Exploring the evolution of protein function in Archaea

BMC Evolutionary Biology

Igor N Berezovsky²  Alexander Goncearenco¹ 

[1] Department of Informatics, University of Bergen, N-5008, Bergen, Norway;Computational Biology Unit, Uni Research, University of Bergen, N-5008, Bergen, Norway

关键词: Functional domains/folds;    Elementary functional loops;    Archaea;    Evolution;    Protein function;   

Others  :  1141164
DOI  :  10.1186/1471-2148-12-75

 received in 2011-11-24, accepted in 2012-02-24,  发布年份 2012

【 摘 要 】

Background

Despite recent progress in studies of the evolution of protein function, the questions what were the first functional protein domains and what were their basic building blocks remain unresolved. Previously, we introduced the concept of elementary functional loops (EFLs), which are the functional units of enzymes that provide elementary reactions in biochemical transformations. They are presumably descendants of primordial catalytic peptides.

Results

We analyzed distant evolutionary connections between protein functions in Archaea based on the EFLs comprising them. We show examples of the involvement of EFLs in new functional domains, as well as reutilization of EFLs and functional domains in building multidomain structures and protein complexes.

Conclusions

Our analysis of the archaeal superkingdom yields the dominating mechanisms in different periods of protein evolution, which resulted in several levels of the organization of biochemical function. First, functional domains emerged as combinations of prebiotic peptides with the very basic functions, such as nucleotide/phosphate and metal cofactor binding. Second, domain recombination brought to the evolutionary scene the multidomain proteins and complexes. Later, reutilization and de novo design of functional domains and elementary functional loops complemented evolution of protein function.

