Skip to main content
NCBI home page
Microbial Cell Factories logoLink to Microbial Cell Factories
. 2004 Jun 2;3:7. doi: 10.1186/1475-2859-3-7

Potential use of sugar binding proteins in reactors for regeneration of CO2 fixation acceptor D-Ribulose-1,5-bisphosphate

Sourav Mahato 1, Debojyoti De 1, Debajyoti Dutta 1, Moloy Kundu 1, Sumana Bhattacharya 2, Marc T Schiavone 2, Sanjoy K Bhattacharya 3,✉
PMCID: PMC421735  PMID: 15175111

Abstract

Sugar binding proteins and binders of intermediate sugar metabolites derived from microbes are increasingly being used as reagents in new and expanding areas of biotechnology. The fixation of carbon dioxide at emission source has recently emerged as a technology with potentially significant implications for environmental biotechnology. Carbon dioxide is fixed onto a five carbon sugar D-ribulose-1,5-bisphosphate. We present a review of enzymatic and non-enzymatic binding proteins, for 3-phosphoglycerate (3PGA), 3-phosphoglyceraldehyde (3PGAL), dihydroxyacetone phosphate (DHAP), xylulose-5-phosphate (X5P) and ribulose-1,5-bisphosphate (RuBP) which could be potentially used in reactors regenerating RuBP from 3PGA. A series of reactors combined in a linear fashion has been previously shown to convert 3-PGA, (the product of fixed CO2 on RuBP as starting material) into RuBP (Bhattacharya et al., 2004; Bhattacharya, 2001). This was the basis for designing reactors harboring enzyme complexes/mixtures instead of linear combination of single-enzyme reactors for conversion of 3PGA into RuBP. Specific sugars in such enzyme-complex harboring reactors requires removal at key steps and fed to different reactors necessitating reversible sugar binders. In this review we present an account of existing microbial sugar binding proteins and their potential utility in these operations.

Review

Rapid industrialization has led to a dramatically accelerated consumption of fossil fuels with a consequent increase in atmospheric levels of the greenhouse gas carbon dioxide (CO2). This sustained increase of atmospheric CO2 has already initiated a chain of events with negative ecological consequences [1-3]. Failure to reduce these greenhouse gas emissions will have a catastrophic impact upon both the environment and the economy on a global scale [4,5]. The reduction has to be brought about by global concerted effort by all countries in order to be effective and meaningful.

At one end of the spectrum – that of generation and utilization of energy resulting in generation of carbon dioxide – hydrocarbons serve as intermediaries for energy storage. Hydrocarbons are not energy by themselves but store energy in their bonds, which is released during combustion. They are thus intermediates for obtaining stored bond energy within them and carbon dioxide is emitted as a consequence of combustion to extract this stored energy. In recent times hydrogen has received renewed attention as the potential replacement for hydrocarbons [6-10]. However, hydrogen too is an intermediary for obtaining stored bond energy. Recent reports suggest that hydrogen as intermediary may not be entirely free from problems. Also, the problems from use of hydrogen as fuel are yet to be fully realized or foreseen [11,12]. In all these endeavors a key question, that whether the hydrocarbons will be still retained as intermediaries in energy utilization and the problem of air pollution caused as a result of their combustion can be technologically ameliorated, has not been looked in as much detail as perhaps it should have been. This can possibly be achieved by contained handling of carbon dioxide. The contained handling and fixation of CO2 can be achieved biotechnologically, chemically or by a combination of both.

Sugar binding proteins derived from microbial and other sources have been used for various applications such as diagnostics and affinity purification [13,14], however they have not been used in environmental biotechnological applications. The possibility of their potential application in environmental biotechnology and review of a few potential candidates is presented here.

The methods in environmental biotechnology that enables efficient capture [15] and fixation of CO2 at emission source/site into concatenated carbon compounds has been pioneered by our group [16-19]. The first part in the biocatalytic carbon dioxide fixation is the capture of gaseous CO2. We have pioneered novel reactors employing immobilized carbonic anhydrase for this purpose [15]. Subsequent to capture the carbon dioxide becomes solublized (as carbonic acid or bicarbonate). After adjustment of pH using controllers and pH-stat the solution is fed to immobilized Rubisco reactors [18] where acceptor D-Ribulose-1,5-bisphosphate (RuBP) after CO2 fixation is converted into 3-phosphoglycerate [16,17]. However, inasmuch as the recycling of acceptor RuBP is central to continuous CO2 fixation, we have invented a novel scheme (Figure 1), which proceeds with no loss of CO2 (unlike cellular biochemical systems) in 11 steps in a series of bioreactors [20]. This scheme is very different from generation of RuBP from D-glucose for start-up process [21] and employing 11 steps in different reactors requiring large volume and weight. The linear combination of reactors with large volume and weight are unsuitable for use with mobile CO2 emitters leaving only the stationary source of emission to be controlled using this technology [17]. To circumvent these problems we have devised a new scheme presented in Figure 2[22]. Based on this scheme, we have designed enzymes as functionally interacting complexes/interactomes or successive conversion in radial flow with layers of uniformly oriented enzymes in concentric circle with axial collection flow system for three enzymes in first reactor for the scheme presented in Figure 2. The four reactors harboring enzymatic complexes/mixtures replace the current 11 reactors. This leads to a faster conversion rate and requires less volume and material weight. However, 4 sugar moieties [3-phosphoglyceraldehyde (3PGAL), Dihydroxyacetone phosphate (DHAP), Xylulose-5-phosphate (X5P) and Ribulose-1, 5-bisphosphate (RuBP)] must be separated at four key steps, as illustrated in Figure 2. In figure 2, using four symbols with solid for bound state and empty for released state, for potential binders: plus for 3PGA, circle for DHAP, cylinder for X5P and box for RuBP, the possible place for utility of these binders have been depicted. In the course of this review, we will consider the availability of enzymatic proteins and non-enzymatic proteins that would be potentially useful as specific binders for these sugar molecules. With a recombinant mutant enzyme we illustrate that such an approach has potential to be used as an in-situ reversible binding matrix for sugar binding and release.

Figure 1.

Figure 1

Open in a new tab

Scheme for generation of D-ribulose-1,5-bisphosphate (RuBP) from 3-phosphoglycerate (3PGA) obtained from fixation of CO2 on RuBP. The continuous regeneration of RuBP in this scheme enables continuous fixation of CO2 at stationary emission sites.

Figure 2.

Figure 2

Open in a new tab

An alternate arrangement of enzymes in the scheme outlined in Fig. 1. This schemes harbors four reactors with indicated enzyme complexes enabling internal channeling, greatly reduces volume and weight for regenerating reactors with faster overall conversion rate to RuBP starting with 3PGA making the system compatible for application in mobile devices in addition to stationary emitters. The reactors may use the sugar binding entities at indicated positions, the hollow and solid symbols represent binding and release phase of the binding-molecules, the plus, circle, cylinder and box are symbols for 3PGA, DHAP, X5P and RuBP binders respectively.

Potential utilizable sugar binding proteins in RuBP regeneration

Three categories of binding proteins can be potentially employed for differential absorption of sugars and for subsequent elution and feeding the reactors downstream in conversion cascade. These are: mutant enzymatic proteins that retain the ability of binding but completely lack any catalytic activity, lectins or proteins of non-immunogenic origin [23] having more than one binding site for the sugar (in nature they cause agglutination of due to sugar binding at multiple sites) and mutant or wild type receptors that binds sugars but are incapable of eliciting further biological activities. The desirable proteins in all these categories are those for which binding affinity is high in a condition close to pH of the emanating solution from the reactor and other conditions for reactor effluent, ability to bind reversibly with respect to some simple but easily manipulable physicochemical parameter (such as temperature, pH, salt concentration), and the ability to be easily attached to a matrix using simple chemistry without loss of binding ability and a long shelf life.

We undertook this review because, although the comprehensive information on a large number of enzymes have been accumulated in BRENDA database [24,25], but the systematic information on their mutants is lacking and non-enzymatic binders of sugar ligands are not identified / listed in the database.

Proteins that bind 3-phosphoglycerate/3-phosphoglyceraldehye

Both enzymatic and non-enzymatic proteins bind these sugar entities. A number of mutants of many enzymes that bind to either 3-phosphoglycerate or 3-phosphoglyceraldehyde are also known, for example, Phosphoglyceromutase (EC 5.4.2.1), Enolase (EC 4.2.1.11), Mannosyl-3-phosphoglycerate phosphatase (EC 3.1.3.70), Mannosyl-3-phosphoglycerate synthase (EC 2.4.1.217), Phosphoglycerate kinase, (EC 2.7.2.3), Bisphosphoglycerate mutase (EC 5.4.2.4), 2,3-bisphosphoglycerate-independent phosphoglycerate mutase (EC 5.4.2.1), D-3-phosphoglycerate dehydrogenase 2 (EC 1.1.1.95), Cyclic 2,3-diphosphoglycerate-synthetase, Phosphoglycerate dehydrogenase, Transketolase, and Triosephosphate isomerase, BRENDA database shows only three enzymes: Phosphoglycerate dehydrogenase, Mannosyl-3-phosphoglycerate synthase and Phosphoglycerate kinase. A number of mutants of enzymes that binds 3-phosphoglycerate and shows some change in enzymatic activity or kinetic parameters are listed in Table 1. Many of these proteins are reported to retain ligand binding ability with varying degree of loss in catalytic ability (inactive mutants are in bold face), the non-enzymatic protein that also has been reported in literature has been placed towards the bottom part of Table 1. The proteins which retain binding ability but with complete loss in catalytic activity are the ones which warrant further investigation in batch and continuous processes for exploring their suitability as binding proteins in continuous RuBP regenerating reactors (Figure 2). A number of non-enzymatic protein summarized in Table 1 also warrant further exploration. The only binding entity of significance for 3-phosphoglyceraldehyde is 3-phosphoglyceraldehyde dehydrogenase (EC 1.2.1.12) and has not been reviewed.

