Further studies with the equivalent Ala-375 residue of form I Rubisco have also recently shown that this residue influences the ability of the cyanobacterial enzyme to support aerobic chemolithoautotrophic growth in the R. capsulatus system. Moreover, as expected, this residue also directly affects the Ko value (S Satagopan et al., unpublished results).
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Conclusions |
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TopAbstractIntroductionThe different forms of...Phylogenetic relationships in...The diversity and evolution...Recent structure/function...ConclusionsReferences |
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It is apparent that Rubisco, and its homologue, the Rubisco-like protein, share an interesting history and undoubtedly present a classic example of divergent evolution. The different forms of Rubisco found in nature, some of which must function in very extreme or inhospitable environments, almost by definition, have made structural adaptations to allow catalysis to occur. Investigating these structural adaptations is very useful, as such studies provide a framework for understanding more about Rubisco structure and function in general.
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Acknowledgements |
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This work was supported by grant GM24497 from the National Institutes of Health and grants DE-FG02-01ER63241 and DE-FG02-91ER20033 from the offices of Biological and Environmental Research (Genomics: GTL Program) and Energy Biosciences, respectively, of the US Department of Energy.
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References |
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TopAbstractIntroductionThe different forms of...Phylogenetic relationships in...The diversity and evolution...Recent structure/function...ConclusionsReferences |
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Andersson I. Large structures at high resolution: the 1.6 Å crystal structure of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase complexed with 2-carboxyarabinitol bisphosphate. Journal of Moecular Biology (1996) 259:160–174.[CrossRef]
Andersson I, Knight S, Schneider G, Lindqvist Y, Lundqvist T, Branden C-I, Lorimer GH. Crystal structure of the active site of ribulose-bisphosphate carboxylase. Nature (1989) 337:229–234.[CrossRef]
Andersson I, Taylor TC. Structural framework for catalysis and regulation in ribulose-1,5-bisphosphate carboxylase/oxygenase. Archives of Biochemistry and Biophysics (2003) 414:130–140.[CrossRef][Web of Science][Medline]
Andrews TJ. Catalysis by cyanobacterial ribulose bisphosphate carboxylase large subunits in the complete absence of small subunits. Journal of Biological Chemistry (1988) 263:12213–12219.
Ashida H, Saito Y, Kojima C, Kobayashi K, Ogasawara N, Yokota A. A functional link between rubisco-like protein of Bacillus and photosynthetic rubisco. Science (2003) 302:286–290.
Cleland WW, Andrews JT, Gutteridge S, Hartman FC, Lorimer GH. Mechanism of Rubisco: the carbamate as general base. Chemical Reviews (1998) 98:549–561.[CrossRef][Web of Science][Medline]
Delwiche CF, Palmer JD. Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Molecular and Biological Evolution (1996) 13:873–882.
Falcone DL, Tabita FR. Expression of endogenous and foreign ribulose 1,5-bisphosphate carboxylase-oxygenase (Rubisco) genes in a Rubisco deletion mutant of Rhodobacter sphaeroides. Journal of Bacteriology (1991) 173:2099–2108.
Finn MW, Tabita FR. Synthesis of catalytically active form III ribulose 1,5-bisphosphate carboxylase/oxygenase in archaea. Journal of Bacteriology (2003) 185:3049–3059.
Fuchs G, Lange S, Rude E, Schaefer S, Schauder R, Scholtz R, Stupperich E. Autotrophic CO2 fixation in chemotrophic anaerobic bacteria. In: Microbial growth on C1 compounds—Van Verseveld HW, Duine JA, eds. (1987) Dordrecht, The Netherlands: Martinus Nijhoff. 39–43.
Green DM, Whitney SM, Matsumura I. Artificially evolved PCC6301 Rubisco variants exhibit improvements in folding and catalytic efficiency. Biochemical Journal (2007) 404:517–524.[CrossRef][Web of Science][Medline]
Hanson TE, Tabita FR. 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. Proceedings of the National Academy of Sciences, USA (2001) 98:4397–4402.
Hanson TE, Tabita FR. Insights into the stress response and sulfur metabolism revealed by proteome analysis of a Chlorobium tepidum mutant lacking the Rubisco-like protein. Photosynthesis Research (2003) 78:231–48.[CrossRef][Web of Science][Medline]
Hartman FC, Harpel MR. Structure, function, regulation and assembly of D-ribulose-1,5-bisphosphate carboxylase/oxygenase. Annual Review of Biochemistry (1994) 63:197–234.[CrossRef][Web of Science][Medline]
Imker HJ, Fedorov AA, Fedorov EV, Almo SC, Gerlt JA. Mechanistic diversity in the Rubisco superfamily: the ‘enolase’ in the methionine salvage pathway in Geobacillus kaustophilus. Biochemistry (2007) 46:4077–4089.[CrossRef][Web of Science][Medline]
Kitano K, Maeda N, Fukui T, Atomi H, Imanaka T, Miki K. Crystal structure of a novel-type archaeal rubisco with pentagonal symmetry. Structure (2001) 9:473–481.[Medline]
Kreel NE, Tabita FR. Substitutions at methionine 295 of Archaeoglobus fulgidus ribulose-1,5-bisphosphate carboxylase/oxygenase affect oxygen binding and CO2/O2 specificity. Journal of Biological Chemistry (2007) 282:1341–1351.
