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Biophysical Reviews

, Volume 10, Issue 2, pp 153–162 | Cite as

Molecular evolution of an oligomeric biocatalyst functioning in lysine biosynthesis

  • Tatiana P. Soares da Costa
  • Belinda M. Abbott
  • Anthony R. Gendall
  • Santosh Panjikar
  • Matthew A. Perugini
Review

Abstract

Dihydrodipicolinate synthase (DHDPS) is critical to the production of lysine through the diaminopimelate (DAP) pathway. Elucidation of the function, regulation and structure of this key class I aldolase has been the focus of considerable study in recent years, given that the dapA gene encoding DHDPS has been found to be essential to bacteria and plants. Allosteric inhibition by lysine is observed for DHDPS from plants and some bacterial species, the latter requiring a histidine or glutamate at position 56 (Escherichia coli numbering) over a basic amino acid. Structurally, two DHDPS monomers form the active site, which binds pyruvate and (S)-aspartate β-semialdehyde, with most dimers further dimerising to form a tetrameric arrangement around a solvent-filled centre cavity. The architecture and behaviour of these dimer-of-dimers is explored in detail, including biophysical studies utilising analytical ultracentrifugation, small-angle X-ray scattering and macromolecular crystallography that show bacterial DHDPS tetramers adopt a head-to-head quaternary structure, compared to the back-to-back arrangement observed for plant DHDPS enzymes. Finally, the potential role of pyruvate in providing substrate-mediated stabilisation of DHDPS is considered.

Keywords

Allostery Antibiotic Crystal Herbicide SAXS Sedimentation 

Notes

Acknowledgements

We would like to thank the present and past members of the Perugini laboratory for their contributions over the past 15 years and their helpful discussions during the preparation of this review. We also acknowledge the Australian Synchrotron and the La Trobe University—Comprehensive Proteomics Platform for providing infrastructure that has supported the primary research reviewed here, and the Australian Research Council, Defence Threat Reduction Agency, La Trobe University Research Focus Area—Securing Food, Water & the Environment, and National Health & Medical Research Council for contributing to funding over the past 15 years to the research described in this review.

