A Tandem duplication of manganese superoxide dismutase in nosema bombycis and its evolutionary origins

Journal of Molecular Evolution

Volumn 71, Issue 5-6, 2010, Pages 401-414

  Xiang, Heng ^a   Pan, Guoqing ^a   Vossbrinck, Charles R ^c   Zhang, Ruizhi ^a   Xu, Jinshan ^b   Li, Tian ^a   Zhou, Zeyang ^a,b   Lu, Cheng ^a   Xiang, Zhonghuai ^a  

^a SOUTHWEST UNIVERSITY   (China)

^b CHONGQING NORMAL UNIVERSITY   (China)

^c Northeast Regional Center for Excellence in Vector Borne Diseases   (United States)

Author keywords

Gene duplication; Horizontal gene transfer; Manganese superoxide dismutase; Microsporidia; Structure; Subcellular localization

Indexed keywords

SUPEROXIDE DISMUTASE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CELL FRACTIONATION; CHEMICAL PHENOMENA; CHEMISTRY; CLUSTER ANALYSIS; ENZYMOLOGY; FUNGAL GENOME; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENETIC SELECTION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NOSEMA; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CLUSTER ANALYSIS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR SEQUENCE DATA; NOSEMA; PHYLOGENY; PROTEIN TRANSPORT; SELECTION, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SUBCELLULAR FRACTIONS; SUPEROXIDE DISMUTASE; TRANSCRIPTION, GENETIC;

ANIMALIA; ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; MICROSPORIDIA; NOSEMA; NOSEMA BOMBYCIS;

EID: 78649982617     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-010-9394-3     Document Type: Article

References (89)

