Oligomerization and characteristics of phosphoenolpyruvate carboxylase in Synechococcus PCC 7002.
Allosteric Regulation
Bacterial Proteins
/ metabolism
Chromatography, Gel
Crystallization
Crystallography, X-Ray
Dimerization
Escherichia coli
/ metabolism
Glutamine
/ metabolism
Magnesium
/ metabolism
Phosphoenolpyruvate Carboxylase
/ metabolism
Protein Conformation
Scattering, Small Angle
Synechococcus
/ metabolism
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
27 02 2020
27 02 2020
Historique:
received:
18
09
2019
accepted:
10
02
2020
entrez:
29
2
2020
pubmed:
29
2
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Phosphoenolpyruvate carboxylase (PEPc) is an essential enzyme in plants. A photosynthetic form is present both as dimer and tetramer in C4 and CAM metabolism. Additionally, non-photosynthetic PEPcs are also present. The single, non-photosynthetic PEPc of the unicellular cyanobacterium Synechococcus PCC 7002 (Synechococcus), involved in the TCA cycle, was examined. Using size exclusion chromatography (SEC) and small angle X-ray scattering (SAXS), we observed that PEPc in Synechococcus exists as both a dimer and a tetramer. This is the first demonstration of two different oligomerization states of a non-photosynthetic PEPc. High concentration of Mg
Identifiants
pubmed: 32107404
doi: 10.1038/s41598-020-60249-2
pii: 10.1038/s41598-020-60249-2
pmc: PMC7046716
doi:
Substances chimiques
Bacterial Proteins
0
Glutamine
0RH81L854J
Phosphoenolpyruvate Carboxylase
EC 4.1.1.31
Magnesium
I38ZP9992A
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3607Références
Durall, C. & Lindblad, P. Mechanisms of carbon fixation and engineering for increased carbon fixation in cyanobacteria. Algal Res. 11, 263–270 (2015).
doi: 10.1016/j.algal.2015.07.002
O’Leary, B., Park, J. & Plaxton, W. C. The remarkable diversity of plant PEPC (phosphoenolpyruvate carboxylase): recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPCs. Biochem. J. 436, 15–34 (2011).
pubmed: 21524275
doi: 10.1042/BJ20110078
Schuller, K. A., Plaxton, W. C. & Turpin, D. H. Regulation of phosphoenolpyruvate carboxylase from the green alga Selenastrum minutum: properties associated with replenishment of tricarboxylic acid cycle intermediates during ammonium assimilation. Plant Physiol. 93, 1303–1311 (1990).
pubmed: 16667617
pmcid: 1062672
doi: 10.1104/pp.93.4.1303
Rivoal, J., Dunford, R., Plaxton, W. C. & Turpin, D. H. Purification and Properties of Four Phosphoenolpyruvate Carboxylase Isoforms from the Green Alga Selenastrum minutum: Evidence That Association of the 102-kDa Catalytic Subunit with Unrelated Polypeptides May Modify the Physical and Kinetic Properties of the Enzyme. Arch. Biochem. Biophys. 332, 47–57 (1996).
pubmed: 8806708
doi: 10.1006/abbi.1996.0315
Rivoal, J., Plaxton, W. C. & Turpin, D. H. Purification and characterization of high-and low-molecular-mass isoforms of phosphoenolpyruvate carboxylase from. Chlamydomonas reinhardtii. Biochem. J. 331, 201–29 (1998).
pubmed: 9512480
Rivoal, J., Trzos, S., Gage, D. A., Plaxton, W. C. & Turpin, D. H. Two unrelated phosphoenolpyruvate carboxylase polypeptides physically interact in the high molecular mass isoforms of this enzyme in the unicellular green alga Selenastrum minutum. J. Biol Chem. 276, 12588–12597 (2001).
pubmed: 11278626
doi: 10.1074/jbc.M010150200
Chen, L. M., Omiya, T., Hata, S. & Izui, K. Molecular characterization of a phosphoenolpyruvate carboxylase from a thermophilic cyanobacterium, Synechococcus vulcanus with unusual allosteric properties. Plant Cell. Physiol. 43, 159–169 (2002).
pubmed: 11867695
doi: 10.1093/pcp/pcf019
Owttrim, G. W. & Colman, B. Purification and characterization of phosphoenolpyruvate carboxylase from a cyanobacterium. J. Bacteriol. 168, 207–212 (1986).
pubmed: 3093461
pmcid: 213439
doi: 10.1128/JB.168.1.207-212.1986
Takeya, M., Hirai, M. Y. & Osanai, T. Allosteric inhibition of phosphoenolpyruvate carboxylases is determined by a single amino acid residue in cyanobacteria. Sci. Rep. 7, 41080 (2017).