Compliance with ethical standards

Conflict of interest

Tatiana P. Soares da Costa declares that she has no conflict of interest. Belinda M. Abbott declares that she has no conflict of interest. Anthony R. Gendall declares that he has no conflict of interest. Santosh Panjikar declares that he has no conflict of interest. Matthew A. Perugini declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Aghaie A, Lechaplais C, Sirven P et al (2008) New insights into the alternative D-glucarate degradation pathway. J Biol Chem 283:15638–15646.  https://doi.org/10.1074/jbc.M800487200 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Atkinson SC, Dogovski C, Newman J, Dobson RC, Perugini MA (2011) Cloning, expression, purification and crystallization of dihydrodipicolinate synthase from the grapevine Vitis vinifera. Acta Crystallogr Sect F Struct Biol Cryst Commun 67:1537–1541.  https://doi.org/10.1107/s1744309111038395 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Atkinson SC, Dogovski C, Dobson RC, Perugini MA (2012a) Cloning, expression, purification and crystallization of dihydrodipicolinate synthase from Agrobacterium tumefaciens. Acta Crystallogr Sect F Struct Biol Cryst Commun 68:1040–1047.  https://doi.org/10.1107/s1744309112033052 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Atkinson SC, Dogovski C, Downton MT et al (2012b) Crystal, solution and in silico structural studies of dihydrodipicolinate synthase from the common grapevine. PLoS One 7:e38318.  https://doi.org/10.1371/journal.pone.0038318 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Atkinson SC, Dogovski C, Downton MT et al (2013) Structural, kinetic and computational investigation of Vitis vinifera DHDPS reveals new insight into the mechanism of lysine-mediated allosteric inhibition. Plant Mol Biol 81:431–446.  https://doi.org/10.1007/s11103-013-0014-7 CrossRefPubMedGoogle Scholar
  6. Atkinson SC, Hor L, Dogovski C, Dobson RC, Perugini MA (2014) Identification of the bona fide DHDPS from a common plant pathogen. Proteins 82:1869–1883.  https://doi.org/10.1002/prot.24539 CrossRefPubMedGoogle Scholar
  7. Bakhiet N, Forney FW, Stahly DP, Daniels L (1984) Lysine biosynthesis in Methanobacterium thermoautotrophicum is by the diaminopimelic acid pathway. Curr Microbiol 10:195–198.  https://doi.org/10.1007/BF01627254 CrossRefGoogle Scholar
  8. Barbosa JA, Smith BJ, DeGori R et al (2000) Active site modulation in the N-acetylneuraminate lyase sub-family as revealed by the structure of the inhibitor-complexed Haemophilus influenzae enzyme. J Mol Biol 303:405–421.  https://doi.org/10.1006/jmbi.2000.4138 CrossRefPubMedGoogle Scholar
  9. Becker D, Selbach M, Rollenhagen C et al (2006) Robust Salmonella metabolism limits possibilities for new antimicrobials. Nature 440:303–307.  https://doi.org/10.1038/nature04616 CrossRefPubMedGoogle Scholar
  10. Blickling S, Beisel HG, Bozic D, Knäblein J, Laber B, Huber R (1997a) Structure of dihydrodipicolinate synthase of Nicotiana sylvestris reveals novel quaternary structure. J Mol Biol 274:608–621.  https://doi.org/10.1006/jmbi.1997.1393 CrossRefPubMedGoogle Scholar
  11. Blickling S, Renner C, Laber B, Pohlenz HD, Holak TA, Huber R (1997b) Reaction mechanism of Escherichia coli dihydrodipicolinate synthase investigated by X-ray crystallography and NMR spectroscopy. Biochemistry 36:24–33.  https://doi.org/10.1021/bi962272d CrossRefPubMedGoogle Scholar