1. F Abascal R Zardoya D Posada 2005 ProtTest: selection of best-fit models of protein evolution Bioinformatics 21 2104 2105 1:CAS:528:DC%2BD2MXjsl2ns7Y%3D 10.1093/bioinformatics/bti263 15647292 (Pubitemid 40668057)
2. RG Alscher N Erturk LS Heath 2002 Role of superoxide dismutases (SODs) in controlling oxidative stress in plants J Exp Bot 53 1331 1341 1:CAS:528:DC%2BD38XktFSlsL4%3D 10.1093/jexbot/53.372.1331 11997379
3. SF Altschul W Gish W Miller EW Myers DJ Lipman 1990 Basic local alignment search tool J Mol Biol 215 403 410 1:CAS:528:DyaK3MXitVGmsA%3D%3D 2231712
4. MP Babitha SG Bhat HS Prakash HS Shetty 2002 Differential induction of superoxide dismutase in downy mildew-resistant and -susceptible genotypes of pearl millet Plant Pathol 51 480 486 1:CAS:528:DC%2BD38Xnt1Wmsro%3D 10.1046/j.1365-3059.2002.00733.x (Pubitemid 34923154)
5. F Bagnoli M Capuana ML Raccfii 1998 Developmental changes of catalase and superoxide dismutase isoenzymes in zygotic and somatic embryos of horse chestnut J Plant Physiol 25 909 913 1:CAS:528:DyaK1MXht1emtrg%3D
6. F Bagnoli D Giannino S Caparrini A Camussi D Mariotti ML Racchi 2002 Molecular cloning, characterisation and expression of a manganese superoxide dismutase gene from peach (Prunus persica [L.] Batsch) Mol Genet Genomics 267 321 328 1:CAS:528:DC%2BD38XlvFSjsLg%3D 10.1007/s00438-002-0664-7 12073034 (Pubitemid 34587827)
7. D Barra ME Schinina F Bossa K Puget P Durosay A Guissani AM Michelson 1990 A tetrameric iron superoxide dismutase from the eucaryote Tetrahymena pyriformis J Biol Chem 265 17680 17687 1:CAS:528:DyaK3MXhsF2kt7k%3D 2170391
8. PA Belinky D Goldberg B Krinfeld M Burger N Rothschild U Cogan CG Dosoretz 2002 Manganese-containing superoxide dismutase from the white-rot fungus Phanerochaete chrysosporium: its function, expression and gene structure Enzyme Microb Tech 31 754 764 1:CAS:528:DC%2BD38Xns1aks7c%3D 10.1016/S0141-0229(02)00180-1 (Pubitemid 35279814)
9. LM Blackman HJ Mitchell AR Hardham 2005 Characterisation of manganese superoxide dismutase from Phytophthora nicotianae Mycol Res 109 1171 1183 1:CAS:528:DC%2BD2MXhtVags7rM 10.1017/S0953756205003771 16279411 (Pubitemid 41411611)
10. CJ Bond J Huang R Hajduk KE Flick PJ Heath BL Stoddard 2000 Cloning, sequence and crystallographic structure of recombinant iron superoxide dismutase from Pseudomonas ovalis Acta Crystallogr 56 1359 1366 1:STN:280: DC%2BD3M7htlKnsg%3D%3D
11. D Bordo K Djinovic M Bolognesi 1994 Conserved patterns in the Cu, Zn superoxide dismutase family J Mol Biol 238 366 386 1:CAS:528:DyaK2cXkt12rtro%3D 10.1006/jmbi.1994.1298 8176730 (Pubitemid 24154718)
12. GE Borgstahl HE Parge MJ Hickey WF Beyer Jr RA Hallewell JA Tainer 1992 The structure of human mitochondrial manganese superoxide dismutase reveals a novel tetrameric interface of two 4-helix bundles Cell 71 107 118 1:CAS:528:DyaK38XmsVOksro%3D 10.1016/0092-8674(92)90270-M 1394426
13. GEO Borgstahl M Pokross R Chehab A Sekher EH Snell 2000 Cryo-trapping the six-coordinate, distorted-octahedral active site of manganese superoxide dismutase1 J Mol Biol 296 951 959 1:CAS:528:DC%2BD3cXht1Omsr4%3D 10.1006/jmbi.1999.3506 10686094
14. M Brouwer TH Brouwer W Grater JJ Enghild IB Thogersen 1997 The paradigm that all oxygen-respiring eukaryotes have cytosolic CuZn-superoxide dismutase and that Mn-superoxide dismutase is localized to the mitochondria does not apply to a large group of marine arthropods Biochemistry 36 13381 13388 1:CAS:528:DyaK2sXmsVegsro%3D 10.1021/bi971052c 9341231 (Pubitemid 27473387)