Knight S, Andersson I, Branden CI. Crystallographic analysis of ribulose 1,5-bisphosphate carboxylase from spinach at 2.4 Å resolution. Subunit interactions and active site. Journal of Molecular Biology (1990) 215:113–160.[CrossRef][Web of Science][Medline]
Lee B, Berka R, Tabita FR. Mutations in the small subunit of cyanobacterial ribulose bisphosphate carboxylase/oxygenase that modulate interactions with large subunits. Journal of Biological Chemistry (1991a) 266:7417–7422.
Lee B, Read BA, Tabita FR. Catalytic properties of recombinant octameric, hexadecameric, and heterologous cyanobacterial/bacterial ribulose-1,5 bisphosphate carboxylase/oxygenase. Archives of Biochemistry and Biophysics (1991b) 291:263–269.[CrossRef][Web of Science][Medline]
Lee B, Tabita FR. Purification of recombinant ribulose-1,5-bisphosphate carboxylase/oxygenase large subunits suitable for reconstitution and assembly of active L8S8 enzyme. Biochemistry (1990) 29:9352–9357.[CrossRef][Web of Science][Medline]
Li H, Sawaya MR, Tabita FR, Eisenberg D. Crystal structure of a novel Rubisco-like protein from the green sulfur bacterium Chlorobium tepidum. Structure (2005) 13:779–789.[Medline]
Parikh MR, Greene DH, Woods KK, Matsumuara I. Directed evolution of Rubisco hypermorphs through genetic selection in engineered E. coli. Protein Engineering Design and Selection (2006) 19:113–119.
Paoli GC, Vichivanives P, Tabita FR. Physiological control and cbb gene regulation in Rhodobacter capsulatus. Journal of Bacteriology (1998) 180:4258–4269.
Portis AR Jr. Regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase activity. Annual Review of Plant Physiology (1992) 43:415–437.[CrossRef][Web of Science]
Read BA, Tabita FR. Amino acid substitutions in the small subunit of ribulose-1,5carboxylase/oxygense that influence catalytic activity of the holoenzyme. Biochemistry (1992a) 31:519–525.[CrossRef][Web of Science][Medline]
Read BA, Tabita FR. A hybrid ribulose bisphosphate carboxylase/oxygenase enzyme exhibiting a substantial increase in substrate specificity factor. Biochemistry (1992b) 31:5554–5560.
Schneider G, Lindqvist Y, Branden CI. RUBISCO: structure and mechanism. Annual Review of Biophysical and Biomolecular Structure (1992) 21:119–143.[CrossRef][Web of Science][Medline]
Schneider G, Lindqvist Y, Lundqvist T. Crystallographic refinement and structure of ribulose-1,5-bisphosphate carboxylase from Rhodospirillum rubrum at 1.7 A resolution. Journal of Molecular Biology (1990) 211:989–1008.[CrossRef][Web of Science][Medline]
Smith SA, Tabita FR. Positive and negative bioselection of mutant forms of prokaryotic (cyanobacterial) ribulose-1, 5-bisphosphate carboxylase/oxygenase. Journal of Molecular Biology (2003) 331:557–569.[CrossRef][Web of Science][Medline]
Smith SA, Tabita FR. Glycine 176 affects catalytic properties and stability of the Synechococcus sp. strain PCC 6301 ribulose 1,5-bisphosphate carboxylase/oxygenase. Journal of Biological Chemistry (2004) 279:25632–25637.
Spreitzer RJ. Questions about the complexity of chloroplast ribulose-1, 5-bisphosphate carboxylase/oxygenase. Photosynthesis Research (1999) 60:29–42.[CrossRef][Web of Science]
Spreitzer RJ, Salvucci ME. Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annual Review of Plant Biology (2002) 53:449–475.[CrossRef][Medline]
Spreitzer RJ, Srinivasa RP, Satagopan S. Phylogenetic engineering at an interface between large and small subunits imparts land-plant kinetic properties to algal Rubisco. Proceedings of the National Academy of Sciences, USA (2005) 102:17225–17230.
Tabita FR. Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a different perspective. Photosynthesis Research (1999) 60:1–28.[CrossRef][Web of Science]
Tabita FR, Hanson TE, Li H, Satagopan S, Singh J, Chan S. Function, evolution, and structure of the Rubisco-like proteins and their Rubisco homologs. Microbiology and Molecular Biology Reviews (2007) 71:576–599.
Tabita FR, McFadden BA. D-Ribulose 1, 5-diphosphate carboxylase from Rhodospirillum rubrum. Il. Quaternary structure, composition, catalytic and immunological properties. Journal of Biological Chemistry (1974) 249:3459–3464.
Watson GM, Yu JP, Tabita FR. Unusual ribulose 1,5-bisphosphate carboxylase/oxygenase of anoxic archaea. Journal of Bacteriology (1999) 181:1569–1575.
Yooseph S, Sutton G, Rusch DB, et al. The Sorcerer II global ocean sampling expedition: expanding the universe of protein families. PLoS Biology (2007) 5:e16.[CrossRef][Medline]
Yoon KS, Hanson TE, Gibson JL, Tabita FR. Autotrophic CO2 metabolism. In: Encyclopedia of microbiology—Lederburg J, ed. (2000) 2nd edn. San Diego, CA: Academic Press Inc. 349–358.
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