Table 1.

Proteins that bind 3-phosphoglycerate

Source Mutation Remarks References
Enzymatic proteins
Phosphoglycerate mutase 1 (EC 5.4.2.1)
E. coli Glu327 Lower Vmax 26
S. cerevisiae Gly13Ser 2-fold increase in activity 27
S. cerevisiae His181Ala 11-fold increase in the Km 28
S. cerevisiae C-terminal 7 res. Deletion Loss of activity, retention of ligand binding 29
B. stearothermophilus S62A Loss of activity, retention of ligand binding 30
S. pombe H163Q Reduced mutase and phosphatase activities 31
E. coli R257A 11-fold increase in Vmax 26
E. coli R307A 700-fold decrease in Vmax 26
Enolase (EC 4.2.1.11)
S. cerrevisiae S39A Loss of over 90% activity 32
S. cerrevisiae H157A, H159A Loss of over 90% activity 33
S. cerrevisiae H159A Loss of over 98% activity 34
Escherichia coli N341D Loss of catalytic activity 35
S. cerrevisiae Gcr1-1 mutation 20-fold reduction in activity 36
Phosphoglycerate kinase, (EC 2.7.2.3)
S. cerrevisiae H388G Reduced kcat and Km 37
S. cerrevisiae R168K Increase in Km 38
S. cerrevisiae R168M Increase in Km 38
S. cerrevisiae H62D Increase in Km and Vmax 39
S. cerrevisiae D372N reduction in Vmax by 10-folds 40
S. cerrevisiae R38A Complete loss of activity 41
S. cerrevisiae R38Q Complete loss of activity 41
S. cerrevisiae R65Q Increase in Kd, decrease in Km 42
S. cerrevisiae R65A Increase in Kd, decrease in Km 42
S. cerrevisiae R65S Increase in Kd, decrease in Km 42
S. cerrevisiae F194W (and F194L) decrease in Km, Vmax 43
S. cerrevisiae R203P Reduction in kcat 44
Bisphosphoglycerate mutase (EC 5.4.2.4)
S. cerevisiae H181A Decrease in kcat 28
Transketolase
S. cerevisiae E418Q, E418A 98–99% reduction in activity 45
S. cerevisiae E418A E418 is essential for catalytic activity 45
S. cerevisiae H103A, H103N and H103F 95–99.9% reduced activity 46
S. cerevisiae E162A (G) Impaired catalytic activity and binding 47
S. cerevisiae D382N(A) Impaired catalytic activity and binding 47
S. cerevisiae H481A/S/G 98.5% reduced specific activity 48
S. cerevisiae N477A 1000-fold decrease in kcat/Km 49
S. cerevisiae H263A Reduced activity 50
D-3-phosphoglycerate dehydrogenase 2 (EC 1.1.1.95)
Escherichia coli L-Serine Reduced activity 51
Triosephosphate isomerase
Kluyveromyces lactis Kltpi1 mutant Loss of activity 52
Plasmodium falciparum Y74G Reduced stability 53
Plasmodium falciparum C13D 7-fold reduction in activity 54
Trypanosoma brucei W12F Reduced stability 55
Leishmania mexicana E65Q Increased stability 56
K. lactis DeltaTPI1 mutants Complete loss of activity 57
Vibrio marinus A238S mutant Reduced activity 58
Trypanosoma brucei C14L Reduced stability and altered kinetics 59
Saccharomyces cerevisiae K12R Vmax reduced by factor of 180 60
Saccharomyces cerevisiae K12H No catalytic activity at neutral pH 60
Saccharomyces cerevisiae E165D 100-fold loss in catalytic activity 61
Salmonella typhimurium R179L Reduction in binding affinity 62
Trypanosoma brucei H47N Reduced stability 63
Escherechia coli E165D 100-fold reduction in specific activity 64
Escherechia coli N78D Lower kcat 65
Saccharomyces cerevisiae H95G 400-fold decrease in catalytic activity 66
Non-enzymatic proteins
Phosphoglycerate transporter protein
Salmonella typhimurium 67
Salmonella typhimurium 68
Bacillus cereus 69
Bacillus anthracis 70
Salmonella typhi 71
Salmonella typhi 72
Histone like DNA-binding protein (HU homolog)
Mycobacterium leprae 73
Mycobacterium leprae 74
Mycobacterium tuberculosis 75
Mycobacterium tuberculosis 76
40S ribosomal protein SA (P40)
Chlorohydra viridissima 77
Strongylocentrotus purpuratus 78
Tripneustes gratilla 79
Urechis caupo 79
Laminin-binding protein
Streptococcus agalactiae 80
Streptococcus agalactiae 81
Streptococcus pyogenes 82
Streptococcus agalactiae 83
Streptococcus agalactiae 83
Streptococcus agalactiae 83
Serine-rich protein (TYE7)
Saccharomyces cerevisiae 84
Saccharomyces cerevisiae 85
Open in a new tab

Proteins that bind dihydroxyacetone phosphate

Several enzymes: dihydroxyacetone phosphate acyltransferase, Glycerol-3-phosphate dehydrogenase, Aldolase A, fructose-bisphosphatase, Aldolase B, fructose-bisphosphatase, L-aspartate oxidase, Quinolinate synthetase A, Dihydroxyacetone kinase 1 (Glycerone kinase 1), Glycerol-3-phosphate acyltransferase, NAD(P)H-dependent dihydroxyacetone-phosphate reductase, Dihydroxyacetone phosphate acyltransferase, Alkyl-dihydroxyacetonephosphate synthase, Dihydroxyacetone kinase isoenzyme I, Alpha-glycerophosphate oxidase and Triose phosphate isomerase binds DHAP (Table 2), however, BRENDA shows only four of these proteins, glycerol-3-phosphate dehydrogenase (EC 1.1.1.8), acylglycerone-phosphate reductase (EC 1.1.1.101), glycerone-phosphate O-acyltransferase (EC 2.3.1.42) and alkylglycerone-phosphate synthase (2.5.1.26). The mutants of enzymes with no chemical conversion ability but with high affinity for binding dihydroxyacetone phosphate but very low affinity for other proteins and reversible binding with respect to temperature, salt or pH are desirable properties for the binders.

Table 2.

Proteins that bind Dihydroxyacetone phosphate

Source Organism Mutation Remarks References
Enzymatic proteins
Glyceraldehyde-3-phosphate dehydrogenase
S. cerevisiae ald5 mutant Higher catalytic activity 86
S. cerevisiae gpd2 delta mutant Improved ethanol production 87
Dihydroxyacetone kinase 1 (Glycerone kinase 1)
Hansenula polymorpha per6-210 mutant Lacks enzymatic activity 88
Glycerol-3-phosphate acyltransferase
Escherichia coli G1045A Reduced specific activity, increased Km 89
Escherichia coli D311E Reduced catalytic activity 90
S. cerevisiae tpa1 mutant 2-fold decrease in activity 91
NAD(P)H-dependent dihydroxyacetone-phosphate reductase
Escherichia coli Q15R/K, W37R/K Inactive with NADP+ 92
Escherichia coli Q15K-W37R and Q15R-W37R 30-fold higher Km for NADP+ 92
Escherichia coli gamma-R97Q 10-fold increased Km for NAD 93
Escherichia coli G252A Reverse transhydrogenation activity 94
Pseudomonas fluorescens K295A and K295M 104–106-fold lower turnover 95
M. thermoautotrophicum R11K and R136K Decreased Km 96
Alkyl-dihydroxyacetonephosphate synthase
Hansenula polymorpha ts6 and ts44 mutant Peroxisomes absent 97
Dihydroxyacetone phosphate acyltransferase
Corynebacterium glutamicum S187C Reduced enzymatic activity 98
Triose phosphate isomerase
Kluyveromyces lactis Kltpi1 mutant Loss of enzymatic activity 52
Plasmodium falciparum Y74G Reduced stability 53, 54
Plasmodium falciparum C13D 7-fold reduction in the enzymatic activity 53, 54
Trypanosoma brucei W12F Reduced stability 55
Leishmania mexicana E65Q Increased stability 56
K. lactis DeltaTPI1 mutants Complete loss of activity 57
Bacillus stearothermophilus N12H Prevent deamidation at high temperature 99
Vibrio marinus A238S catalytic activity reduced 58
Trypanosoma brucei C14L Reduced stability and altered kinetics 59
Saccharomyces cerevisiae K12R Vmax reduced by a factor of 180, Km elevated 60
Saccharomyces cerevisiae K12H No catalytic activity at neutral pH 60
Saccharomyces cerevisiae E165D 1000-fold reduction in catalytic activity 61
Salmonella typhimurium R179L Reduction in binding affinity 62
Trypanosoma brucei H47N Reduced stability 63
Escherechia coli E165D 1000-fold reduction in specific activity 64
Escherechia coli N78D Lowered Kcat 65
Saccharomyces cerevisiae H95G 400-fold decrease in catalytic activity 66
Non-enzymatic protein
DHAP transporter
Saccharomyces cerevisiae 100
mycoplasma mycoides 101
E. coli 102
Pseudomonas aeruginosa 103
Escherichia coli 104
Escherichia coli 105
Escherichia coli 106
Escherichia coli 107
Open in a new tab

Proteins binding xylulose-5-phosphate

As shown in Table 3 several enzymatic proteins binds to xylulose-5-phosphate. Xylulose-5-phosphate phosphoketolase, Dihydroxyacetone synthase, xylulose kinase, Protein phosphatase 2A B alpha isoform, Xylulose 5-phosphate-activated protein phosphatase, 1-deoxy-D-xylulose 5-phosphate reductoisomerase, 1-deoxy-D-xylulose 5-phosphate synthase 1 and 2 are examples of such enzymes. The non-enzymatic xylulose-5-phosphate binders are shown in the bottom part of Table 3. BRENDA database shows following five proteins, 1-deoxy-D-xylulose-5-phosphate reductoisomerase (EC 1.1.1.267), formaldehyde transketolase (EC 2.2.1.3), 1-deoxy-D-xylulose 5-phosphate synthase (EC 2.2.1.7), Phosphoketolase (EC 4.1.2.9), Ribulose-phosphate 3-epimerase (EC 5.1.3.1).