  12. Brookes E, Cao W, Demeler B (2010) A two-dimensional spectrum analysis for sedimentation velocity experiments of mixtures with heterogeneity in molecular weight and shape. Eur Biophys J 39:405–414.  https://doi.org/10.1007/s00249-009-0413-5 CrossRefPubMedGoogle Scholar
  13. Bukhari AI, Taylor AL (1971) Genetic analysis of diaminopimelic acid- and lysine-requiring mutants of Escherichia coli. J Bacteriol 105:844–854PubMedPubMedCentralGoogle Scholar
  14. Burgess BR, Dobson RC, Bailey MF et al (2008a) Structure and evolution of a novel dimeric enzyme from a clinically important bacterial pathogen. J Biol Chem 283:27598–27603.  https://doi.org/10.1074/jbc.M804231200 CrossRefPubMedGoogle Scholar
  15. Burgess BR, Dobson RC, Dogovski C, Jameson GB, Parker MW, Perugini MA (2008b) Purification, crystallization and preliminary X-ray diffraction studies to near-atomic resolution of dihydrodipicolinate synthase from methicillin-resistant Staphylococcus aureus. Acta Crystallogr Sect F Struct Biol Cryst Commun 64:659–661.  https://doi.org/10.1107/s1744309108016746 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Butour JL, Felenbok B, Patte JC (1974) Synthesis of dihydrodipicolinate synthetase in Escherichia coli K12. Ann Microbiol 125:459–462Google Scholar
  17. Cahyanto MN, Kawasaki H, Nagashio M, Fujiyama K, Seki T (2006) Regulation of aspartokinase, aspartate semialdehyde dehydrogenase, dihydrodipicolinate synthase and dihydrodipicolinate reductase in Lactobacillus plantarum. Microbiology 152:105–112.  https://doi.org/10.1099/mic.0.28092-0 CrossRefPubMedGoogle Scholar
  18. Chen NY, Jiang SQ, Klein DA, Paulus H (1993) Organization and nucleotide sequence of the Bacillus subtilis diaminopimelate operon, a cluster of genes encoding the first three enzymes of diaminopimelate synthesis and dipicolinate synthase. J Biol Chem 268:9448–9465PubMedGoogle Scholar
  19. Christensen JB, Soares da Costa TP, Faou P, Pearce FG, Panjikar S, Perugini MA (2016) Structure and function of cyanobacterial DHDPS and DHDPR. Sci Rep 6:37111.  https://doi.org/10.1038/srep37111 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Cremer J, Treptow C, Eggeling L, Sahm H (1988) Regulation of enzymes of lysine biosynthesis in Corynebacterium glutamicum. Microbiol 134:3221–3229.  https://doi.org/10.1099/00221287-134-12-3221 CrossRefGoogle Scholar
  21. Demeler B, van Holde KE (2004) Sedimentation velocity analysis of highly heterogeneous systems. Anal Biochem 335:279–288.  https://doi.org/10.1016/j.ab.2004.08.039 CrossRefPubMedGoogle Scholar
  22. Dereppe C, Bold G, Ghisalba O, Ebert E, Schär HP (1992) Purification and characterization of dihydrodipicolinate synthase from pea. Plant Physiol 98:813–821CrossRefPubMedPubMedCentralGoogle Scholar
  23. Devenish SR, Huisman FH, Parker EJ, Hadfield AT, Gerrard JA (2009) Cloning and characterisation of dihydrodipicolinate synthase from the pathogen Neisseria meningitidis. Biochim Biophys Acta 1794:1168–1174.  https://doi.org/10.1016/j.bbapap.2009.02.003 CrossRefPubMedGoogle Scholar
  24. Dobson RC, Griffin MD, Roberts SJ, Gerrard JA (2004) Dihydrodipicolinate synthase (DHDPS) from Escherichia coli displays partial mixed inhibition with respect to its first substrate, pyruvate. Biochimie 86:311–315.  https://doi.org/10.1016/j.biochi.2004.03.008 CrossRefPubMedGoogle Scholar
  25. Dobson RC, Griffin MD, Jameson GB, Gerrard JA (2005) The crystal structures of native and (S)-lysine-bound dihydrodipicolinate synthase from Escherichia coli with improved resolution show new features of biological significance. Acta Crystallogr D Biol Crystallogr 61:1116–1124.  https://doi.org/10.1107/s0907444905016318 CrossRefPubMedGoogle Scholar
