Research Article
Crystal structure of a trimeric archaeal adenylate kinase from the mesophile Methanococcus maripaludis with an unusually broad functional range and thermal stability
Milya Davlieva,
Yousif Shamoo,
Milya Davlieva
Department of Biochemistry and Cell Biology, Rice University, Houston, Texas 77005-1892
Search for more papers by this authorCorresponding Author
Yousif Shamoo
Department of Biochemistry and Cell Biology, Rice University, Houston, Texas 77005-1892
Department of Biochemistry and Cell Biology, Rice University, 6100 Main St. MS-140, Houston, TX 7005-1892===Search for more papers by this authorMilya Davlieva,
Yousif Shamoo,
Milya Davlieva
Department of Biochemistry and Cell Biology, Rice University, Houston, Texas 77005-1892
Search for more papers by this authorCorresponding Author
Yousif Shamoo
Department of Biochemistry and Cell Biology, Rice University, Houston, Texas 77005-1892
Department of Biochemistry and Cell Biology, Rice University, 6100 Main St. MS-140, Houston, TX 7005-1892===Search for more papers by this authorAbstract
The structure of the trimeric adenylate kinase from the Archaebacteria Methanococcus mariplaludis (AKMAR) has been solved to 2.5-Å resolution and the temperature dependent stability and kinetics of the enzyme measured. The KM and Vmax of AKMAR exhibit only modest temperature dependence from 30°–60°C. Although M. mariplaludis is a mesophile with a maximum growth temperature of 43°C, AKMAR has a very broad functional range and stability (Tm = 74.0°C) that are more consistent with a thermophilic enzyme with high thermostability and exceptional activity over a wide range of temperatures, suggesting that this microbe may have only recently invaded a mesophilic niche and has yet to fully adapt. A comparison of the Local Structural Entropy (LSE) for AKMAR to the related adenylate kinases from the mesophile Methanococcus voltae and thermophile Methanococcus thermolithotrophicus show that changes in LSE are able to fully account for the intermediate stability of AKMAR and highlights a general mechanism for protein adaptation in this class of enzymes. Proteins 2010. © 2009 Wiley-Liss, Inc.
REFERENCES
- 1 Counago R,Shamoo Y. Gene replacement of adenylate kinase in the gram-positive thermophile Geobacillus stearothermophilus disrupts adenine nucleotide homeostasis and reduces cell viability. Extremophiles 2005; 9: 135–144.
- 2 Counago R,Chen S,Shamoo Y. In vivo molecular evolution reveals biophysical origins of organismal fitness. Mol Cell 2006; 22: 441–449.
- 3 Counago R,Wilson CJ,Pena MI,Wittung-Stafshede P,Shamoo Y. An adaptive mutation in adenylate kinase that increases organismal fitness is linked to stability-activity trade-offs. Protein Eng Des Sel 2008; 21: 19–27.
- 4 Henzler-Wildman KA,Lei M,Thai V,Kerns JS,Martin Karplus M,Kern D. A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 2007; 450: 913–916.
- 5 Whitford PC,Gosavi S,Onuchic JN. Conformational transitions in adenylate kinase. Allosteric communication reduces misligation J Biol Chem 2008; 283: 2042–2048.
- 6 Bae E,Bannen RM,Phillips GNJr. Bioinformatic method for protein thermal stabilization by structural entropy optimization. Proc Natl Acad Sci U S A 2008; 105: 9594–9597.
- 7 Lu Q,Wang J. Single molecule conformational dynamics of adenylate kinase: energy landscape, structural correlations, and transition state ensembles. J Am Chem Soc 2008; 130: 4772–4783.
- 8 Whitford PC,Miyashita O,Levy Y,Onuchic JN. Conformational transitions of adenylate kinase: switching by cracking. J Mol Biol 2007; 366: 1661–1671.
- 9 Arora K,Brooks CL3rd. Large-scale allosteric conformational transitions of adenylate kinase appears to involve a population-shift mechanism. Proc Natl Acad Sci U S A 2007; 104: 18496–18501.
- 10 Bae E,Phillips GNJr. Roles of static and dynamic domains in stability and catalysis of adenylate kinase. Proc Nat Acad Sci U S A 2006; 103: 2132–2137.
- 11 Wolf-Watz M,Thai V,Henzler-Wildman KA,Hadjipavlou G,Eisenmesser EZ,Kern D. Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nat Struct Mol Biol 2004; 11: 945–949.
- 12 Bae E,Phillips GNJr. Structures and analysis of highly homologous psychrophilic, mesophilic, and thermophilic adenylate kinases. J Biol Chem 2004; 279: 28202–28208.
- 13 Criswell AR,Bae E,Stec B,Konisky J,Phillips GNJr. Structures of thermophilic and mesophilic adenylate kinases from the genus Methanococcus. J Mol Biol 2003; 330: 1087–1099.