Table 3.

Proteins that bind Xylulose-5-phosphate

Source Mutation Remarks References
Enzymatic proteins
1-deoxy-D-xylulose 5-phosphate reductoisomerase
Escherichia coli E231K 0.24% wild-type kcat 108
Escherichia coli H153Q 3.5-fold increase in Km 108
Escherichia coli H209Q 7.6-fold increase in Km 108
Escherichia coli H257Q 19-fold increase in Km 108
xylulose kinase
Escherichia coli XylB- mutant Lack of growth on xylitol 109
Dihydroxyacetone synthase
Hansenula polymorpha Pex1–6(ts) Peroxisome-deficient 110
Hansenula polymorpha Deltapex14 Lack normal peroxisomes 111
Non-enzymatic proteins
Xylulose-5-phosphate receptor
Mycobacterium tuberculosis 112
Xylulose-5-phosphate trasporter
Arabidopsis sp. 113
Open in a new tab

Proteins binding D-Ribulose-1,5-bisphosphate

A number of Ribulose-1,5-bisphosphate and metabolizing enzymes such as Ribulose phosphate kinase and their mutants binds D-ribulose-1,5-bisphosphate. The RuBP binding entities devoid of any enzymatic activities are very valuable in reactors necessitating extraction and separation of RuBP from other sugar compounds (Table 4). Very few non-enzymatic proteins bind RuBP and none of them are microbial sources, and hence have not been incorporated in this review, Rubisco associated protein from soybean is one of them, that show significant RuBP binding [137].

Table 4.

Enzymes that bind D-Ribulose-1,5-bisphosphate

Source organism Mutation Remarks References
Rubisco
Chamydomonas reinhardtii C256F, K258R, L265V 85% decrease in Catalytic efficiency (Vmax/Km) 114
Chamydomonas reinhardtii G54V 83% decrease in the carboxylation-Vmax 115
Anacystis nidulans L339F, A340L, S341M Decrease in Kcat and (Vmax/Km) by 90%and 36.3% respectively 116
Anacystis nidulans T342I, K343L Decrease in Kcat and (Vmax/Km) by 90%and 36.3% respectively 116
Anacystis nidulans T342I Decrease in Kcat and (Vmax/Km) 40.5%and 40.5% respectively 116
Anacystis nidulans K343L Decrease in Kcat and (Vmax/Km) 48.1%and 18.5% respectively 116
Anacystis nidulans V346Y, D347H, L348T Inactive 116
Anacystis nidulans L326I Decrease in Kcat and (Vmax/Km) 54.4%and 34.2% respectively 116
Anacystis nidulans S328A Decrease in Kcat and (Vmax/Km) 5.6%and 41.5% respectively 116
Anacystis nidulans N123H 16.5% decrease in Kcat 116
Anacystis nidulans L332M, L332I >65% decrease in carboxylase but not in oxygenase activity 117
Anacystis nidulans >65% decrease in carboxylase but not in oxygenase activity 117
Anacystis nidulans L332V 67% decrease in specificity factor (CO2/O2) 117
Anacystis nidulans L332T 67% decrease in specificity factor (CO2/O2) 117
Anacystis nidulans L332A >65% decrease in specificity and carboxylase activity 117
Rhodospirillum rubrum deleation of F327 99.5% decrease in carboxylase activity 118
Rhodospirillum rubrum F327L Increase in Km (RuBP) 118
Rhodospirillum rubrum F327V Increase in Km (RuBP) 118
Rhodospirillum rubrum F327A Increase in Km (RuBP) 118
Rhodospirillum rubrum F327G 165-fold increase in Km (RuBP) 118
Rhodospirillum rubrum N111G Km(RuBP), kcat are 320 fold increased and 88-fold decreased 119
Rhodospirillum rubrum N111L Mutant show a very low carboxylase activity 119
Rhodospirillum rubrum N111Q Mutant show a very low carboxylase activity 119
Rhodospirillum rubrum N111B Mutant show a very low carboxylase activity 119
Synechococcus sp.PCC6301 I87V Mutant show a very low carboxylase activity (kcat = 35%) 120
Synechococcus sp.PCC6301 R88K Mutant show a very low carboxylase activity (kcat = 35%) 120
Synechococcus sp.PCC6301 G91V Mutant show a very low carboxylase activity (kcat = 35%) 120
Synechococcus sp.PCC6301 F92L Mutant show a very low carboxylase activity (kcat = 35%) 120
Synechococcus sp.PCC6803 C172A 40–60% decline in Rubisco turnover number 121
Chlamydomonas reinhardtii N123G Decrease in specificity factor 122
Chlamydomonas reinhardtii S379A Decrease in specificity factor 122
Anacystis nidulans S376 C 99% and ~99.9% decrease in carboxylase and oxygenase activity 123
Anacystis nidulans S376T 99% and ~99.9% decrease in carboxylase and oxygenase activity 123
Anacystis nidulans S376 A 99% and ~16% decrease in carboxylase and oxygenase activity 123
Rhodospirillum rubrum I164T 6% decrease in carboxylase activity with 40-fold lower Kcat/Km 124
Rhodospirillum rubrum I164N 1% decrease in carboxylase activity with 900-fold lower Kcat/Km 124
Rhodospirillum rubrum I164B 0.01–1% decrease in carboxylase activity 124
Rhodospirillum rubrum H287N 103-fold decrase in carboxylation catalysis 125
Rhodospirillum rubrum H287Q 105-fold decrase in carboxylation catalysis 125
Rhodospirillum rubrum M330L 126
Rubisco (large subunit)
Chamydomonas reinhardtii R59A Decrease in Vmax for carboxylation reaction 127
Chamydomonas reinhardtii Y67A Decrease in Vmax for carboxylation reaction 127
Chamydomonas reinhardtii Y68A Decrease in Vmax for carboxylation reaction 127
Chamydomonas reinhardtii D69A Decrease in Vmax for carboxylation reaction 127
Chamydomonas reinhardtii R71A decrease in Vmax (for carboxylation reaction) and thermal stability 127
Chamydomonas reinhardtii A222T, V262L, L290F Improved specificity factor and thermal stability 128
Phosphoribulokinase
Rhodobacter sphaeroides T18A 8-fold decrease in Vmax 129
Rhodobacter sphaeroides S14A 40-fold decrease in Vmax 129
Rhodobacter sphaeroides S19A 500-fold and >1500-fold decrease in Vmax and Vmax/Km of RuBP 129
Rhodobacter sphaeroides K165M, K165C 103-fold decrease in catalytic activity 130
Rhodobacter sphaeroides R168Q >300-fold decrease in catalytic efficiency 131
Rhodobacter sphaeroides R173Q 15-fold decrease in Vmax, 100-fold increase in Km for RuBP 131
Chlamydomonas reinhardtii R64C Almost inactive 132
Chlamydomonas reinhardtii R64A Decrease in activity 132
Chlamydomonas reinhardtii R64K Decrease in activity 132
Synechocystis sp. S222F Retains one-tenth catalytic activity 133
Rhodobacter sphaeroides H45N 40-fold increase in Km for RuBP 134
Rhodobacter sphaeroides N49Q 200-fold increase in Km for RuBP 134
Rhodobacter sphaeroides K53M No effect on catalysis or substrate binding 134
Rhodobacter sphaeroides D169A Vmax diminished by 4-orders of magnitude 135
Rhodobacter sphaeroides D42A Vmax diminished by 5-orders of magnitude 135
Rhodobacter sphaeroides D42N Vmax diminished by 5-orders of magnitude 135
Rhodobacter sphaeroides R31A Unlike wild-type, shows hyperbolic kinetics for ATP and NADH 136
Open in a new tab

Illustrating example

In order to illustrate the utility of non-catalytic enzymatic mutants as specific sugar binders for in-situ separation in reactors, recombinant Saccharomyces cerevisiae 3-phosphoglycerate kinase mutant R38Q [41] was prepared. Mutagenesis was carried out using wild type protein construct in plasmid pET19b as a template. The R38Q mutant was constructed with the Quickchange/Chameleon site-directed mutagenesis kit from stategene using primers as described elsewhere [41]. DNA sequencing of the plasmid identified the mutant. Recombinant wild-type and mutant (R38Q) 3-phosphoglycerate kinase (PGK) were purified to apparent homogeneity as described previously [20] have been shown in Figure 3A. The wild-type and mutant protein was incubated with 10 mM 3-phosphoglycerate barium salt (3PGA) in 50 mM Tris-Cl buffer, pH 7.5 containing 50 mM NaCl for overnight at room temperature. No modification of 3PGA was observed after incubation with R38Q mutant protein (data not shown). The R38Q was coupled with Protein A sepharose beads using dimethylpimelimidate. The recombinant R38Q mutant protein beads (R38Q-PGK) was incubated overnight at room temperature with a mixture of sugars, 3-phosphoglycerate, barium salt (3PGA), ribulose-5-phosphate (R5P), Glucose-6-phosphate (G6P) and Fructose-6-posphate (F1,6-bP) each at a concentration of 10 mM in a volume of 200 μl. After incubation they were washed with 1.5 ml of 180 mM NaCl in 50 mM Tris-Cl buffer, pH 7.5. They were subjected to elution with 1 M NaCl. Lane 1, mixture of sugar prior to incubation with R38Q-PGK and Lane-2 after elution with 1 M NaCl.