  26. Dogovski C, Atkinson SC, Dommaraju SR et al (2009) Lysine biosynthesis in bacteria: an unchartered pathway for novel antibiotic design. Encycl Life Supp Syst 11:116–136Google Scholar
  27. Dogovski C, Atkinson SC, Dommaraju SR et al (2012) Enzymology of bacterial lysine biosynthesis. In: Ekinci D (ed) Biochemistry. InTech Open Access Publisher, pp 225–262Google Scholar
  28. Dogovski C, Gorman MA, Ketaren NE et al (2013) From knock-out phenotype to three-dimensional structure of a promising antibiotic target from Streptococcus pneumoniae. PLoS One 8:e83419.  https://doi.org/10.1371/journal.pone.0083419 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Domigan LJ, Scally SW, Fogg MJ et al (2009) Characterisation of dihydrodipicolinate synthase (DHDPS) from Bacillus anthracis. Biochim Biophys Acta 1794:1510–1516.  https://doi.org/10.1016/j.bbapap.2009.06.020 CrossRefPubMedGoogle Scholar
  30. Dommaraju S, Gorman MA, Dogovski C et al (2010) Cloning, expression and crystallization of dihydrodipicolinate reductase from methicillin-resistant Staphylococcus aureus. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:57–60.  https://doi.org/10.1107/s1744309109047964 CrossRefPubMedGoogle Scholar
  31. Dommaraju SR, Dogovski C, Czabotar PE, Hor L, Smith BJ, Perugini MA (2011) Catalytic mechanism and cofactor preference of dihydrodipicolinate reductase from methicillin-resistant Staphylococcus aureus. Arch Biochem Biophys 512:167–174.  https://doi.org/10.1016/j.abb.2011.06.006 CrossRefPubMedGoogle Scholar
  32. Evans G, Schuldt L, Griffin MD et al (2011) A tetrameric structure is not essential for activity in dihydrodipicolinate synthase (DHDPS) from Mycobacterium tuberculosis. Arch Biochem Biophys 512:154–159.  https://doi.org/10.1016/j.abb.2011.05.014 CrossRefPubMedGoogle Scholar
  33. Forsyth RA, Haselbeck RJ, Ohlsen KL et al (2002) A genome-wide strategy for the identification of essential genes in Staphylococcus aureus. Mol Microbiol 43:1387–1400CrossRefPubMedGoogle Scholar
  34. Frisch DA, Gengenbach BG, Tommey AM, Sellner JM, Somers DA, Myers DE (1991) Isolation and characterization of dihydrodipicolinate synthase from maize. Plant Physiol 96:444–452CrossRefPubMedPubMedCentralGoogle Scholar
  35. Frizzi A, Huang S, Gilbertson LA, Armstrong TA, Luethy MH, Malvar TM (2008) Modifying lysine biosynthesis and catabolism in corn with a single bifunctional expression/silencing transgene cassette. Plant Biotechnol J 6:13–21.  https://doi.org/10.1111/j.1467-7652.2007.00290.x PubMedGoogle Scholar
  36. Fullerton SW, Griffiths JS, Merkel AB et al (2006) Mechanism of the Class I KDPG aldolase. Bioorg Med Chem 14:3002–3010.  https://doi.org/10.1016/j.bmc.2005.12.022 CrossRefPubMedGoogle Scholar
  37. García-Rodríguez FM, Zekri S, Toro N (2000) Characterization of the Sinorhizobium meliloti genes encoding a functional dihydrodipicolinate synthase (dapA) and dihydrodipicolinate reductase (dapB). Arch Microbiol 173:438–444CrossRefPubMedGoogle Scholar
  38. Gefflaut T, Blonski C, Perie J, Willson M (1995) Class I aldolases: substrate specificity, mechanism, inhibitors and structural aspects. Prog Biophys Mol Biol 63:301–340CrossRefPubMedGoogle Scholar
  39. Gerdes SY, Scholle MD, Campbell JW et al (2003) Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J Bacteriol 185:5673–5684CrossRefPubMedPubMedCentralGoogle Scholar
  40. Ghislain M, Frankard V, Jacobs M (1995) A dinucleotide mutation in dihydrodipicolinate synthase of Nicotiana sylvestris leads to lysine overproduction. Plant J 8:733–743CrossRefPubMedGoogle Scholar