【 授权许可】

   
2012 Goncearenco and Berezovsky; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Tokuriki N, Tawfik DS: Protein dynamism and evolvability. Science 2009, 324:203-207.
• [2]Romero PA, Arnold FH: Exploring protein fitness landscapes by directed evolution. Nat Rev Mol Cell Biol 2009, 10:866-876.
• [3]Glasner ME, Gerlt JA, Babbitt PC: Evolution of enzyme superfamilies. Curr Opin Chem Biol 2006, 10:492-497.
• [4]Koonin EV, Tatusov RL, Galperin MY: Beyond complete genomes: from sequence to structure and function. Curr Opin Struct Biol 1998, 8:355-363.
• [5]Koonin EV, Wolf YI, Karev GP: The structure of the protein universe and genome evolution. Nature 2002, 420:218-223.
• [6]Bershtein S, Tawfik DS: Advances in laboratory evolution of enzymes. Curr Opin Chem Biol 2008, 12:151-158.
• [7]Roodveldt C, Aharoni A, Tawfik DS: Directed evolution of proteins for heterologous expression and stability. Curr Opin Struct Biol 2005, 15:50-56.
• [8]Chothia C, Gough J, Vogel C, Teichmann SA: Evolution of the protein repertoire. Science 2003, 300:1701-1703.
• [9]Trifonov EN, Kirzhner A, Kirzhner VM, Berezovsky IN: Distinct stages of protein evolution as suggested by protein sequence analysis. J Mol Evol 2001, 53:394-401.
• [10]Goncearenco A, Berezovsky IN: Prototypes of elementary functional loops unravel evolutionary connections between protein functions. Bioinformatics 2010, 26:i497-i503.
• [11]Goncearenco A, Berezovsky IN: Computational reconstruction of primordial prototypes of elementary functional loops in modern proteins. Bioinformatics 2011, 27:2368-2375.
• [12]Lupas AN, Ponting CP, Russell RB: On the evolution of protein folds: are similar motifs in different protein folds the result of convergence, insertion, or relics of an ancient peptide world? J Struct Biol 2001, 134:191-203.
• [13]Berezovsky IN, Grosberg AY, Trifonov EN: Closed loops of nearly standard size: common basic element of protein structure. FEBS Lett 2000, 466:283-286.
• [14]Berezovsky IN, Trifonov EN: Van der Waals locks: loop-n-lock structure of globular proteins. J Mol Biol 2001, 307:1419-1426.
• [15]Yew BK, Chintapalli SV, Upton GGC, Reynolds CA: Conservation of closed loops. J Mol Graph Model 2007, 26:652-655.
• [16]Fernandez-Fuentes N, Dybas JM, Fiser A: Structural characteristics of novel protein folds. PLoS Comput Biol 2010, 6:e1000750.
• [17]Chintapalli SV, Yew BK, Illingworth CJR, Upton GJG, Reeves PJ, Parkes KEB, Snell CR, Reynolds CA: Closed loop folding units from structural alignments: experimental foldons revisited. J Comput Chem 2010, 31:2689-2701.
• [18]Alexander VE: Structural motifs are closed into cycles in proteins. Biochem Biophys Res Commun 2010, 399:412-415.
• [19]Berezovsky IN: Discrete structure of van der Waals domains in globular proteins. Protein Eng 2003, 16:161-167.
• [20]Berezovsky IN, Kirzhner VM, Kirzhner A, Trifonov EN: Protein folding: looping from hydrophobic nuclei. Proteins 2001, 45:346-350.
• [21]Trifonov EN, Berezovsky IN: Evolutionary aspects of protein structure and folding. Curr Opin Struct Biol 2003, 13:110-114.
• [22]Ittah V, Haas E: Nonlocal interactions stabilize long range loops in the initial folding intermediates of reduced bovine pancreatic trypsin inhibitor. Biochemistry 1995, 34:4493-4506.
• [23]Gutteridge A, Thornton JM: Understanding nature's catalytic toolkit. Trends Biochem Sci 2005, 30:622-629.
• [24]Holliday GL, Mitchell JBO, Thornton JM: Understanding the functional roles of amino acid residues in enzyme catalysis. J Mol Biol 2009, 390:560-577.
• [25]Makarova KS, Aravind L, Galperin MY, Grishin NV, Tatusov RL, Wolf YI, Koonin EV: Comparative genomics of the Archaea (Euryarchaeota): evolution of conserved protein families, the stable core, and the variable shell. Genome Res 1999, 9:608-628.
• [26]Makarova KS, Sorokin AV, Novichkov PS, Wolf YI, Koonin EV: Clusters of orthologous genes for 41 archaeal genomes and implications for evolutionary genomics of archaea. Biol Direct 2007, 2:33. BioMed Central Full Text
• [27]Thauer RK: Biochemistry of methanogenesis: a tribute to Marjory Stephenson. 1998 Marjory Stephenson Prize Lecture. Microbiology 1998, 144:2377-2406.
• [28]Shima S, Warkentin E, Thauer RK, Ermler U: Structure and function of enzymes involved in the methanogenic pathway utilizing carbon dioxide and molecular hydrogen. J Biosci Bioeng 2002, 93:519-530.
• [29]Ferry JG: Enzymology of one-carbon metabolism in methanogenic pathways. FEMS Microbiol Rev 1999, 23:13-38.
• [30]Kaster AK, Goenrich M, Seedorf H, Liesegang H, Wollherr A, Gottschalk G, Thauer RK: More than 200 genes required for methane formation from H and CO and energy conservation are present in Methanothermobacter marburgensis and Methanothermobacter thermautotrophicus. Archaea 2011, 2011:973848.
• [31]Reeve JN, Nolling J, Morgan RM, Smith DR: Methanogenesis: genes, genomes, and who's on first? J Bacteriol 1997, 179:5975-5986.
• [32]Murzin AG, Brenner SE, Hubbard T, Chothia C: SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 1995, 247:536-540.