Figure 3.

Figure 3

Open in a new tab

The recombinant his-tagged wild-type and R38Q mutant 3-phosphoglycerate kinase was subjected to affinity purification on Ni-NTA column as described previously [20]. A. SDS-PAGE of recombinant wild-type and R38Q mutant S. cerevisiae 3-phosphoglycerate kinase. The proteins (1 and 1.8 μg respectively) was separated in 10% polyacrylamide gel and stained with Coommassie blue R250. B. TLC analysis of sugars prior to and after in-situ separation with R38Q. The recombinant R38Q mutant (R38Q-PGK) was coupled with Protein A sepharose beads and incubated overnight with a mixture of sugars, 3-phosphoglycerate (3PGA), ribulose-5-phosphate (R5P), Glucose-6-phosphate (G6P) and Fructose-6-posphate (F1,6-bP). After washing with 180 mM NaCl, the sugars were eluted with 1 M NaCl. Lane 1, mixture of sugar prior to incubation with R38Q-PGK and Lane-2 after elution with 1 M NaCl.

Conclusion

The enzyme-mutants lacking catalytic activity represent an important group of proteins that could be used for development of sugar-binding proteins reversible with respect to physicochemical parameters such as pH or salt concentration. Nevertheless, the non-enzymatic proteins also represent a suitable repertoire of such potential scaffolds, which could be used for development as sugar-binding proteins to be used in reactors for simultaneous separation of sugars that would be used in subsequent conversion steps. We have developed a RuBP production scheme from 3PGA [16,17] and also a de novo RuBP production scheme from D-glucose [21] for continuous CO2 fixation and for start-up of the fixation respectively employing series of reactors. Both systems for production of RuBP will benefit from specific sugar binders but besides their use in environmental biotechnology, they will find application in diagnostics, separation technologies and also as research reagents.

Acknowledgments

Acknowledgements

We thank Dr. Paramita Ray for help with literature search and Dr. Surabhi Choudhuri for her comments on the manuscript.

Contributor Information

Sourav Mahato, Email: mahatosourav_007@rediffmail.com.

Debojyoti De, Email: debajyoti_de@rediffmail.com.

Debajyoti Dutta, Email: debjyoti_dutta47@rediffmail.com.

Moloy Kundu, Email: moloy_kundu@rediffmail.com.

Sumana Bhattacharya, Email: sbc-abrd@usa.net.

Marc T Schiavone, Email: schiavone@rediffmail.com.

Sanjoy K Bhattacharya, Email: bhattas@ccf.org.