  41. Girish TS, Sharma E, Gopal B (2008) Structural and functional characterization of Staphylococcus aureus dihydrodipicolinate synthase. FEBS Lett 582:2923–2930.  https://doi.org/10.1016/j.febslet.2008.07.035 CrossRefPubMedGoogle Scholar
  42. Gordon SE, Weber DK, Downton MT, Wagner J, Perugini MA (2016) Dynamic modelling reveals ‘hotspots’ on the pathway to enzyme–substrate complex formation. PLoS Comput Biol 12:e1004811.  https://doi.org/10.1371/journal.pcbi.1004811 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Griffin MD, Dobson RC, Pearce FG et al (2008) Evolution of quaternary structure in a homotetrameric enzyme. J Mol Biol 380:691–703.  https://doi.org/10.1016/j.jmb.2008.05.038 CrossRefPubMedGoogle Scholar
  44. Griffin MD, Dobson RC, Gerrard JA, Perugini MA (2010) Exploring the dihydrodipicolinate synthase tetramer: how resilient is the dimer–dimer interface? Arch Biochem Biophys 494:58–63.  https://doi.org/10.1016/j.abb.2009.11.014 CrossRefPubMedGoogle Scholar
  45. Griffin MD, Billakanti JM, Wason A et al (2012) Characterisation of the first enzymes committed to lysine biosynthesis in Arabidopsis thaliana. PLoS One 7:e40318.  https://doi.org/10.1371/journal.pone.0040318 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Gunji Y, Tsujimoto N, Shimaoka M, Ogawa-Miyata Y, Sugimoto S, Yasueda H (2004) Characterization of the L-lysine biosynthetic pathway in the obligate methylotroph Methylophilus methylotrophus. Biosci Biotechnol Biochem 68:1449–1460.  https://doi.org/10.1271/bbb.68.1449 CrossRefPubMedGoogle Scholar
  47. Halling SM, Stahly DP (1976) Dihydrodipicolinic acid synthase of bacillus licheniformis. Quaternary structure, kinetics, and stability in the presence of sodium chloride and substrates. Biochim Biophys Acta 452:580–596CrossRefPubMedGoogle Scholar
  48. Hudson AO, Bless C, Macedo P, Chatterjee SP, Singh BK, Gilvarg C, Leustek T (2005) Biosynthesis of lysine in plants: evidence for a variant of the known bacterial pathways. Biochim Biophys Acta 1721:27–36.  https://doi.org/10.1016/j.bbagen.2004.09.008 CrossRefPubMedGoogle Scholar
  49. Hutton CA, Perugini MA, Gerrard JA (2007) Inhibition of lysine biosynthesis: an evolving antibiotic strategy. Mol BioSyst 3:458–465.  https://doi.org/10.1039/b705624a CrossRefPubMedGoogle Scholar
  50. Izard T, Lawrence MC, Malby RL, Lilley GG, Colman PM (1994) The three-dimensional structure of N-acetylneuraminate lyase from Escherichia coli. Structure 2:361–369CrossRefPubMedGoogle Scholar
  51. Joerger AC, Mayer S, Fersht AR (2003) Mimicking natural evolution in vitro: an N-acetylneuraminate lyase mutant with an increased dihydrodipicolinate synthase activity. Proc Natl Acad Sci U S A 100:5694–5699.  https://doi.org/10.1073/pnas.0531477100 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Jones-Held S, Ambrozevicius LP, Campbell M, Drumheller B, Harrington E, Leustek T (2012) Two Arabidopsis thaliana dihydrodipicolinate synthases, DHDPS1 and DHDPS2, are unequally redundant. Funct Plant Biol 39:1058–1067.  https://doi.org/10.1071/FP12169 CrossRefGoogle Scholar
  53. Kaneko T, Hashimoto T, Kumpaisal R, Yamada Y (1990) Molecular cloning of wheat dihydrodipicolinate synthase. J Biol Chem 265:17451–17455PubMedGoogle Scholar
  54. Kaur N, Gautam A, Kumar S et al (2011) Biochemical studies and crystal structure determination of dihydrodipicolinate synthase from Pseudomonas aeruginosa. Int J Biol Macromol 48:779–787.  https://doi.org/10.1016/j.ijbiomac.2011.03.002 CrossRefPubMedGoogle Scholar