• [33]Castillo RM, Mizuguchi K, Dhanaraj V, Albert A, Blundell TL, Murzin AG: A six-stranded double-psi beta barrel is shared by several protein superfamilies. Structure 1999, 7:227-236.
• [34]Boyington JC, Gladyshev VN, Khangulov SV, Stadtman TC, Sun PD: Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster. Science 1997, 275:1305-1308.
• [35]Ermler U, Grabarse W, Shima S, Goubeaud M, Thauer RK: Crystal structure of methyl-coenzyme M reductase: the key enzyme of biological methane formation. Science 1997, 278:1457-1462.
• [36]Thauer RK, Kaster AK, Goenrich M, Schick M, Hiromoto T, Shima S: Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage. Annu Rev Biochem 2010, 79:507-536.
• [37]Dym O, Eisenberg D: Sequence-structure analysis of FAD-containing proteins. Protein Sci 2001, 10:1712-1728.
• [38]Kobayashi T, Takimura T, Sekine R, Kelly VP, Kamata K, Sakamoto K, Nishimura S, Yokoyama S: Structural snapshots of the KMSKS loop rearrangement for amino acid activation by bacterial tyrosyl-tRNA synthetase. J Mol Biol 2005, 346:105-117.
• [39]Golovin A, Henrick K: MSDmotif: exploring protein sites and motifs. BMC Bioinformatics 2008, 9:312. BioMed Central Full Text
• [40]Andrade MA, Perez-Iratxeta C, Ponting CP: Protein repeats: structures, functions, and evolution. J Struct Biol 2001, 134:117-131.
• [41]Yadid I, Tawfik DS: Functional beta-propeller lectins by tandem duplications of repetitive units. Protein Eng Des Sel 2011, 24:185-195.
• [42]Yadid I, Tawfik DS: Reconstruction of functional beta-propeller lectins via homo-oligomeric assembly of shorter fragments. J Mol Biol 2007, 365:10-17.
• [43]Fairman-Williams ME, Guenther UP, Jankowsky E: SF1 and SF2 helicases: family matters. Curr Opin Struct Biol 2010, 20:313-324.
• [44]Singleton MR, Wigley DB: Modularity and specialization in superfamily 1 and 2 helicases. J Bacteriol 2002, 184:1819-1826.
• [45]Atta M, Mulliez E, Arragain S, Forouhar F, Hunt JF, Fontecave M: S-Adenosylmethionine-dependent radical-based modification of biological macromolecules. Curr Opin Struct Biol 2010, 20:684-692.
• [46]Beyer A: Sequence analysis of the AAA protein family. Protein Sci 1997, 6:2043-2058.
• [47]Chen M, Abele R, Tampe R: Functional non-equivalence of ATP-binding cassette signature motifs in the transporter associated with antigen processing (TAP). J Biol Chem 2004, 279:46073-46081.
• [48]Diederichs K, Diez J, Greller G, Muller C, Breed J, Schnell C, Vonrhein C, Boos W, Welte W: Crystal structure of MalK, the ATPase subunit of the trehalose/maltose ABC transporter of the archaeon Thermococcus litoralis. EMBO J 2000, 19:5951-5961.
• [49]Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM: Metal-MACiE: a database of metals involved in biological catalysis. Bioinformatics 2009, 25:2088-2089.
• [50]Gough J, Chothia C: SUPERFAMILY: HMMs representing all proteins of known structure. SCOP sequence searches, alignments and genome assignments. Nucleic Acids Res 2002, 30:268-272.
• [51]Brenner SE, Koehl P, Levitt M: The ASTRAL compendium for protein structure and sequence analysis. Nucleic Acids Res 2000, 28:254-256.
• [52]Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T: Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13:2498-2504.
• [53]Marchler-Bauer A, Anderson JB, Cherukuri PF, DeWeese-Scott C, Geer LY, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, et al.: CDD: a conserved domain database for protein classification. Nucleic Acids Res 2005, 33:D192-D196.
• [54]Shoemaker BA, Zhang D, Thangudu RR, Tyagi M, Fong JH, Marchler-Bauer A, Bryant SH, Madej T, Panchenko AR: Inferred biomolecular interaction server–a web server to analyze and predict protein interacting partners and binding sites. Nucleic Acids Res 2010, 38:D518-D524.
• [55]Holliday GL, Bartlett GJ, Almonacid DE, O'Boyle NM, Murray-Rust P, Thornton JM, Mitchell JB: MACiE: a database of enzyme reaction mechanisms. Bioinformatics 2005, 21:4315-4316.
• [56]Kanehisa M, Goto S: KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000, 28:27-30.
• [57]Schwede T, Kopp Jr, Guex N, Peitsch MC: SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 2003, 31:3381-3385.
• [58]Axelrod HL, Das D, Abdubek P, Astakhova T, Bakolitsa C, Carlton D, Chen C, Chiu HJ, Clayton T, Deller MC, et al.: Structures of three members of Pfam PF02663 (FmdE) implicated in microbial methanogenesis reveal a conserved alpha + beta core domain and an auxiliary C-terminal treble-clef zinc finger. Acta Crystallogr Sect F Struct Biol Cryst Commun 2010, 66:1335-1346.
• [59]Schindelin H, Kisker C, Hilton J, Rajagopalan KV, Rees DC: Crystal structure of DMSO reductase: redox-linked changes in molybdopterin coordination. Science 1996, 272:1615-1621.
• [60]Holliday GL, Thornton JM, Marquet A, Smith AG, Rebeille F, Mendel R, Schubert HL, Lawrence AD, Warren MJ: Evolution of enzymes and pathways for the biosynthesis of cofactors. Nat Prod Rep 2007, 24:972-987.
• [61]Scheller S, Goenrich M, Boecher R, Thauer RK, Jaun B: The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane. Nature 2010, 465:606-608.