pubmed: 28117365
pmcid: 5259782
doi: 10.1038/srep41080
Luinenburg, I. & Coleman, J. R. A requirement for phosphoenolpyruvate carboxylase in the cyanobacterium Synechococcus PCC 7942. Arch. Microbiol. 154, 471–474 (1990).
doi: 10.1007/BF00245230
Shylajanaciyar, M. et al. Analysis and elucidation of phosphoenolpyruvate carboxylase in cyanobacteria. Proteins 34, 73–81 (2015).
doi: 10.1007/s10930-015-9598-x
Andreo, C. S., Gonzalez, D. H. & Iglesias, A. A. Higher plant phosphoenolpyruvate carboxylase. FEBS Letters 213, 1–8 (1987).
doi: 10.1016/0014-5793(87)81454-0
Ishijima, S. et al. Comparison of amino acid sequences between phosphoenolpyruvate carboxylases from Escherichia coli (allosteric) and Anacystis nidulans (non-allosteric): Identification of conserved and variable regions. Biochem. Biophys. Res. Commun. 133, 436–441 (1985).
pubmed: 3936496
doi: 10.1016/0006-291X(85)90925-8
Smith, A. A. & Plazas, M. C. In silico characterization and homology modeling of cyanobacterial phosphoenolpyruvate carboxylase enzymes with computational tools and bioinformatics servers. Am. J. Biochem. Mol. Biol. 1, 319–336 (2011).
doi: 10.3923/ajbmb.2011.319.336
Coleman, J. R. & Colman, B. Demonstration of C3 photosynthesis in a blue-green alga. Planta 149, 318–320 (1980).
pubmed: 24306306
doi: 10.1007/BF00384573
Geiger, D. R. & Servaites, J. C. Diurnal regulation of photosynthetic carbon metabolism in C3 plants. Annu. Rev. Plant. Biol. 45, 235–256 (1994).
doi: 10.1146/annurev.pp.45.060194.001315
Liang, F. & Lindblad, P. Synechocystis PCC 6803 overexpressing RuBisCO grow faster with increased photosynthesis. Metab. Eng. Commun. 4, 29–36 (2017).
pubmed: 29468130
pmcid: 5779733
doi: 10.1016/j.meteno.2017.02.002
Eisenhut, M. et al. Metabolome phenotyping of inorganic carbon limitation in cells of the wild type and photorespiratory mutants of the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiol. 148, 2109–2120 (2008).
pubmed: 18945936
pmcid: 2593672
doi: 10.1104/pp.108.129403
Ehleringer, J. R. & Cerling, T. E. C3 and C4 photosynthesis. Encyclop. Glob. Envir. Change 2, 186–190 (2002).
Wu, M. X. & Wedding, R. T. Regulation of phosphoenolpyruvate carboxylase from Crassula by interconversion of oligomeric forms. Archiv. Biochem. Biophys. 240, 655–662 (1985).
doi: 10.1016/0003-9861(85)90073-6
Yu, J. et al. Synechococcus elongatus UTEX 2973, a fast growing cyanobacterial chassis for biosynthesis using light and CO
pubmed: 25633131
pmcid: 5389031
doi: 10.1038/srep08132
Willeford, K. O. & Wedding, R. T. Oligomerization and regulation of higher plant phosphoenolpyruvate carboxylase. Plant Physiol. 99, 755–758 (1992).
pubmed: 16668950
pmcid: 1080529
doi: 10.1104/pp.99.2.755
Jiao, J. A. & Chollet, R. Posttranslational regulation of phosphoenolpyruvate carboxylase in C4 and Crassulacean acid metabolism plants. Plant Physiol. 95, 981–985 (1991).
pubmed: 16668131
pmcid: 1077640
doi: 10.1104/pp.95.4.981
Kai, Y. et al. Three-dimensional structure of phosphoenolpyruvate carboxylase: a proposed mechanism for allosteric inhibition. Proc. Natl. Acad. Sci. 96, 823–828 (1999).
pubmed: 9927652
doi: 10.1073/pnas.96.3.823
Matsumura, H. et al. Crystal structures of C4 form maize and quaternary complex of E. coli phosphoenolpyruvate carboxylases. Structure 10, 1721–1730 (2002).
pubmed: 12467579
doi: 10.1016/S0969-2126(02)00913-9
Durall, C., Rukminasari, N. & Lindblad, P. Enhanced growth at low light intensity in the cyanobacterium Synechocystis PCC 6803 by overexpressing phosphoenolpyruvate carboxylase. Algal Res. 16, 275–281 (2016).
doi: 10.1016/j.algal.2016.03.027
Mukerji, S. K. Corn leaf phosphoenolpyruvate carboxylases: the effect of divalent cations on activity. Archiv. Biochem. Biophys. 182, 352–359 (1977).
