Abstract
The protein derived from the Methanocaldococcus jannaschii MJ0458 gene is annotated as a δ-1-pyrroline 5-carboxylate synthetase and is predicted to be related to aspartokinase and uridylate kinase. Analysis of the predicted protein sequence indicated that it is a unique kinase with few similarities to either uridylate or adenylate kinase. Here, we report that the MJ0458 gene product is a second type of archaeal adenylate kinase, AdkB. This enzyme is different from the established archaeal-specific adenylate kinase in both sequence and predicted tertiary structure.
This is a preview of subscription content, log in via an institution to check access.
References
Cheek S, Zhang H, Grishin NV (2002) Sequence and structure classification of kinases. J Mol Biol 320:855–881
Cheek S, Ginalski K, Zhang H, Grishin NV (2005) A comprehensive update of the sequence and structure classification of kinases. BMC Struct Biol 5:6
Chistoserdova L, Vorholt JA, Thauer RK, Lidstrom ME (1998) C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic archaea. Science 281:99–102
Counago R, Wilson CJ, Pena MI, Wittung-Stafshede P, Shamoo Y (2008) An adaptive mutation in adenylate kinase that increases organismal fitness is linked to stability-activity trade-offs. Protein Eng Des Sel 21:19–27. doi:10.1093/protein/gzm072
Criswell AR, Bae E, Stec B, Konisky J, Phillips GN Jr (2003) Structures of thermophilic and mesophilic adenylate kinases from the genus Methanococcus. J Mol Biol 330:1087–1099. doi:S0022283603006557
Davlieva M, Shamoo Y (2009) Structure and biochemical characterization of an adenylate kinase originating from the psychrophilic organism Marinibacillus marinus. Acta Crystallogr Sect F Struct Biol Cryst Commun 65:751–756. doi:10.1107/S1744309109024348
Davlieva M, Shamoo Y (2010) Crystal structure of a trimeric archaeal adenylate kinase from the mesophile Methanococcus maripaludis with an unusually broad functional range and thermal stability. Proteins 78:357–364. doi:10.1002/prot.22549
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Ferber DM, Haney PJ, Berk H, Lynn D, Konisky J (1997) The adenylate kinase genes of M. voltae, M. thermolithotrophicus, M. jannaschii, and M. igneus define a new family of adenylate kinases. Gene 185:239–244. doi:S0378-1119(96)00651-8
Giometti CS et al (2002) Global analysis of a “simple” proteome: Methanococcus jannaschii. J Chromatogr B Analyt Technol Biomed Life Sci 782:227–243. doi:S1570023202005688
Gorris LG, Voet AC, van der Drift C (1991) Structural characteristics of methanogenic cofactors in the non-methanogenic archaebacterium Archaeoglobus fulgidus. Biofactors 3:29–35
Graupner M, White RH (2001) Methanococcus jannaschii generates l-proline by cyclization of l-ornithine. J Bacteriol 183:5203–5205
Grochowski LL, White RH (2010) Biosynthesis of the methanogenic coenzymes. In: Begley T (ed) Comprehensive natural products chemistry II. Elsevier, Amsterdam, pp 711–748
Grochowski LL, Xu H, White RH (2006) Methanocaldococcus jannaschii uses a modified mevalonate pathway for biosynthesis of isopentenyl diphosphate. J Bacteriol 188:3192–3198. doi:10.1128/JB.188.9.3192-3198.2006
Howell DM, Graupner M, Xu H, White RH (2000) Identification of enzymes homologous to isocitrate dehydrogenase that are involved in coenzyme B and leucine biosynthesis in methanoarchaea. J Bacteriol 182:5013–5016
Jensen KS, Johansson E, Jensen KF (2007) Structural and enzymatic investigation of the Sulfolobus solfataricus uridylate kinase shows competitive UTP inhibition and the lack of GTP stimulation. Biochemistry 46:2745–2757. doi:10.1021/bi0618159
Kath T, Schafer G (1995) A secY homologous gene in the crenarchaeon Sulfolobus acidocaldarius. Biochim Biophys Acta 1264:155–158
Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306. doi:10.1093/bib/bbn017
