Consistent mutational paths predict eukaryotic thermostability

BMC Evolutionary Biology

Volumn 13, Issue 1, 2013, Pages

  Van Noort, Vera ^a   Bradatsch, Bettina ^b   Arumugam, Manimozhiyan ^a   Amlacher, Stefan ^b   Bange, Gert ^b,e   Creevey, Chris ^c   Falk, Sebastian ^b   Mende, Daniel R ^a   Sinning, Irmgard ^b   Hurt, Ed ^b   Bork, Peer ^a,d  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c GRANGE RESEARCH CENTRE   (Ireland)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^e PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Comparative genomics; Eukaryotes; Fungi; Protein engineering; Thermophily

Indexed keywords

ADAPTATION; AMINO ACID; BIOTECHNOLOGY; COMPARATIVE STUDY; EUKARYOTE; FUNGUS; MOLECULAR ANALYSIS; MUTATION; PHYLOGENETICS; PROKARYOTE; PROTEIN; PROTEOMICS; THERMOPHILIC BACTERIUM; THERMOREGULATION;

ARCHAEA; BACTERIA (MICROORGANISMS); CHAETOMIUM; CHAETOMIUM THERMOPHILUM; CORYNASCUS HETEROTHALLICUS; EUKARYOTA; FUNGI; PROKARYOTA; SORDARIOMYCETES; THIELAVIA TERRESTRIS;

PROTEOME;

ADAPTATION; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CLASSIFICATION; EVOLUTION; FUNGAL GENOME; GENETICS; HEAT; MOLECULAR GENETICS; MUTATION; PHYLOGENY; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; SORDARIALES;

ADAPTATION, BIOLOGICAL; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BIOLOGICAL EVOLUTION; GENOME, FUNGAL; HOT TEMPERATURE; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEOME; SORDARIALES;

MLCS; MLOWN;

EID: 84872110106     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-13-7     Document Type: Article

References (51)