- 14 Rusnak P,Haney P,Konisky J. The adenylate kinases from a mesophilic and three thermophilic methanogenic members of the archaea. J Bacteriol 1995; 177: 2977–2981.
- 15 Haney PJ,Stess M,Konisky J. Analysis of thermal stabilizing interactions in mesophilic and thermophilic adenylate kinases from genus Methanococcus. J Biol Chem 1999; 274: 28453–28458.
- 16 Liu Y,Guo L,Guo R,Wong RL,Hernandez H,Hu J,Chu Y,Amster IJ,Whitman WB,Huang L. The Sac10b homolog in Methanococcus maripaludis Binds DNA at Specific Sites. J Bacteriol 2009; 191: 2315–2329.
- 17 Glaser P,Presecan E,Delepierre M,Surewicz WK,Mantsch HH,Barzu O Gilles AM. Zinc, a novel structural element found in the family of bacterial adenylate kinases. Biochemistry 1992; 31: 3038–3043.
- 18 John DM,Weeks KM. Van't Hoff enthalpies without baselines. Protein Sci 2000; 9: 1416–1419.
- 19 Jancaric J,Kim SH. Sparse matrix sampling: a screening method for crystallization of proteins. J Appl Cryst 1991; 24: 409–411.
- 20 Pfugrath JW. The finer things in the X-ray diffraction data collection. Acta Crystallogr D Biol Crystallogr 1999; 55: 1718–1725.
- 21 McCoy AJ,Grosse-Kunstleve RW,Adams PD,Winn MD,Storoni LC,Read RJ. Phaser crystallographic software. J Appl Cryst 2007; 40: 658–674.
- 22 Potterton E,Briggs P,Turkenburg M,Dodson E. A graphical user interface to the CCP4 program suite. Acta Crystallogr D Biol Crystallogr 2003; 59: 1131–1137.
- 23 Kantardjieff KA,Rupp B. Matthews coefficient probabilities: Improved estimates for unit cell contents of proteins, DNA, and protein-nucleic acid complex. Protein Sci 2003; 12: 1865–1871.
- 24 Brunger AT,Adams PD,Clore GM,Delano WL,Gros P,Grosse-Kunstleve RW Jiang JS,Kuszewski J,Nilges M,Pannu NS,Read RJ,Rice LM,Simonson T,Warren GL. Crystallography and NMR system (CNS): a new software system for macromolecular structure determination. Acta Crystallog sect D 1998; 54: 905–921.
- 25 Adams PD,Grosse-Kunstleve RW,Hung LW,Ioerger TR,McCoy AJ,Moriarty NW,Read RJ,Sacchettini JC,Sauter NK,Terwilliger TC. Phenix: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 2002; 58: 1948–1954.
- 26 Murshudov GN,Vagin AA,Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 1997; 53(Part 3): 240–255.
- 27 Emsley P,Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Part 12 Part 1): 2126–2132, 2004.
- 28 Painter J,Merritt EA. TLSMD web server for the generation of multi-group TLS models. J Appl Cryst 2006; 39: 109–111.
- 29 Davis IW,Leaver-Fay A,Chen VB,Block JN,Kapral GJ,Wang X,Murray LW,Arendall WB,Snoeyink J,Richardson JS,Richardson DC. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 2007; 35: W375–W383.
- 30 Kath T,Schmid R,Schafer G. Identification, cloning, and expression of the gene for adenylate kinase from the thermoacidophilic archaebacterium Sulfolobus acidocaldarius. Arch Biochem Biophys 1993; 307: 407–410.
- 31 Lacher K,Schafer G. Archaebacterial adenylate kinase from the thermoacidophile Sulfolobus acidocaldarius: purification, characterization and partial sequence. Arch Biochem Biophys 1993; 302: 391–397.
- 32 Vonrhein C,Bonisch H,Schafer G,Schulz GE. The structure of a trimeric archaeal adenylate kinase. J Mol Biol 1998; 282: 167–179.
- 33 Chan C-H,Liang H-K,Nsiao N-W,Ko M-T,Lyu P-C,Hwang J-K. Relationship between local structural entropy and protein thermostability. Proteins 2004; 57: 684–691.
- 34 Violot S,Aghajari N,Czjzek M,Feller G,Sonan GK,Gouet P,Gerday C,Haser R,Receveur-Brechot V. Structure of a full length psychrophilic cellulase from Pseudoalteromonas haloplanktis revealed by X-ray diffraction and small angle X-ray scattering. J Mol Biol 2005; 348: 1211–1224.
- 35
Davlieva M,Shamoo Y.
Crystal structure and biochemical characterization of the adenylate kinase originated from the psychrophilic organism Marinibacillus marinus.
Acta Crystallogr F
2009;
65:
751–756.
10.1107/S1744309109024348 Google Scholar
- 36 Thompson JD,Higgins DG,Gilbson TJ. CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22: 4673–4680.
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