doi: 10.1016/0003-9861(77)90316-2
Willeford, K. O., Wu, M. X., Meyer, C. R. & Wedding, R. T. The role of oligomerization in regulation of maize phosphoenolpyruvate carboxylase activity: Influence of Mg-PEP and malate on the oligomeric equilibrium of PEP carboxylase. Biochem. Biophys. Res. Com. 168, 778–785 (1990).
pubmed: 2334435
doi: 10.1016/0006-291X(90)92389-H
Park, S., Lee, W., Kim, H., Pack, S. P. & Lee, J. Characterization of Phosphoenolpyruvate Carboxylase from Oceanimonas smirnovii in Escherichia coli. Appl. Biochem. Biotechnol. 177, 217–25 (2015).
pubmed: 26142903
doi: 10.1007/s12010-015-1739-3
Owttrim, G. W. & Colman, B. Phosphoenolpyruvate carboxylase mediated carbon flow in a cyanobacterium. Biochem. Cell Biol. 66, 93–99 (1988).
doi: 10.1139/o88-012
Hanai, M. et al. The effects of dark incubation on cellular metabolism of the wild type cyanobacterium Synechocystis sp. PCC 6803 and a mutant lacking the transcriptional regulator cyAbrB2. Life 4, 770–787 (2014).
pubmed: 25423139
pmcid: 4284466
doi: 10.3390/life4040770
Price, G. D. Inorganic carbon transporters of the cyanobacterial CO
pubmed: 21359551
doi: 10.1007/s11120-010-9608-y
Coleman, J. R. & Colman, B. Inorganic carbon accumulation and photosynthesis in a blue-green alga as a function of external pH. Plant Physiol. 67, 917–921 (1981).
pubmed: 16661792
pmcid: 425800
doi: 10.1104/pp.67.5.917
Weigend, M. & Hincha, D. K. Quaternary structure of phosphoenolpyruvate carboxylase from CAM-C4-and C3-plants-no evidence for diurnal changes in oligomeric state. J. Plant Physiol. 140, 653–660 (1992).
doi: 10.1016/S0176-1617(11)81019-9
Ozaki, H. & Shiior, I. Regulation of the TCA and glyoxylate cycles in Brevibacterium flavum: II. Regulation of phosphoenolpyruvate carboxylase and pyruvate kinase. J. Biochem. 6, 297–311 (1969).
doi: 10.1093/oxfordjournals.jbchem.a129148
Wong, K. F. & Davies, D. D. Regulation of Phosphoenolpyruvate Carboxylase of Zea mays by Metabolites. Biochem J. 131, 451–458 (1973).
pubmed: 4720710
pmcid: 1177493
doi: 10.1042/bj1310451
Sugiharto, B., Suzuki, I., Burnell, J. N. & Sugiyama, T. Glutamine induces the N-dependent accumulation of mRNAs encoding phosphoenolpyruvate carboxylase and carbonic anhydrase in detached maize leaf tissue. Plant Physiol. 100, 2066–70 (1992).
pubmed: 16653241
pmcid: 1075908
doi: 10.1104/pp.100.4.2066
Swinehart, D. F. The Beer-Lambert Law. J. Chem. Educ. 39, 333–335 (1962).
doi: 10.1021/ed039p333
Förster, S., Apostol, L. & Bras, W. Scatter: software for the analysis of nano-and mesoscale small-angle scattering. J. Appl. Crystallogr. 43, 639–646 (2010).
doi: 10.1107/S0021889810008289
Franke, D. et al. ATSAS 2.8: a comprehensive data analysis suite for small-angle scattering from macromolecular solutions. J. Appl. Crystallogr. 50, 1212–1225 (2017).
pubmed: 28808438
pmcid: 5541357
doi: 10.1107/S1600576717007786
Piiadov, V. et al. SAXSMoW 2.0: Online calculator of the molecular weight of proteins in dilute solution from experimental SAXS data measured on a relative scale. Protein Sci. 28, 454–463 (2019).
pubmed: 30371978
doi: 10.1002/pro.3528
Schneidman-Duhovny, D., Hammel, M., Tainer, J. A. & Sali, A. Accurate SAXS profile computation and its assessment by contrast variation experiments. Biophys. J. 105, 962–974 (2013).
pubmed: 23972848
pmcid: 3752106
doi: 10.1016/j.bpj.2013.07.020
Armougom, F. et al. Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee. Nucleic Acids Res. 34, 604–608 (2006).
doi: 10.1093/nar/gkl092
Codd, G. A. & Stewart, W. D. P. Pathways of glycollate metabolism in the blue-green alga Anabaena Cylindrica. Archiv. Mikrobiol. 94, 11–28 (1973).
doi: 10.1007/BF00414075