  55. Kobayashi K, Ehrlich SD, Albertini A et al (2003) Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A 100:4678–4683.  https://doi.org/10.1073/pnas.0730515100 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774–797.  https://doi.org/10.1016/j.jmb.2007.05.022 CrossRefPubMedGoogle Scholar
  57. Kumpaisal R, Hashimoto T, Yamada Y (1987) Purification and characterization of dihydrodipicolinate synthase from wheat suspension cultures. Plant Physiol 85:145–151CrossRefPubMedPubMedCentralGoogle Scholar
  58. Laber B, Gomis-Rüth FX, Romao MJ, Huber R (1992) Escherichia coli dihydrodipicolinate synthase. Identification of the active site and crystallization. Biochem J 288(Pt 2):691–695CrossRefPubMedPubMedCentralGoogle Scholar
  59. Lawrence MC, Barbosa JA, Smith BJ et al (1997) Structure and mechanism of a sub-family of enzymes related to N-acetylneuraminate lyase. J Mol Biol 266:381–399.  https://doi.org/10.1006/jmbi.1996.0769 CrossRefPubMedGoogle Scholar
  60. Matthews BF, Widholm JM (1979) Expression of aspartokinase, dihydrodipicolinic acid synthase and homoserine dehydrogenase during growth of carrot cell suspension cultures on lysine- and threonine-supplemented media. Z Naturforsch C Biosci 34:1177–1185Google Scholar
  61. Mirwaldt C, Korndorfer I, Huber R (1995) The crystal structure of dihydrodipicolinate synthase from Escherichia coli at 2.5 Å resolution. J Mol Biol 246:227–239.  https://doi.org/10.1006/jmbi.1994.0078 CrossRefPubMedGoogle Scholar
  62. Mitsakos V, Dobson RC, Pearce FG et al (2008) Inhibiting dihydrodipicolinate synthase across species: towards specificity for pathogens? Bioorg Med Chem Lett 18:842–844.  https://doi.org/10.1016/j.bmcl.2007.11.026 CrossRefPubMedGoogle Scholar
  63. Miyazaki T, Miyazaki J, Yamane H, Nishiyama M (2004) α-Aminoadipate aminotransferase from an extremely thermophilic bacterium, Thermus thermophilus. Microbiology 150:2327–2334.  https://doi.org/10.1099/mic.0.27037-0 CrossRefPubMedGoogle Scholar
  64. Muscroft-Taylor AC, Soares da Costa TP, Gerrard JA (2010) New insights into the mechanism of dihydrodipicolinate synthase using isothermal titration calorimetry. Biochimie 92:254–262.  https://doi.org/10.1016/j.biochi.2009.12.004 CrossRefPubMedGoogle Scholar
  65. Nelson TG, Ramsay GD, Perugini MA (2016) Fluorescence-detection system. In: Uchiyama S, Arisaka F, Stafford WF, Laue TM (eds) Analytical ultracentrifugation: instrumentation, software, and application. Springer, Tokyo, pp 39-61Google Scholar
  66. Panchy N, Lehti-Shiu M, Shiu SH (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316.  https://doi.org/10.1104/pp.16.00523 PubMedPubMedCentralGoogle Scholar
  67. Pearce FG, Dobson RC, Weber A et al (2008) Mutating the tight-dimer interface of dihydrodipicolinate synthase disrupts the enzyme quaternary structure: toward a monomeric enzyme. Biochemistry 47:12108–12117.  https://doi.org/10.1021/bi801094t CrossRefPubMedGoogle Scholar
  68. Perugini MA, Griffin MD, Smith BJ et al (2005) Insight into the self-association of key enzymes from pathogenic species. Eur Biophys J 34:469–476.  https://doi.org/10.1007/s00249-005-0491-y CrossRefPubMedGoogle Scholar
  69. Peverelli MG, Soares da Costa TP, Kirby N, Perugini MA (2016) Dimerization of bacterial diaminopimelate decarboxylase is essential for catalysis. J Biol Chem 291:9785–9795.  https://doi.org/10.1074/jbc.M115.696591 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Phenix CP, Palmer DR (2008) Isothermal titration microcalorimetry reveals the cooperative and noncompetitive nature of inhibition of Sinorhizobium meliloti L5-30 dihydrodipicolinate synthase by (S)-lysine. Biochemistry 47:7779–7781.  https://doi.org/10.1021/bi800629n CrossRefPubMedGoogle Scholar