Lacher K, Schafer G (1993) Archaebacterial adenylate kinase from the thermoacidophile Sulfolobus acidocaldarius: purification, characterization, and partial sequence. Arch Biochem Biophys 302:391–397. doi:10.1006/abbi.1993.1229
Lee MJ, Chien-Liang L, Tsai JY, Sue WT, Hsia WS, Huang H (2010) Identification and biochemical characterization of a unique Mn2+-dependent UMP kinase from Helicobacter pylori. Arch Microbiol 192:739–746. doi:10.1007/s00203-010-0600-x
Lobley A, Sadowski MI, Jones DT (2009) pGenTHREADER and pDomTHREADER: new methods for improved protein fold recognition and superfamily discrimination. Bioinformatics 25:1761–1767. doi:10.1093/bioinformatics/btp302
Marco-Marin C, Escamilla-Honrubia JM, Rubio V (2005a) First-time crystallization and preliminary X-ray crystallographic analysis of a bacterial-archaeal type UMP kinase, a key enzyme in microbial pyrimidine biosynthesis. Biochim Biophys Acta 1747:271–275. doi:10.1016/j.bbapap.2004.11.010
Marco-Marin C, Gil-Ortiz F, Rubio V (2005b) The crystal structure of Pyrococcus furiosus UMP kinase provides insight into catalysis and regulation in microbial pyrimidine nucleotide biosynthesis. J Mol Biol 352:438–454. doi:10.1016/j.jmb.2005.07.045
Mashhadi Z, Xu H, Grochowski LL, White RH (2010) Archaeal RibL: a new FAD synthetase that is air sensitive. Biochemistry 49:8748–8755. doi:10.1021/bi100817q
Meier C et al (2008) The crystal structure of UMP kinase from Bacillus anthracis (BA1797) reveals an allosteric nucleotide-binding site. J Mol Biol 381:1098–1105. doi:10.1016/j.jmb.2008.06.078
Rusnak P, Haney P, Konisky J (1995) The adenylate kinases from a mesophilic and three thermophilic methanogenic members of the Archaea. J Bacteriol 177:2977–2981
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Scheer M et al (2011) BRENDA, the enzyme information system in 2011. Nucleic Acids Res 39:D670–D676. doi:10.1093/nar/gkq1089
Sheng XR, Li X, Pan XM (1999) An iso-random Bi Bi mechanism for adenylate kinase. J Biol Chem 274:22238–22242
Traut TW (1994) The functions and consensus motifs of nine types of peptide segments that form different types of nucleotide-binding sites. Eur J Biochem 222:9–19
White RH (1993) Structures of the modified folates in the thermophilic archaebacteria Pyrococcus furiosus. Biochemistry 32:745–753
White RH (2006) The difficult road from sequence to function. J Bacteriol 188:3431–3432. doi:10.1128/JB.188.10.3431-3432.2006
Xia Q, Wang T, Hendrickson EL, Lie TJ, Hackett M, Leigh JA (2009) Quantitative proteomics of nutrient limitation in the hydrogenotrophic methanogen Methanococcus maripaludis. BMC Microbiol 9:149. doi:10.1186/1471-2180-9-149
Zhu W, Reich CI, Olsen GJ, Giometti CS, Yates JR 3rd (2004) Shotgun proteomics of Methanococcus jannaschii and insights into methanogenesis. J Proteome Res 3:538–548
Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166
Note added in proof
We have recently identified the enzyme catalyzing the formation of dihydro-6-hydroxymethylpterin-PP and AMP from ATP and dihydro-6-hydroxymethylpterin that is involved in the biosynthesis of methanopterin. We propose that AdkB is involved in converting the AMP product of this reaction to ATP.
Acknowledgments
This research was supported by the U.S. National Science Foundation Grant MCB 0722787 to R.H.W. We thank Walter Niehaus for assistance with editing this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Harald Huber.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Grochowski, L.L., Censky, K., Xu, H. et al. A new class of adenylate kinase in methanogens is related to uridylate kinase. Arch Microbiol 194, 141–145 (2012). https://doi.org/10.1007/s00203-011-0759-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-011-0759-9