References

  1. Victor DG. Strategies for cutting Carbon. Nature. 1998;395:837–838. doi: 10.1038/27532. [DOI] [Google Scholar]
  2. Joos F, Plattner G-K, Stocker TF, Marchal O, Schmittner A. Global warming and marine carbon cycle feedbacks on future atmospheric CO2. Science. 1999;284:464–467. doi: 10.1126/science.284.5413.464. [DOI] [PubMed] [Google Scholar]
  3. Schnur R. The investment Forecast. Nature. 2002;415:483–484. doi: 10.1038/415483a. [DOI] [PubMed] [Google Scholar]
  4. De Leo GA, Gatto M, Caizzi A, Cellina F. The ecological and economic consequences of global climate change. In: Bhattacharya SK, Chakrabarti S, Mal TK, editor. In Recent Research Developments in Biotechnol Bioengg. Research Signpost, Kerala; 2002. pp. 163–183. [Google Scholar]
  5. De Leo GA, Rizzi L, Caizzi A, Gatto M. Carbon emissions. The economic benefits of the Kyoto Protocol. Nature. 2001;413:478–479. doi: 10.1038/35097156. [DOI] [PubMed] [Google Scholar]
  6. Cortright RD, Davda RR, Dumesic JA. Hydrogen from catalytic reforming of biomass-derived hydrocarbons in liquid water. Nature. 2002;418:964–967. doi: 10.1038/nature01009. [DOI] [PubMed] [Google Scholar]
  7. Service RF. Fuel cells. Biofuel cells. Science. 2002;296:1223. doi: 10.1126/science.296.5571.1223. [DOI] [PubMed] [Google Scholar]
  8. Schultz MG, Diehl T, Brasseur GP, Zittel W. Air pollution and climate-forcing impacts of a global hydrogen economy. Science. 2003;302:624–627. doi: 10.1126/science.1089527. [DOI] [PubMed] [Google Scholar]
  9. Prather MJ. Atmospheric science. An environmental experiment with H2? Science. 2003;302:581–582. doi: 10.1126/science.1091060. [DOI] [PubMed] [Google Scholar]
  10. Brumfiel G. Hydrogen cars fuel debate on basic research. Nature. 2003;422:104. doi: 10.1038/422108a. [DOI] [PubMed] [Google Scholar]
  11. Rahn T, Eiler JM, Boering KA, Wennberg PO, McCarthy MC, Tyler S, Schauffler S, Donnelly S, Atlas E. Extreme deuterium enrichment in stratospheric hydrogen and the global atmospheric budget of H2. Nature. 2003;424:918–921. doi: 10.1038/nature01917. [DOI] [PubMed] [Google Scholar]
  12. Tromp TK, Shia RL, Allen M, Eiler JM, Yung YL. Potential environmental impact of a hydrogen economy on the stratosphere. Science. 2003;300:1740–1742. doi: 10.1126/science.1085169. [DOI] [PubMed] [Google Scholar]
  13. Raphael SJ. The meanings of markers: ancillary techniques in diagnosis of thyroid neoplasia. Endocr Pathol. 2002;13:301–311. doi: 10.1385/EP:13:4:301. [DOI] [PubMed] [Google Scholar]
  14. Jackson A, Kemp P, Giddings J, Sugar R. Development and validation of a lectin-based assay for the quantitation of rat respiratory mucin. Novartis Found Symp. 2002;248:94–105. doi: 10.1002/0470860790.ch7. [DOI] [PubMed] [Google Scholar]
  15. Bhattacharya S, Nayak A, Schiavone M, Bhattacharya SK. Solubilization and Concentration of Carbon dioxide: Novel Spray reactors with immobilized Carbonic anhydrase. Biotechnol Bioeng. 2004;86:37–46. doi: 10.1002/bit.20042. [DOI] [PubMed] [Google Scholar]
  16. Bhattacharya SK. Conversion of carbon dioxide from ICE exhausts by fixation. US patent number 6258335. 2001. pp. 1–18.
  17. Bhattacharya S, Chakrabarti S, Bhattacharya SK. Bioprocess for recyclable CO2 fixation: A general description. In: Bhattacharya SK, Chakrabarti S, Mal TK, editor. In Recent Research Developments in Biotechnol Bioengg. Research Signpost, Kerala; 2002. pp. 109–120. [Google Scholar]
  18. Chakrabarti S, Bhattacharya S, Bhattacharya SK. Immobilization of D-ribulose-1,5-bisphosphate carboxylase/oxygenase: A step toward carbon dioxide fixation bioprocess. Biotechnol Bioengg. 2003;81:705–711. doi: 10.1002/bit.10515. [DOI] [PubMed] [Google Scholar]
  19. Chakrabarti S, Bhattacharya S, Bhattacharya SK. Biochemical engineering: cues from cells. Trends Biotechnol. 2003;21:204–209. doi: 10.1016/S0167-7799(03)00077-5. [DOI] [PubMed] [Google Scholar]
  20. Bhattacharya S, Schiavone M, Gomes J, Bhattacharya SK. Cascade of bioreactors in series for conversion of 3-phospho-D-glycerate into D-ribulose-1,5-bisphosphate: Kinetic parameters of enzymes and operation variables. J Biotechnol. 2004. [DOI] [PubMed]
  21. Bhattacharya S, Nayak A, Gomes J, Bhattacharya SK. A continuous process for production of D-ribulose-1,5-bisphosphate from D-glucose. Biochem Engg J. 2004;19:229–235. [Google Scholar]
  22. Bhattacharya SK. Use of enzyme mixtures for complex biosynthesis. Curr Opin Biotechnol. 2004. [DOI] [PubMed]
  23. Hart DA. Lectins in biological systems: applications to microbiology. Am J Clin Nutr. 1980;33:2416–2425. doi: 10.1093/ajcn/33.11.2416. [DOI] [PubMed] [Google Scholar]
  24. Schomburg I, Chang A, Ebeling C, Gremse M, Heldt C, Huhn G, Schomburg D. BRENDA, the enzyme database: updates and major new developments. Nucleic Acids Res. 2004;32:D431–D433. doi: 10.1093/nar/gkh081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pharkya P, Nikolaev EV, Maranas CD. Review of the BRENDA Database. Metab Eng. 2003;5:71–73. doi: 10.1016/S1096-7176(03)00008-9. [DOI] [PubMed] [Google Scholar]
  26. Lin K, Li L, Correia JJ, Pilkis SJ. Arg-257 and Arg-307 of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase bind the C-2 phospho group of fructose-2,6-bisphosphate in the fructose-2,6-bisphosphatase domain. J Biol Chem. 1992;267:19163–19171. [PubMed] [Google Scholar]
  27. Garel MC, Arous N, Calvin MC, Craescu CT, Rosa J, Rosa R. A recombinant bisphosphoglycerate mutase variant with acid phosphatase homology degrades 2,3-diphosphoglycerate. Proc Natl Acad Sci U S A. 1994;91:3593–3597. doi: 10.1073/pnas.91.9.3593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. White MF, Fothergill-Gilmore LA. Development of a mutagenesis, expression and purification system for yeast phosphoglycerate mutase. Investigation of the role of active-site His181. Eur J Biochem. 1992;207:709–714. doi: 10.1111/j.1432-1033.1992.tb17099.x. [DOI] [PubMed] [Google Scholar]
  29. Walter RA, Nairn J, Duncan D, Price NC, Kelly SM, Rigden DJ, Fothergill-Gilmore LA. The role of the C-terminal region in phosphoglycerate mutase. Biochem J. 1999;337:89–95. doi: 10.1042/0264-6021:3370089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rigden DJ, Lamani E, Mello LV, Littlejohn JE, Jedrzejas MJ. Insights into the catalytic mechanism of cofactor-independent phosphoglycerate mutase from X-ray crystallography, simulated dynamics and molecular modeling. J Mol Biol. 2003;328:909–920. doi: 10.1016/S0022-2836(03)00350-4. [DOI] [PubMed] [Google Scholar]
  31. Nairn J, Price NC, Kelly SM, Rigden D, Fothergill-Gilmore LA, Krell T. Phosphoglycerate mutase from Schizosaccharomyces pombe: development of an expression system and characterisation of three histidine mutants of the enzyme. Biochim Biophys Acta. 1996;1296:69–75. doi: 10.1016/0167-4838(96)00046-5. [DOI] [PubMed] [Google Scholar]
  32. Brewer JM, Glover CV, Holland MJ, Lebioda L. Significance of the enzymatic properties of yeast S39A enolase to the catalytic mechanism. Biochim Biophys Acta. 1998;1383:351–355. doi: 10.1016/S0167-4838(98)00004-1. [DOI] [PubMed] [Google Scholar]
  33. Vinarov DA, Nowak T. Role of His159 in yeast enolase catalysis. Biochemistry. 1999;38:12138–12149. doi: 10.1021/bi990760q. [DOI] [PubMed] [Google Scholar]
  34. Brewer JM, Holland MJ, Lebioda L. The H159A mutant of yeast enolase 1 has significant activity. Biochem Biophys Res Commun. 2000;276:1199–1202. doi: 10.1006/bbrc.2000.3618. [DOI] [PubMed] [Google Scholar]
  35. Gulick AM, Hubbard BK, Gerlt JA, Rayment I. Evolution of enzymatic activities in the enolase superfamily: identification of the general acid catalyst in the active site of D-glucarate dehydratase from Escherichia coli. Biochemistry. 2001;40:10054–10062. doi: 10.1021/bi010733b. [DOI] [PubMed] [Google Scholar]
  36. Holland MJ, Yokoi T, Holland JP, Myambo K, Innis MA. The GCR1 gene encodes a positive transcriptional regulator of the enolase and glyceraldehyde-3-phosphate dehydrogenase gene families in Saccharomyces cerevisiae. Mol Cell Biol. 1987;7:813–820. doi: 10.1128/mcb.7.2.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wilson CA, Hardman N, Fothergill-Gilmore LA, Gamblin SJ, Watson HC. Yeast phosphoglycerate kinase: investigation of catalytic function by site-directed mutagenesis. Biochem J. 1987;241:609–614. doi: 10.1042/bj2410609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Walker PA, Littlechild JA, Hall L, Watson HC. Site-directed mutagenesis of yeast phosphoglycerate kinase. The 'basic-patch' residue arginine 168. Eur J Biochem. 1989;183:49–55. doi: 10.1111/j.1432-1033.1989.tb14895.x. [DOI] [PubMed] [Google Scholar]
  39. Fairbrother WJ, Hall L, Littlechild JA, Walker PA, Watson HC, Williams RJ. Site-directed mutagenesis of histidine 62 in the 'basic patch' region of yeast phosphoglycerate kinase. FEBS Lett. 1989;258:247–250. doi: 10.1016/0014-5793(89)81665-5. [DOI] [PubMed] [Google Scholar]
  40. Ballery N, Minard P, Desmadril M, Betton JM, Perahia D, Mouawad L, Hall L, Yon JM. Introduction of internal cysteines as conformational probes in yeast phosphoglycerate kinase. Protein Eng. 1990;3:199–204. doi: 10.1093/protein/3.3.199. [DOI] [PubMed] [Google Scholar]