1. Structure of the 30S ribosomal subunit. Wimberly BT, Brodersen DE, Clemons WM Jr, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V, Nature 2000 407 6802 327 339 10.1038/35030006 11014182
2. Genomic and proteomic adaptations to growth at high temperature. Hickey DA, Singer GA, Genome Biol 2004 5 10 117 10.1186/gb-2004-5-10-117 15461805 (Pubitemid 39485397)
3. Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Amlacher S, Sarges P, Flemming D, van Noort V, Kunze R, Devos DP, Arumugam M, Bork P, Hurt E, Cell 2011 146 2 277 289 10.1016/j.cell.2011.06.039 21784248
4. Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris. Berka RM, Grigoriev IV, Otillar R, Salamov A, Grimwood J, Reid I, Ishmael N, John T, Darmond C, Moisan MC, Henrissat B, Coutinho PM, Lombard V, Natvig DO, Lindquist E, Schmutz J, Lucas S, Harris P, Powlowski J, Bellemare A, Taylor D, Butler G, de Vries RP, Allijn IE, van den Brink J, Ushinsky S, Storms R, Powell AJ, Paulsen IT, Elbourne LD, Baker SE, Magnuson J, Laboissiere S, Clutterbuck AJ, Martinez D, Wogulis M, de Leon AL, Rey MW, Tsang A, Nat Biotechnol 2011 29 10 922 927 10.1038/nbt.1976 21964414
5. Thermophilic fungi in an aridland ecosystem. Powell AJ, Parchert KJ, Bustamante JM, Ricken B, Hutchinson MI, Natvig DO, Mycologia 2012 104 4 813 825 10.3852/11-298 22505432
6. The fungi of wheat straw compost: I. Ecological studies. Chang Y, Hudson HJ, Trans Br Mycol Soc 1967 50 4 649 666 10.1016/S0007-1536(67)80097-4
7. The biology of composting: A review. de Bertoldi M, Vallini G, Pera A, Waste Manag Res 1983 1 2 157 176 10.1016/0734-242X(83)90055-1 (Pubitemid 14067436)
8. Thermophilic fungi in a municipal waste compost system. Kane BE, Mullins JT, Mycologia 1973 65 5 1087 1100 10.2307/3758290 4585097
9. Microbiological aspects of wood chip storage in tropical environments. Greaves H, Aust J Biol Sci 1975 28 3 323 330 810126
10. Isolation of thermophilic fungi from self-heated, industrial wood chip piles. Tansey M, Mycologia 1971 63 3 537 547 10.2307/3757550
11. Ultrastructural alterations produced by sertaconazole on several opportunistic pathogenic fungi. Figueras MJ, Cano JF, Guarro J, J Med Vet Mycol 1995 33 6 395 401 10.1080/02681219580000761 8683408 (Pubitemid 26093957)
12. The genome sequence of the filamentous fungus Neurospora crassa. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Schulte U, Kothe GO, Jedd G, Mewes W, Staben C, Marcotte E, Greenberg D, Roy A, Foley K, Naylor J, Stange-Thomann N, Barrett R, Gnerre S, Kamal M, Kamvysselis M, Mauceli E, Bielke C, Rudd S, Frishman D, Krystofova S, Rasmussen C, Metzenberg RL, Perkins DD, Kroken S, Cogoni C, Macino G, Catcheside D, Li W, Pratt RJ, Osmani SA, DeSouza CP, Glass L, Orbach MJ, Berglund JA, Voelker R, Yarden O, Plamann M, Seiler S, Dunlap J, Radford A, Aramayo R, Natvig DO, Alex LA, Mannhaupt G, Ebbole DJ, Freitag M, Paulsen I, Sachs MS, Lander ES, Nusbaum C, Birren B, Nature 2003 422 6934 859 868 10.1038/nature01554 12712197 (Pubitemid 36520034)
13. Structure of two fungal beta-1,4-galactanases: searching for the basis for temperature and pH optimum. Le Nours J, Ryttersgaard C, Lo Leggio L, Ostergaard PR, Borchert TV, Christensen LL, Larsen S, Protein Sci 2003 12 6 1195 1204 10.1110/ps.0300103 12761390 (Pubitemid 36597506)
14. Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. Harris PV, Welner D, McFarland KC, Re E, Navarro Poulsen JC, Brown K, Salbo R, Ding H, Vlasenko E, Merino S, Xu F, Cherry J, Larsen S, Lo Leggio L, Biochemistry 2010 49 15 3305 3316 10.1021/bi100009p 20230050
15. Three-dimensional structures of thermophilic beta-1,4-xylanases from Chaetomium thermophilum and Nonomuraea flexuosa. Comparison of twelve xylanases in relation to their thermal stability. Hakulinen N, Turunen O, Janis J, Leisola M, Rouvinen J, Eur J Biochem 2003 270 7 1399 1412 10.1046/j.1432-1033.2003. 03496.x 12653995 (Pubitemid 36459578)