15. M Brouwer T Hoexum Brouwer W Grater N Brown-Peterson 2003 Replacement of a cytosolic copper/zinc superoxide dismutase by a novel cytosolic manganese superoxide dismutase in crustaceans that use copper (haemocyanin) for oxygen transport Biochem J 374 219 228 1:CAS:528:DC%2BD3sXmtF2gsrc%3D 10.1042/BJ20030272 12769817 (Pubitemid 37046946)
16. Canning EU (1993) Microsporidia. In: Kreier JP (ed) Parasitic protozoa. Academic Press, New York
17. MG Claros P Vincens 1996 Computational method to predict mitochondrially imported proteins and their targeting sequences Eur J Biochem 241 779 786 1:CAS:528:DyaK28XmvFCjurw%3D 10.1111/j.1432-1033.1996.00779.x 8944766
18. JM Comeron 1999 K-Estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals Bioinformatics 15 763 764 1:CAS:528:DyaK1MXnt1Cks7g%3D 10.1093/bioinformatics/15.9.763 10498777 (Pubitemid 29484339)
19. JB Cooper K McIntyre MO Badasso SP Wood Y Zhang TR Garbe D Young 1995 X-ray structure analysis of the iron-dependent superoxide dismutase from Mycobacterium tuberculosis at 2.0 Angstroms resolution reveals novel dimer-dimer interactions J Mol Biol 246 531 544 1:CAS:528:DyaK2MXktF2rsb0%3D 10.1006/jmbi.1994.0105 7877174
20. AL Delcher KA Bratke EC Powers SL Salzberg 2007 Identifying bacterial genes and endosymbiont DNA with Glimmer Bioinformatics 23 673 679 1:CAS:528:DC%2BD2sXkt1GhtL8%3D 10.1093/bioinformatics/btm009 17237039 (Pubitemid 46554717)
21. I Desportes Y Le Charpentier A Galian F Bernard B Cochand-Priollet A Lavergne P Ravisse R Modigliani 1985 Occurrence of a new microsporidan: Enterocytozoon bieneusi n.g., n. sp., in the enterocytes of a human patient with AIDS J Protozool 32 250 254 1:STN:280:DyaL2M3jslWnug%3D%3D 4009510
22. B Diez C Schleissner MA Moreno M Rodriguez A Collados JL Barredo 1998 The manganese superoxide dismutase from the penicillin producer Penicillium chrysogenum Curr Genet 33 387 394 1:CAS:528:DyaK1cXjvF2qsro%3D 10.1007/s002940050351 9644201 (Pubitemid 28346998)
23. RC Edgar 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res 32 1792 1797 1:CAS:528:DC%2BD2cXisF2ks7w%3D 10.1093/nar/gkh340 15034147 (Pubitemid 38832724)
24. HA El-Taweel LA El-Zawawy DE Said GM Sharara 2007 Influence of the antioxidant drug (Antox) on experimental giardiasis and microsporidiosis J Egypt Soc Parasitol 37 189 204 17580577
25. O Emanuelsson H Nielsen S Brunak G von Heijne 2000 Predicting subcellular localization of proteins based on their N-terminal amino acid sequence J Mol Biol 300 1005 1016 1:CAS:528:DC%2BD3cXks1OntrY%3D 10.1006/jmbi.2000.3903 10891285
26. GC Fang RM Hanau LJ Vaillancourt 2002 The SOD2 gene, encoding a manganese-type superoxide dismutase, is up-regulated during conidiogenesis in the plant-pathogenic fungus Colletotrichum graminicola Fungal Genet Biol 36 155 165 1:CAS:528:DC%2BD38XkslKmu74%3D 10.1016/S1087-1845(02)00008-7 12081469 (Pubitemid 34757041)
27. NM Fast JS Law BA Williams PJ Keeling 2003 Bacterial catalase in the microsporidian Nosema locustae: implications for microsporidian metabolism and genome evolution Eukaryot Cell 2 1069 1075 1:CAS:528:DC%2BD3sXos1Gkurs%3D 10.1128/EC.2.5.1069-1075.2003 14555490 (Pubitemid 37298721)
28. J Felsenstein 1978 Cases in which parsimony or compatibility methods will be positively misleading Syst Biol 27 401 410
29. WM Fitch FJ Ayala 1994 The superoxide dismutase molecular clock revisited Proc Natl Acad Sci USA 91 6802 6807 1:CAS:528:DyaK2cXlvF2gtbY%3D 10.1073/pnas.91.15.6802 8041700 (Pubitemid 24226750)