  41. Sherman MA, Szpikowska BK, Dean SA, Mathiowetz AM, McQueen NL, Mas MT. Probing the role of arginines and histidines in the catalytic function and activation of yeast 3-phosphoglycerate kinase by site-directed mutagenesis. J Biol Chem. 1990;265:10659–10665. [PubMed] [Google Scholar]
  42. Sherman MA, Dean SA, Mathiowetz AM, Mas MT. Site-directed mutations of arginine 65 at the periphery of the active site cleft of yeast 3-phosphoglycerate kinase enhance the catalytic activity and eliminate anion-dependent activation. Protein Eng. 1991;4:935–940. doi: 10.1093/protein/4.8.935. [DOI] [PubMed] [Google Scholar]
  43. Joao HC, Taddei N, Williams RJ. Investigating interdomain region mutants Phe194Leu and Phe194Trp of yeast phosphoglycerate kinase by 1H-NMR spectroscopy. Eur J Biochem. 1992;205:93–104. doi: 10.1111/j.1432-1033.1992.tb16755.x. [DOI] [PubMed] [Google Scholar]
  44. Tougard P, Le TH, Minard P, Desmadril M, Yon JM, Bizebard T, Lebras G, Dumas C. Structural and functional properties of mutant Arg203Pro from yeast phosphoglycerate kinase, as a model of phosphoglycerate kinase-Uppsala. Protein Eng. 1996;9:181–187. doi: 10.1093/protein/9.2.181. [DOI] [PubMed] [Google Scholar]
  45. Wikner C, Meshalkina L, Nilsson U, Nikkola M, Lindqvist Y, Sundstrom M, Schneider G. Analysis of an invariant cofactor-protein interaction in thiamin diphosphate-dependent enzymes by site-directed mutagenesis. Glutamic acid 418 in transketolase is essential for catalysis. J Biol Chem. 1994;269:32144–32150. [PubMed] [Google Scholar]
  46. Wikner C, Meshalkina L, Nilsson U, Backstrom S, Lindqvist Y, Schneider G. His103 in yeast transketolase is required for substrate recognition and catalysis. Eur J Biochem. 1995;233:750–755. doi: 10.1111/j.1432-1033.1995.750_3.x. [DOI] [PubMed] [Google Scholar]
  47. Meshalkina L, Nilsson U, Wikner C, Kostikowa T, Schneider G. Examination of the thiamin diphosphate binding site in yeast transketolase by site-directed mutagenesis. Eur J Biochem. 1967;244:646–652. doi: 10.1111/j.1432-1033.1997.t01-1-00646.x. [DOI] [PubMed] [Google Scholar]
  48. Wikner C, Nilsson U, Meshalkina L, Udekwu C, Lindqvist Y, Schneider G. Identification of catalytically important residues in yeast transketolase. Biochemistry. 1997;36:5643–15649. doi: 10.1021/bi971606b. [DOI] [PubMed] [Google Scholar]
  49. Nilsson U, Hecquet L, Gefflaut T, Guerard C, Schneider G. Asp477 is a determinant of the enantioselectivity in yeast transketolase. FEBS Lett. 1998;424:49–52. doi: 10.1016/S0014-5793(98)00136-7. [DOI] [PubMed] [Google Scholar]
  50. Fiedler E, Golbik R, Schneider G, Tittmann K, Neef H, Konig S, Hubner G. Examination of donor substrate conversion in yeast transketolase. J Biol Chem. 2001;276:16051–16058. doi: 10.1074/jbc.M007936200. [DOI] [PubMed] [Google Scholar]
  51. Al-Rabiee R, Lee EJ, Grant GA. The mechanism of velocity modulated allosteric regulation in D-3-phosphoglycerate dehydrogenase. Cross-linking adjacent regulatory domains with engineered disulfides mimics effector binding. J Biol Chem. 1996;271:13013–13017. doi: 10.1074/jbc.271.22.13013. [DOI] [PubMed] [Google Scholar]
  52. Capitanio D, Merico A, Ranzi BM, Compagno C. Effects of the loss of triose phosphate isomerase activity on carbon metabolism in Kluyveromyces lactis. Res Microbiol. 2002;153:593–598. doi: 10.1016/S0923-2508(02)01365-7. [DOI] [PubMed] [Google Scholar]
  53. Maithal K, Ravindra G, Balaram H, Balaram P. Inhibition of plasmodium falciparum triose-phosphate isomerase by chemical modification of an interface cysteine. Electrospray ionization mass spectrometric analysis of differential cysteine reactivities. J Biol Chem. 2002;277:25106–25114. doi: 10.1074/jbc.M202419200. [DOI] [PubMed] [Google Scholar]
  54. Maithal K, Ravindra G, Nagaraj G, Singh SK, Balaram H, Balaram P. Subunit interface mutation disrupting an aromatic cluster in Plasmodium falciparum triosephosphate isomerase: effect on dimer stability. Protein Eng. 2002;15:575–584. doi: 10.1093/protein/15.7.575. [DOI] [PubMed] [Google Scholar]
  55. Chanez-Cardenas ME, Fernandez-Velasco DA, Vazquez-Contreras E, Coria R, Saab-Rincon G, Perez-Montfort R. Unfolding of triosephosphate isomerase from Trypanosoma brucei: identification of intermediates and insight into the denaturation pathway using tryptophan mutants. Arch Biochem Biophys. 2002;399:117–129. doi: 10.1006/abbi.2001.2749. [DOI] [PubMed] [Google Scholar]
  56. Lambeir AM, Backmann J, Ruiz-Sanz J, Filimonov V, Nielsen JE, Kursula I, Norledge BV, Wierenga RK. The ionization of a buried glutamic acid is thermodynamically linked to the stability of Leishmania mexicana triose phosphate isomerase. Eur J Biochem. 2000;267:2516–2524. doi: 10.1046/j.1432-1327.2000.01254.x. [DOI] [PubMed] [Google Scholar]
  57. Compagno C, Boschi F, Daleffe A, Porro D, Ranzi BM. Isolation, nucleotide sequence, and physiological relevance of the gene encoding triose phosphate isomerase from Kluyveromyces lactis. Appl Environ Microbiol. 1999;65:4216–4219. doi: 10.1128/aem.65.9.4216-4219.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Alvarez M, Zeelen JP, Mainfroid V, Rentier-Delrue F, Martial JA, Wyns L, Wierenga RK, Maes D. Triose-phosphate isomerase (TIM) of the psychrophilic bacterium Vibrio marinus. Kinetic and structural properties. J Biol Chem. 1998;273:2199–2206. doi: 10.1074/jbc.273.4.2199. [DOI] [PubMed] [Google Scholar]
  59. Gomez-Puyou A, Saavedra-Lira E, Becker I, Zubillaga RA, Rojo-Dominguez A, Perez-Montfort R. Using evolutionary changes to achieve species-specific inhibition of enzyme action – studies with triosephosphate isomerase. Chem Biol. 1995;2:847–855. doi: 10.1016/1074-5521(95)90091-8. [DOI] [PubMed] [Google Scholar]
  60. Lodi PJ, Chang LC, Knowles JR, Komives EA. Triosephosphate isomerase requires a positively charged active site: the role of lysine-12. Biochemistry. 1994;33:2809–2814. doi: 10.1021/bi00176a009. [DOI] [PubMed] [Google Scholar]
  61. Joseph-McCarthy D, Rost LE, Komives EA, Petsko GA. Crystal structure of the mutant yeast triosephosphate isomerase in which the catalytic base glutamic acid 165 is changed to aspartic acid. Biochemistry. 1994;33:2824–2829. doi: 10.1021/bi00176a011. [DOI] [PubMed] [Google Scholar]
  62. Brzovic PS, Hyde CC, Miles EW, Dunn MF. Characterization of the functional role of a flexible loop in the alpha-subunit of tryptophan synthase from Salmonella typhimurium by rapid-scanning, stopped-flow spectroscopy and site-directed mutagenesis. Biochemistry. 1993;32:10404–10413. doi: 10.1021/bi00090a016. [DOI] [PubMed] [Google Scholar]
  63. Borchert TV, Pratt K, Zeelen JP, Callens M, Noble ME, Opperdoes FR, Michels PA, Wierenga RK. Overexpression of trypanosomal triosephosphate isomerase in Escherichia coli and characterisation of a dimer-interface mutant. Eur J Biochem. 1993;211:703–710. doi: 10.1111/j.1432-1033.1993.tb17599.x. [DOI] [PubMed] [Google Scholar]
  64. Raines RT, Sutton EL, Straus DR, Gilbert W, Knowles JR. Reaction energetics of a mutant triosephosphate isomerase in which the active-site glutamate has been changed to aspartate. Biochemistry. 1986;25:7142–7154. doi: 10.1021/bi00370a057. [DOI] [PubMed] [Google Scholar]
  65. Casal JI, Ahern TJ, Davenport RC, Petsko GA, Klibanov AM. Subunit interface of triosephosphate isomerase: site-directed mutagenesis and characterization of the altered enzyme. Biochemistry. 1987;26:1258–1264. doi: 10.1021/bi00379a009. [DOI] [PubMed] [Google Scholar]
  66. Nickbarg EB, Davenport RC, Petsko GA, Knowles JR. Triosephosphate isomerase: removal of a putatively electrophilic histidine residue results in a subtle change in catalytic mechanism. Biochemistry. 1988;27:5948–5960. doi: 10.1021/bi00416a019. [DOI] [PubMed] [Google Scholar]
  67. Leonard S, Nguyen C, Scott K, Holmes A, Grewal N, Mulvaney E. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature. 2001;413:852–856. doi: 10.1038/35101614. [DOI] [PubMed] [Google Scholar]
  68. Goldrick D, Yu G-Q, Jiang S-Q, Hong J-S. Nucleotide sequence and transcription start point of the phosphoglycerate transporter gene of Salmonella typhimurium. J Bacteriol. 1988;170:3421–3426. doi: 10.1128/jb.170.8.3421-3426.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Ivanova N, Sorokin A, Anderson I, Galleron N, Candelon B, Kapatral V, Bhattacharyya A, Reznik G, Mikhailova N, Lapidus A. Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature. 2003;423:87–91. doi: 10.1038/nature01582. [DOI] [PubMed] [Google Scholar]
  70. Read TD, Peterson SN, Tourasse N, Baillie LW, Paulsen IT, Nelson KE, Tettelin H, Fouts DE, Eisen JA, Gill SR. The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature. 2003;423:81–86. doi: 10.1038/nature01586. [DOI] [PubMed] [Google Scholar]
  71. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, Churcher C, Mungall KL, Bentley SD, Holden MTG, Sebaihia M. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature. 2001;413:848–852. doi: 10.1038/35101607. [DOI] [PubMed] [Google Scholar]