16. Structural insights into tail-anchored protein binding and membrane insertion by Get3. Bozkurt G, Stjepanovic G, Vilardi F, Amlacher S, Wild K, Bange G, Favaloro V, Rippe K, Hurt E, Dobberstein B, Sinning I, Proc Natl Acad Sci USA 2009 106 50 21131 21136 10.1073/pnas.0910223106 19948960
17. The structure of Get4 reveals an alpha-solenoid fold adapted for multiple interactions in tail-anchored protein biogenesis. Bozkurt G, Wild K, Amlacher S, Hurt E, Dobberstein B, Sinning I, FEBS Lett 2010 584 8 1509 1514 10.1016/j.febslet.2010.02.070 20206626
18. Optimized expression of a thermostable xylanase 11 a gene from Chaetomium thermophilum NIBGE 1 in Escherichia coli. Ghaffar A, Khan SA, Mukhtar Z, Latif F, Rajoka MI, Protein Pept Lett 2009 16 4 356 362 10.2174/092986609787848126 19356131
19. Production in trichoderma reesei of three xylanases from Chaetomium thermophilum: a recombinant thermoxylanase for biobleaching of kraft pulp. Mantyla A, Paloheimo M, Hakola S, Lindberg E, Leskinen S, Kallio J, Vehmaanpera J, Lantto R, Suominen P, Appl Microbiol Biotechnol 2007 76 2 377 386 10.1007/s00253-007-1020-y 17549471 (Pubitemid 47101684)
20. Purification and characterization of a thermostable MnSOD from the thermophilic fungus Chaetomium thermophilum. Guo FX, Shi-Jin E, Liu SA, Chen J, Li DC, Mycologia 2008 100 3 375 380 10.3852/06-111R 18751544
21. Toward automatic reconstruction of a highly resolved tree of life. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P, Science 2006 311 5765 1283 1287 10.1126/science.1123061 16513982 (Pubitemid 43334717)
22. eggNOG v2.0: extending the evolutionary genealogy of genes with enhanced non-supervised orthologous groups, species and functional annotations. Muller J, Szklarczyk D, Julien P, Letunic I, Roth A, Kuhn M, Powell S, von Mering C, Doerks T, Jensen LJ, Bork P, Nucleic Acids Res 2010 38 Database issue 190 195 19900971
23. Localization and light-dependent phosphorylation of white collar 1 and 2, the two central components of blue light signaling in Neurospora crassa. Schwerdtfeger C, Linden H, Eur J Biochem 2000 267 2 414 422 10.1046/j.1432-1327. 2000.01016.x 10632711 (Pubitemid 30072901)
24. Circadian clock locus frequency: protein encoded by a single open reading frame defines period length and temperature compensation. Aronson BD, Johnson KA, Dunlap JC, Proc Natl Acad Sci USA 1994 91 16 7683 7687 10.1073/pnas.91.16. 7683 8052643 (Pubitemid 24238249)
25. Microbial ultraviolet sunscreens. Gao Q, Garcia-Pichel F, Nat Rev Microbiol 2011 9 11 791 802 10.1038/nrmicro2649 21963801
26. Protein and DNA sequence determinants of thermophilic adaptation. Zeldovich KB, Berezovsky IN, Shakhnovich EI, PLoS Comput Biol 2007 3 1 5 10.1371/journal.pcbi.0030005 17222055 (Pubitemid 46168819)
27. The pressure dependence of hydrophobic interactions is consistent with the observed pressure denaturation of proteins. Hummer G, Garde S, Garcia AE, Paulaitis ME, Pratt LR, Proc Natl Acad Sci USA 1998 95 4 1552 1555 10.1073/pnas.95.4.1552 9465053 (Pubitemid 28103430)
28. The Humicola grisea Cel12A enzyme structure at 1.2 A resolution and the impact of its free cysteine residues on thermal stability. Sandgren M, Gualfetti PJ, Paech C, Paech S, Shaw A, Gross LS, Saldajeno M, Berglund GI, Jones TA, Mitchinson C, Protein Sci 2003 12 12 2782 2793 10.1110/ps.03220403 14627738 (Pubitemid 37445102)
29. Large differences in the helix propensities of alanine and glycine. Chakrabartty A, Schellman JA, Baldwin RL, Nature 1991 351 6327 586 588 10.1038/351586a0 2046766 (Pubitemid 21896647)
30. Temperature adaptation at homologous sites in proteins from nine thermophile-mesophile species pairs. McDonald JH, Genome Biol Evol 2010 2 267 276 10.1093/gbe/evq017 20624731
31. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Matthews BW, Nicholson H, Becktel WJ, Proc Natl Acad Sci USA 1987 84 19 6663 6667 10.1073/pnas.84.19.6663 3477797
32. Effect of proline substitutions on stability and kinetic properties of a cold adapted subtilase. Arnorsdottir J, Sigtryggsdottir AR, Thorbjarnardottir SH, Kristjansson MM, J Biochem 2009 145 3 325 329 10.1093/jb/mvn168 19074503
33. Stabilization of Bacillus stearothermophilus neutral protease by introduction of prolines. Hardy F, Vriend G, Veltman OR, van der Vinne B, Venema G, Eijsink VG, FEBS Lett 1993 317 1-2 89 92 8428638 (Pubitemid 23043945)
34. Stabilization of proteins by guanidination. Cupo P, El-Deiry W, Whitney PL, Awad WM Jr, J Biol Chem 1980 255 22 10828 10833 6253487
35. Identification of thermophilic species by the amino acid compositions deduced from their genomes. Kreil DP, Ouzounis CA, Nucleic Acids Res 2001 29 7 1608 1615 10.1093/nar/29.7.1608 11266564 (Pubitemid 32288510)
36. Internal correspondence analysis of codon and amino-acid usage in thermophilic bacteria. Lobry JR, Chessel D, J Appl Genet 2003 44 2 235 261 12817570 (Pubitemid 37123440)
37. 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. Nissan TA, Bassler J, Petfalski E, Tollervey D, Hurt E, EMBO J 2002 21 20 5539 5547 10.1093/emboj/cdf547 12374754 (Pubitemid 35231033)
38. Multiple sequence alignment using ClustalW and ClustalX. Thompson JD, Gibson TJ, Higgins DG, Curr Protoc Bioinformatics 2002 2.3.1 2.3.22
39. Structure and function of the methionine aminopeptidases. Lowther WT, Matthews BW, Biochim Biophys Acta 2000 1477 1-2 157 167 10708856 (Pubitemid 30119899)
40. The crystal structure of Ebp1 reveals a methionine aminopeptidase fold as binding platform for multiple interactions. Kowalinski E, Bange G, Bradatsch B, Hurt E, Wild K, Sinning I, FEBS Lett 2007 581 23 4450 4454 10.1016/j.febslet. 2007.08.024 17765895 (Pubitemid 47368204)
41. Directed evolution and structural prediction of cellobiohydrolase II from the thermophilic fungus Chaetomium thermophilum. Wang XJ, Peng YJ, Zhang LQ, Li AN, Li DC, Appl Microbiol Biotechnol 2012 95 6 1469 1478 10.1007/s00253-011- 3799-9 22215071
42. Basic local alignment search tool. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, J Mol Biol 1990 215 3 403 410 2231712
43. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Edgar RC, Nucleic Acids Res 2004 32 5 1792 1797 10.1093/nar/gkh340 15034147 (Pubitemid 38832724)
44. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Castresana J, Mol Biol Evol 2000 17 4 540 552 10.1093/oxfordjournals.molbev.a026334 10742046 (Pubitemid 30210700)
45. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Stamatakis A, Bioinformatics 2006 22 21 2688 2690 10.1093/bioinformatics/btl446 16928733 (Pubitemid 44642609)
46. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Letunic I, Bork P, Bioinformatics 2007 23 1 127 128 10.1093/bioinformatics/btl529 17050570 (Pubitemid 46017867)
47. Phylip-phylogeny inference package (version 3.2). Felsenstein J, Cladistics 1989 5 164 166
48. THE CCP4 SUITE-PROGRAMS FOR PROTEIN CRYSTALLOGRAPHY. Bailey S, ACTA CRYSTALLOGRAPHICA SECTION D-BIOLOGICAL CRYSTALLOGRAPHY 1994 50 5 760 763 10.1107/S0907444994003112 (Pubitemid 2143461)
49. Pushing the boundaries of molecular replacement with maximum likelihood. Read RJ, Acta Crystallogr D Biol Crystallogr 2001 57 1373 1382 10.1107/S0907444901012471 11567148 (Pubitemid 36117185)
50. Coot: model-building tools for molecular graphics. Emsley P, Cowtan K, Acta Crystallogr D Biol Crystallogr 2004 60 Pt 12 Pt 1 2126 2132 15572765 (Pubitemid 41742764)
51. Refinement of macromolecular structures by the maximum-likelihood method. Murshudov GN, Vagin AA, Dodson EJ, Acta Crystallogr D Biol Crystallogr 1997 53 240 255 10.1107/S0907444996012255 15299926 (Pubitemid 27235885)