  71. Pisabarro A, Malumbres M, Mateos LM, Oguiza JA, Martin JF (1993) A cluster of three genes (dapA, orf2, and dapB) of Brevibacterium lactofermentum encodes dihydrodipicolinate synthase, dihydrodipicolinate reductase, and a third polypeptide of unknown function. J Bacteriol 175:2743–2749CrossRefPubMedPubMedCentralGoogle Scholar
  72. Ray SS, Bonanno JB, Rajashankar KR et al (2002) Cocrystal structures of diaminopimelate decarboxylase: mechanism, evolution, and inhibition of an antibiotic resistance accessory factor. Structure 10:1499–1508CrossRefPubMedGoogle Scholar
  73. Richaud F, Richaud C, Ratet P, Patte JC (1986) Chromosomal location and nucleotide sequence of the Escherichia coli dapA gene. J Bacteriol 166:297–300CrossRefPubMedPubMedCentralGoogle Scholar
  74. Shedlarski JG, Gilvarg C (1970) The pyruvate-aspartic semialdehyde condensing enzyme of Escherichia coli. J Biol Chem 245:1362–1373PubMedGoogle Scholar
  75. Siddiqui T, Paxman JJ, Dogovski C, Panjikar S, Perugini MA (2013) Cloning to crystallization of dihydrodipicolinate synthase from the intracellular pathogen Legionella pneumophila. Acta Crystallogr Sect F Struct Biol Cryst Commun 69:1177–1181.  https://doi.org/10.1107/s1744309113024639 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Silk GW, Matthews BF, Somers DA, Gengenbach BG (1994) Cloning and expression of the soybean DapA gene encoding dihydrodipicolinate synthase. Plant Mol Biol 26:989–993CrossRefPubMedGoogle Scholar
  77. Skovpen YV, Palmer DR (2013) Dihydrodipicolinate synthase from Campylobacter jejuni: kinetic mechanism of cooperative allosteric inhibition and inhibitor-induced substrate cooperativity. Biochemistry 52:5454–5462.  https://doi.org/10.1021/bi400693w CrossRefPubMedGoogle Scholar
  78. Soares da Costa TP, Muscroft-Taylor AC, Dobson RC, Devenish SR, Jameson GB, Gerrard JA (2010) How essential is the ‘essential’ active-site lysine in dihydrodipicolinate synthase? Biochimie 92:837–845.  https://doi.org/10.1016/j.biochi.2010.03.004 CrossRefPubMedGoogle Scholar
  79. Soares da Costa TP, Christensen JB, Desbois S et al (2015) Quaternary structure analyses of an essential oligomeric enzyme. Methods Enzymol 562:205–223.  https://doi.org/10.1016/bs.mie.2015.06.020 CrossRefPubMedGoogle Scholar
  80. Soares da Costa TP, Desbois S, Dogovski C et al (2016) Structural determinants defining the allosteric inhibition of an essential antibiotic target. Structure 24:1282–1291.  https://doi.org/10.1016/j.str.2016.05.019 CrossRefPubMedGoogle Scholar
  81. Soares da Costa TP, Patel M, Desbois S, Gupta R, Faou P, Perugini MA (2017) Identification of a dimeric KDG aldolase from Agrobacterium tumefaciens. Proteins 85:2058–2065.  https://doi.org/10.1002/prot.25359 CrossRefPubMedGoogle Scholar
  82. Tam PH, Phenix CP, Palmer DR (2004) MosA, a protein implicated in rhizopine biosynthesis in Sinorhizobium meliloti L5-30, is a dihydrodipicolinate synthase. J Mol Biol 335:393–397CrossRefPubMedGoogle Scholar
  83. Theodossis A, Walden H, Westwick EJ et al (2004) The structural basis for substrate promiscuity in 2-keto-3-deoxygluconate aldolase from the Entner–Doudoroff pathway in Sulfolobus solfataricus. J Biol Chem 279:43886–43892.  https://doi.org/10.1074/jbc.M407702200 CrossRefPubMedGoogle Scholar