  72. Deng W, Liou SR, Plunkett G, III, Mayhew GF, Rose DJ, Burland V, Kodoyianni V, Schwartz DC, Blattner FR. Comparative genomics of Salmonella enterica serovar Typhi strains Ty2 and CT18. J Bacteriol. 2003;185:2330–2337. doi: 10.1128/JB.185.7.2330-2337.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Shimoji Y, Ng V, Matsumura K, Fischetti VA, Rambukkana A. A 21-kDa surface protein of Mycobacterium leprae binds peripheral nerve laminin-2 and mediates Schwann cell invasion. Proc Natl Acad Sci USA. 1999;96:9857–9862. doi: 10.1073/pnas.96.17.9857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, Wheeler PR, Honore N, Garnier T, Churcher C, Harris D, Mungall K, Basham D, Brown D, Chillingworth T, Connor R, Davies RM, Devlin K, Duthoy S, Feltwell T, Fraser A, Hamlin N, Holroyd S, Hornsby T, Jagels K, Lacroix C, Maclean J, Moule S, Murphy L, Oliver K, Quail MA, Rajandream MA, Rutherford KM, Rutter S, Seeger K, Simon S, Simmonds M, Skelton J, Squares R, Squares S, Stevens K, Taylor K, Whitehead S, Woodward JR, Barrell BG. Massive gene decay in the leprosy bacillus. Nature. 2001;409:1007–1011. doi: 10.1038/35059006. [DOI] [PubMed] [Google Scholar]
  75. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Barrell BG. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature. 1998;393:537–544. doi: 10.1038/31159. [DOI] [PubMed] [Google Scholar]
  76. Fleischmann RD, Alland D, Eisen JA, Carpenter L, White O, Peterson J, DeBoy R, Dodson R, Gwinn M, Haft D, Hickey E, Kolonay JF, Nelson WC, Umayam LA, Ermolaeva M, Salzberg SL, Delcher A, Utterback T, Weidman J, Khouri H, Gill J, Mikula A, Bishai W, Jacobs WR, Jr, Venter JC, Fraser CM. Whole-genome comparison of Mycobacterium tuberculosis clinical and laboratory strains. J Bacteriol. 2002;184:5479–5490. doi: 10.1128/JB.184.19.5479-5490.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Keppel E, Schaller HC. A 33 kDa protein with sequence homology to the 'laminin binding protein' is associated with the cytoskeleton in hydra and in mammalian cells. J Cell Sci. 1991;100:789–797. doi: 10.1242/jcs.100.4.789. [DOI] [PubMed] [Google Scholar]
  78. Hung M, Rosenthal ET, Boblett B, Benson S. Characterization and localized expression of the laminin binding protein/p40 (LBP/p40) gene during sea urchin development. Exp Cell Res. 1995;221:221–230. doi: 10.1006/excr.1995.1370. [DOI] [PubMed] [Google Scholar]
  79. Rosenthal ET, Wordeman L. A protein similar to the 67 kDa laminin binding protein and p40 is probably a component of the translational machinery in Urechis caupo oocytes and embryos. J Cell Sci. 1995;108:245–256. doi: 10.1242/jcs.108.1.245. [DOI] [PubMed] [Google Scholar]
  80. Tettelin H, Masignani V, Cieslewicz MJ, Eisen JA, Peterson S, Wessels MR, Paulsen IT, Nelson KE, Margarit I, Read TD, Madoff LC, Wolf AM, Beanan MJ, Brinkac LM, Daugherty SC, DeBoy RT, Durkin AS, Kolonay JF, Madupu R, Lewis MR, Radune D, Fedorova NB, Scanlan D, Khouri H, Mulligan S, Carty HA, Cline RT, Van Aken SE, Gill J, Scarselli M, Mora M, Iacobini ET, Brettoni C, Galli G, Mariani M, Vegni F, Maione D, Rinaudo D, Rappuoli R, Telford JL, Kasper DL, Grandi G, Fraser CM. Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proc Natl Acad Sci USA. 2002;99:12391–12396. doi: 10.1073/pnas.182380799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Glaser P, Rusniok C, Buchrieser C, Chevalier F, Frangeul L, Msadek T, Zouine M, Couve E, Lalioui L, Poyart C, Trieu-Cuot P, Kunst F. Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol Microbiol. 2002;45:1499–1513. doi: 10.1046/j.1365-2958.2002.03126.x. [DOI] [PubMed] [Google Scholar]
  82. Ferretti JJ, McShan WM, Ajdic D, Savic DJ, Savic G, Lyon K, Primeaux C, Sezate S, Suvorov AN, Kenton S, Lai HS, Lin SP, Qian Y, Jia HG, Najar FZ, Ren Q, Zhu H, Song L, White J, Yuan X, Clifton SW, Roe BA, McLaughlin R. Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci USA. 2001;98:4658–4663. doi: 10.1073/pnas.071559398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Granlund M, Michel F, Norgren M. Mutually exclusive distribution of IS1548 and GBSi1, an active group II intron identified in human isolates of group b streptococci. J Bacteriol. 2001;183:2560–2569. doi: 10.1128/JB.183.8.2560-2569.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Loehning C, Ciriacy M. The TYE7 gene of Saccharomyces cerevisiae encodes a putative bHLH-LZ transcription factor required for Ty1-mediated gene expression. Yeast. 1994;10:1329–1339. doi: 10.1002/yea.320101010. [DOI] [PubMed] [Google Scholar]
  85. Nishi K, Park CS, Pepper AE, Eichinger G, Innis MA, Holland MJ. The GCR1 requirement for yeast glycolytic gene expression is suppressed by dominant mutations in the SGC1 gene, which encodes a novel basic-helix-loop-helix protein. Mol Cell Biol. 1995;15:2646–2653. doi: 10.1128/mcb.15.5.2646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Kurita O, Nishida Y. Involvement of mitochondrial aldehyde dehydrogenase ALD5 in maintenance of the mitochondrial electron transport chain in Saccharomyces cerevisiae. FEMS Microbiol Lett. 2003;181:281–287. doi: 10.1016/S0378-1097(99)00523-6. [DOI] [PubMed] [Google Scholar]
  87. Valadi H, Larsson C, Gustafsson L. Improved ethanol production by glycerol-3-phosphate dehydrogenase mutants of Saccharomyces cerevisiae. Appl Microbiol Biotechnol. 1998;50:434–439. doi: 10.1007/s002530051317. [DOI] [PubMed] [Google Scholar]
  88. van der Klei IJ, van der Heide M, Baerends RJ, Rechinger KB, Nicolay K, Kiel JA, Veenhuis M. The Hansenula polymorpha per6 mutant is affected in two adjacent genes which encode dihydroxyacetone kinase and a novel protein, Pak1p, involved in peroxisome integrity. Curr Genet. 1998;34:1–11. doi: 10.1007/s002940050360. [DOI] [PubMed] [Google Scholar]
  89. Heath RJ, Rock CO. A missense mutation accounts for the defect in the glycerol-3-phosphate acyltransferase expressed in the plsB26 mutant. J Bacteriol. 1999;181:1944–1946. doi: 10.1128/jb.181.6.1944-1946.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Heath RJ, Rock CO. A conserved histidine is essential for glycerolipid acyltransferase catalysis. J Bacteriol. 1998;180:1425–1430. doi: 10.1128/jb.180.6.1425-1430.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Minskoff SA, Racenis PV, Granger J, Larkins L, Hajra AK, Greenberg ML. Regulation of phosphatidic acid biosynthetic enzymes in Saccharomyces cerevisiae. J Lipid Res. 1994;35:2254–2262. [PubMed] [Google Scholar]
  92. Cho H, Oliveira MA, Tai HH. Critical residues for the coenzyme specificity of NAD+-dependent 15-hydroxyprostaglandin dehydrogenase. Arch Biochem Biophys. 2003;419:139–146. doi: 10.1016/j.abb.2003.09.019. [DOI] [PubMed] [Google Scholar]
  93. Soundar S, Park JH, Huh TL, Colman RF. Evaluation by mutagenesis of the importance of 3 arginines in alpha, beta, and gamma subunits of human NAD-dependent isocitrate dehydrogenase. J Biol Chem. 2003;278:52146–52153. doi: 10.1074/jbc.M306178200. [DOI] [PubMed] [Google Scholar]
  94. Yamaguchi M, Stout CD. Essential glycine in the proton channel of Escherichia coli transhydrogenase. J Biol Chem. 2003;278:45333–45339. doi: 10.1074/jbc.M308236200. [DOI] [PubMed] [Google Scholar]
  95. Klimacek M, Kavanagh KL, Wilson DK, Nidetzky B. On the role of Bronsted catalysis in Pseudomonas fluorescens mannitol 2-dehydrogenase. Biochem J. 2003;375:141–149. doi: 10.1042/BJ20030733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Saridakis V, Pai EF. Mutational, structural, and kinetic studies of the ATP-binding site of Methanobacterium thermoautotrophicum nicotinamide mononucleotide adenylyltransferase. J Biol Chem. 2003;278:34356–34363. doi: 10.1074/jbc.M205369200. [DOI] [PubMed] [Google Scholar]
  97. Waterham HR, Titorenko VI, Swaving GJ, Harder W, Veenhuis M. Peroxisomes in the methylotrophic yeast Hansenula polymorpha do not necessarily derive from pre-existing organelles. EMBO J. 1993;12:4785–4794. doi: 10.1002/j.1460-2075.1993.tb06167.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Liao HF, Lin LL, Chien HR, Hsu WH. Serine 187 is a crucial residue for allosteric regulation of Corynebacterium glutamicum 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase. FEMS Microbiol Lett. 2001;194:59–64. doi: 10.1016/S0378-1097(00)00507-3. [DOI] [PubMed] [Google Scholar]
  99. Alvarez M, Wouters J, Maes D, Mainfroid V, Rentier-Delrue F, Wyns L, Depiereux E, Martial JA. Lys13 plays a crucial role in the functional adaptation of the thermophilic triose-phosphate isomerase from Bacillus stearothermophilus to high temperatures. J Biol Chem. 1999;274:19181–19187. doi: 10.1074/jbc.274.27.19181. [DOI] [PubMed] [Google Scholar]
  100. Zheng Z, Zou J. The initial step of the glycerolipid pathway: identification of glycerol 3- phosphate/dihydroxyacetone phosphate dual substrate acyltransferases in Saccharomyces cerevisiae. J Biol Chem. 2001;276:41710–41716. doi: 10.1074/jbc.M104749200. [DOI] [PubMed] [Google Scholar]
  101. Vilei EM, Frey J. Genetic and biochemical characterization of glycerol uptake in mycoplasma mycoides subsp. mycoides SC: its impact on H(2)O(2) production and virulence. Clin Diagn Lab Immunol. 2001;8:85–92. doi: 10.1128/CDLI.8.1.85-92.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Ferguson GP, Totemeyer S, MacLean MJ, Booth IR. Methylglyoxal production in bacteria: suicide or survival? Arch Microbiol. 1998;170:209–218. doi: 10.1007/s002030050635. [DOI] [PubMed] [Google Scholar]
  103. Williams SG, Greenwood JA, Jones CW. The effect of nutrient limitation on glycerol uptake and metabolism in continuous cultures of Pseudomonas aeruginosa. Microbiology. 1994;140:2961–2969. doi: 10.1099/13500872-140-11-2961. [DOI] [PubMed] [Google Scholar]
  104. Badia J, Gimenez R, Baldoma L, Barnes E, Fessner WD, Anguilar J. L-lyxose metabolism employs the L-rhamnose pathway in mutant cells of Escherichia coli adapted to grow on L-lyxose. J Bacteriol. 1991;173:5144–5150. doi: 10.1128/jb.173.16.5144-5150.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. Zhu Y, Lin EC. A mutant crp allele that differentially activates the operons of the fuc regulon in Escherichia coli. J Bacteriol. 1988;170:2352–2358. doi: 10.1128/jb.170.5.2352-2358.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Hacking AJ, Lin EC. Disruption of the fucose pathway as a consequence of genetic adaptation to propanediol as a carbon source in Escherichia coli. J Bacteriol. 1976;126:1166–1172. doi: 10.1128/jb.126.3.1166-1172.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Miki K, Lin EC. Anaerobic energy-yielding reaction associated with transhydrogenation from glycerol 3-phosphate to fumarate by an Escherichia coli system. J Bacteriol. 1975;124:1282–1287. doi: 10.1128/jb.124.3.1282-1287.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Kuzuyama T, Takahashi S, Takagi M, Seto H. Characterization of 1-deoxy-D-xylulose 5-phosphate reductoisomerase, an enzyme involved in isopentenyl diphosphate biosynthesis, and identification of its catalytic amino acid residues. J Biol Chem. 2000;275:19928–19932. doi: 10.1074/jbc.M001820200. [DOI] [PubMed] [Google Scholar]
  109. Stevis PE, Ho NW. A novel xylB-based positive selection vector. Plasmid. 1988;20:92–95. doi: 10.1016/0147-619x(88)90011-x. [DOI] [PubMed] [Google Scholar]
  110. Faber KN, van Dijk R, Keizer-Gunnink I, Koek A, van der Klei IJ, Veenhuis M. Import of assembled PTS1 proteins into peroxisomes of the yeast Hansenula polymorpha: yes and no! Biochim Biophys Acta. 2002;1591:157–162. doi: 10.1016/S0167-4889(02)00274-4. [DOI] [PubMed] [Google Scholar]
  111. Salomons FA, Kiel JA, Faber KN, Veenhuis M, van der Klei IJ. Overproduction of Pex5p stimulates import of alcohol oxidase and dihydroxyacetone synthase in a Hansenula polymorpha Pex14 null mutant. J Biol Chem. 2000;275:12603–12611. doi: 10.1074/jbc.275.17.12603. [DOI] [PubMed] [Google Scholar]
  112. Camus JC, Pryor MJ, Medigue C, Cole ST. Re-annotation of the genome sequence of Mycobacterium tuberculosis H37Rv. Microbiology. 2002;148:2967–2973. doi: 10.1099/00221287-148-10-2967. [DOI] [PubMed] [Google Scholar]
  113. Eicks M, Maurino V, Knappe S, Flugge UI, Fischer K. The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiol. 2002;128:512–522. doi: 10.1104/pp.128.2.512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Du YC, Peddi SR, Spreitzer RJ. Assessment of structural and functional divergence far from the large subunit active site of ribulose-1, 5-bisphosphate carboxylase/oxygenase. J Biol Chem. 2003;278:49401–49405. doi: 10.1074/jbc.M309993200. [DOI] [PubMed] [Google Scholar]
  115. Spreitzer RJ, Thow G, Zhu G. Pseudoreversion substitution at large-subunit residue 54 influences the CO2/O2 specificity of chloroplast ribulose-bisphosphate carboxylase/oxygenase. Plant Physiol. 1995;109:681–685. doi: 10.1104/pp.109.2.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Romanova AK, Zhen-Qi-Cheng Z, McFadden BA. Activity and carboxylation specificity factor of mutant ribulose 1,5-bisphosphate carboxylase/oxygenase from Anacystis nidulans. Biochem Mol Biol Int. 1997;42:299–307. doi: 10.1080/15216549700202691. [DOI] [PubMed] [Google Scholar]
  117. Lee GJ, McDonald KA, McFadden BA. Leucine 332 influences the CO2/O2 specificity factor of ribulose-1, 5-bisphosphate carboxylase/oxygenase from Anacystis nidulans. Protein Sci. 1993;2:1147–1154. doi: 10.1002/pro.5560020709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Day AG, Chene P, Fersht AR. Role of phenylalanine-327 in the closure of loop 6 of ribulosebisphosphate carboxylase/oxygenase from Rhodospirillum rubrum. Biochemistry. 1993;32:1940–1944. doi: 10.1021/bi00059a009. [DOI] [PubMed] [Google Scholar]
  119. Chene P, Day AG, Fersht AR. Mutation of asparagine 111 of rubisco from Rhodospirillum rubrum alters the carboxylase/oxygenase specificity. J Mol Biol. 1992;225:891–896. doi: 10.1016/0022-2836(92)90408-c. [DOI] [PubMed] [Google Scholar]
  120. Read BA, Tabita FR. Amino acid substitutions in the small subunit of ribulose-1, 5-bisphosphate carboxylase/oxygenase that influence catalytic activity of the holoenzyme. Biochemistry. 1992;31:519–525. doi: 10.1021/bi00117a031. [DOI] [PubMed] [Google Scholar]
  121. Marcus Y, Altman-Gueta H, Finkler A, Gurevitz M. Dual role of cysteine 172 in redox regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase activity and degradation. J Bacteriol. 2003;185:1509–1517. doi: 10.1128/JB.185.5.1509-1517.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Zhu G, Spreitzer RJ. Directed mutagenesis of chloroplast ribulosebisphosphate carboxylase/oxygenase. Substitutions at large subunit asparagine 123 and serine 379 decrease CO2/O2 specificity. J Biol Chem. 1994;269:3952–3956. [PubMed] [Google Scholar]
  123. Lee GJ, McFadden BA. Serine-376 contributes to the binding of substrate by ribulose-bisphosphate carboxylase/oxygenase from Anacystis nidulans. Biochemistry. 1992;31:2304–2308. doi: 10.1021/bi00123a014. [DOI] [PubMed] [Google Scholar]
  124. Chene P, Day AG, Fersht AR. Role of isoleucine-164 at the active site of rubisco from Rhodospirillum rubrum. Biochem Biophys Res Commun. 1997;232:482–486. doi: 10.1006/bbrc.1997.6318. [DOI] [PubMed] [Google Scholar]
  125. Harpel MR, Larimer FW, Hartman FC. Multiple catalytic roles of His 287 of Rhodospirillum rubrum ribulose 1, 5-bisphosphate carboxylase/oxygenase. Protein Sci. 1998;7:730–738. doi: 10.1002/pro.5560070322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  126. Terzaghi BE, Laing WA, Christeller JT, Petersen GB, Hill DF. Ribulose 1, 5-bisphosphate carboxylase. Effect on the catalytic properties of changing methionine-330 to leucine in the Rhodospirillum rubrum enzyme. Biochem J. 1986;235:839–846. doi: 10.1042/bj2350839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Spreitzer RJ, Esquivel MG, Du YC, McLaughlin PD. Alanine-scanning mutagenesis of the small-subunit beta A-beta B loop of chloroplast ribulose-1, 5-bisphosphate carboxylase/oxygenase: substitution at Arg-71 affects thermal stability and CO2/O2 specificity. Biochemistry. 2001;40:5615–5621. doi: 10.1021/bi002943e. [DOI] [PubMed] [Google Scholar]
  128. Du YC, Spreitzer RJ. Suppressor mutations in the chloroplast-encoded large subunit improve the thermal stability of wild-type ribulose-1, 5-bisphosphate carboxylase/oxygenase. J Biol Chem. 2000;275:19844–19847. doi: 10.1074/jbc.M002321200. [DOI] [PubMed] [Google Scholar]
  129. Runquist JA, Rios SE, Vinarov DA, Miziorko HM. Functional evaluation of serine/threonine residues in the P-Loop of Rhodobacter sphaeroides phosphoribulokinase. Biochemistry. 2001;40:14530–14537. doi: 10.1021/bi010778c. [DOI] [PubMed] [Google Scholar]
  130. Runquist JA, Harrison DH, Miziorko HM. Rhodobacter sphaeroides phosphoribulokinase: identification of lysine-165 as a catalytic residue and evaluation of the contributions of invariant basic amino acids to ribulose 5-phosphate binding. Biochemistry. 1999;38:13999–14005. doi: 10.1021/bi9910326. [DOI] [PubMed] [Google Scholar]
  131. Runquist JA, Harrison DH, Miziorko HM. Functional evaluation of invariant arginines situated in the mobile lid domain of phosphoribulokinase. Biochemistry. 1998;37:1221–1226. doi: 10.1021/bi972052f. [DOI] [PubMed] [Google Scholar]
  132. Avilan L, Gontero B, Lebreton S, Ricard J. Information transfer in multienzyme complexes – 2. The role of Arg64 of Chlamydomonas reinhardtii phosphoribulokinase in the information transfer between glyceraldehyde-3-phosphate dehydrogenase and phosphoribulokinase. Eur J Biochem. 1997;250:296–302. doi: 10.1111/j.1432-1033.1997.0296a.x. [DOI] [PubMed] [Google Scholar]
  133. Su X, Bogorad L. A residue substitution in phosphoribulokinase of Synechocystis PCC 6803 renders the mutant light-sensitive. J Biol Chem. 1991;266:23698–23705. [PubMed] [Google Scholar]
  134. Sandbaken MG, Runquist JA, Barbieri JT, Miziorko HM. Identification of the phosphoribulokinase sugar phosphate binding domain. Biochemistry. 1992;31:3715–3719. doi: 10.1021/bi00129a022. [DOI] [PubMed] [Google Scholar]
  135. Charlier HA, Jr, Runquist JA, Miziorko HM. Evidence supporting catalytic roles for aspartate residues in phosphoribulokinase. Biochemistry. 1994;33:9343–9350. doi: 10.1021/bi00197a039. [DOI] [PubMed] [Google Scholar]
  136. Kung G, Runquist JA, Miziorko HM, Harrison DH. Identification of the allosteric regulatory site in bacterial phosphoribulokinase. Biochemistry. 1999;38:15157–15165. doi: 10.1021/bi991033y. [DOI] [PubMed] [Google Scholar]
  137. Staswick PE, Crafts-Brandner SJ, Salvucci ME. cDNA sequence for the ribulose 1,5 bisphosphate carboxylase/oxygenase complex protein. A protein that accumulates in soybean leaves in response to fruit removal. Plant Physiol. 1994;105:1445–1446. doi: 10.1104/pp.105.4.1445. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Microbial Cell Factories are provided here courtesy of BMC

RESOURCES