  84. Torruella G, Suga H, Riutort M, Peretó J, Ruiz-Trillo I (2009) The evolutionary history of lysine biosynthesis pathways within eukaryotes. J Mol Evol 69:240–248.  https://doi.org/10.1007/s00239-009-9266-x CrossRefPubMedGoogle Scholar
  85. Ufaz S, Galili G (2008) Improving the content of essential amino acids in crop plants: goals and opportunities. Plant Physiol 147:954–961.  https://doi.org/10.1104/pp.108.118091 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Van Holde KE, Weischet WO (1978) Boundary analysis of sedimentation-velocity experiments with monodisperse and paucidisperse solutes. Biopolymers 17:1387–1403.  https://doi.org/10.1002/bip.1978.360170602 CrossRefGoogle Scholar
  87. Vauterin M, Jacobs M (1994) Isolation of a poplar and an Arabidopsis thaliana dihydrodipicolinate synthase cDNA clone. Plant Mol Biol 25:545–550CrossRefPubMedGoogle Scholar
  88. Velasco AM, Leguina JI, Lazcano A (2002) Molecular evolution of the lysine biosynthetic pathways. J Mol Evol 55:445–449.  https://doi.org/10.1007/s00239-002-2340-2 CrossRefPubMedGoogle Scholar
  89. Voss JE, Scally SW, Taylor NL et al (2010) Substrate-mediated stabilization of a tetrameric drug target reveals Achilles heel in anthrax. J Biol Chem 285:5188–5195.  https://doi.org/10.1074/jbc.M109.038166 CrossRefPubMedGoogle Scholar
  90. Wallsgrove RM, Mazelis M (1980) The enzymology of lysine biosynthesis in higher plants: complete localization of the regulatory enzyme dihydrodipicolinate synthase in the chloroplasts of spinach leaves. FEBS Lett 116:189–192CrossRefPubMedGoogle Scholar
  91. Webster FH, Lechowich RV (1970) Partial purification and characterization of dihydrodipicolinic acid synthetase from sporulating Bacillus megaterium. J Bacteriol 101:118–126PubMedPubMedCentralGoogle Scholar
  92. Wolterink-van Loo S, Levisson M, Cabrieres MC, Franssen MC, van der Oost J (2008) Characterization of a thermostable dihydrodipicolinate synthase from Thermoanaerobacter tengcongensis. Extremophiles 12:461–469.  https://doi.org/10.1007/s00792-008-0152-z CrossRefPubMedGoogle Scholar
  93. Wubben JM, Dogovski C, Dobson RC et al (2010) Cloning, expression, purification and crystallization of dihydrodipicolinate synthase from the psychrophile Shewanella benthica. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:1511–1516.  https://doi.org/10.1107/s1744309110036791 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Xu H, Andi B, Qian J, West AH, Cook PF (2006) The α-aminoadipate pathway for lysine biosynthesis in fungi. Cell Biochem Biophys 46:43–64.  https://doi.org/10.1385/cbb:46:1:43 CrossRefPubMedGoogle Scholar
  95. Yamakura F, Ikeda Y, Kimura K, Sasakawa T (1974) Partial purification and some properties of pyruvate-aspartic semialdehyde condensing enzyme from sporulating Bacillus subtilis. J Biochem 76:611–621CrossRefPubMedGoogle Scholar
  96. Yugari Y, Gilvarg C (1965) The condensation step in diaminopimelate synthesis. J Biol Chem 240:4710–4716PubMedGoogle Scholar

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© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Biochemistry and Genetics, La Trobe Institute for Molecular ScienceLa Trobe UniversityMelbourneAustralia
  2. 2.Department of Chemistry and Physics, La Trobe Institute for Molecular ScienceLa Trobe UniversityMelbourneAustralia
  3. 3.Department of Animal, Plant and Soil Sciences, AgriBio, Centre for AgriBiosciencesLa Trobe UniversityBundooraAustralia
  4. 4.Australian SynchrotronClayton, MelbourneAustralia
  5. 5.Department of Biochemistry and Molecular BiologyMonash UniversityMelbourneAustralia

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