30. S Fluckiger PRE Mittl L Scapozza H Fijten G Folkers MG Grutter K Blaser R Crameri 2002 Comparison of the crystal structures of the human manganese superoxide dismutase and the homologous Aspergillus fumigatus allergen at 2-A resolution J Immunol 168 1267 1272 1:CAS:528:DC%2BD38XpsFelsQ%3D%3D 11801664
31. E Frealle C Noel N Nolard F Symoens MS Felipe E Dei-Cas D Camus E Viscogliosi L Delhaes 2006 Manganese superoxide dismutase based phylogeny of pathogenic fungi Mol Phylogenet Evol 41 28 39 1:CAS:528:DC%2BD28XpsVWksLw%3D 10.1016/j.ympev.2006.05.001 16781873 (Pubitemid 44322052)
32. I Fridovich 1995 Superoxide radical and superoxide dismutases Annu Rev Biochem 64 97 112 1:CAS:528:DyaK2MXmsl2qsLs%3D 10.1146/annurev.bi.64.070195. 000525 7574505
33. C Gaboriaud V Bissery T Benchetrit JP Mornon 1987 Hydrophobic cluster analysis: an efficient new way to compare and analyse amino acid sequences FEBS Lett 224 149 155 1:CAS:528:DyaL1cXjsVCntg%3D%3D 10.1016/0014-5793(87)80439-8 3678489
34. A Germot H Philippe 1999 Critical analysis of eukaryotic phylogeny: a case study based on the HSP70 family J Eukaryot Microbiol 46 116 124 1:CAS:528:DyaK1MXjvFyhs7s%3D 10.1111/j.1550-7408.1999.tb04594.x 10361733
35. SS Giles I Batinic-Haberle JR Perfect GM Cox 2005 Cryptococcus neoformans mitochondrial superoxide dismutase: an essential link between antioxidant function and high-temperature growth Eukaryot Cell 4 46 54 1:CAS:528: DC%2BD2MXhtlOhsbk%3D 10.1128/EC.4.1.46-54.2005 15643059 (Pubitemid 40234421)
36. EE Gill NM Fast 2006 Assessing the microsporidia-fungi relationship: combined phylogenetic analysis of eight genes Gene 375 103 109 1:CAS:528:DC%2BD28Xlt12ru70%3D 10.1016/j.gene.2006.02.023 16626896 (Pubitemid 43817397)
37. S Guindon O Gascuel 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood Syst Biol 52 696 704 10.1080/10635150390235520 14530136 (Pubitemid 37365050)
38. HM Hassan 1989 Microbial superoxide dismutases Adv Genet 26 65 97 1:CAS:528:DyaK3cXhsFCjtL8%3D 10.1016/S0065-2660(08)60223-0 2554697
39. T Hunter WH Bannister GJ Hunter 1997 Cloning, expression, and characterization of two manganese superoxide dismutases from Caenorhabditis elegans J Biol Chem 272 28652 28659 1:CAS:528:DyaK2sXntlCqsb0%3D 10.1074/jbc.272.45.28652 9353332 (Pubitemid 27517820)
40. LD Hurst 2002 The Ka/Ks ratio: diagnosing the form of sequence evolution Trends Genet 18 486 487 10.1016/S0168-9525(02)02722-1 12175810
41. SM Jackson JB Cooper 1998 An analysis of structural similarity in the iron and manganese superoxide dismutases based on known structures and sequences Biometals 11 159 173 1:CAS:528:DyaK1cXit1WrtLg%3D 10.1023/A:1009238214394 9542069 (Pubitemid 28140337)
42. TY James F Kauff CL Schoch PB Matheny V Hofstetter CJ Cox G Celio C Gueidan E Fraker J Miadlikowska HT Lumbsch A Rauhut V Reeb AE Arnold A Amtoft JE Stajich K Hosaka GH Sung D Johnson B O'Rourke M Crockett M Binder JM Curtis JC Slot Z Wang AW Wilson A Schussler JE Longcore K O'Donnell S Mozley-Standridge D Porter PM Letcher MJ Powell JW Taylor MM White GW Griffith DR Davies RA Humber JB Morton J Sugiyama AY Rossman JD Rogers DH Pfister D Hewitt K Hansen S Hambleton RA Shoemaker J Kohlmeyer B Volkmann-Kohlmeyer RA Spotts M Serdani PW Crous KW Hughes K Matsuura E Langer G Langer WA Untereiner R Lucking B Budel DM Geiser A Aptroot P Diederich I Schmitt M Schultz R Yahr DS Hibbett F Lutzoni DJ McLaughlin JW Spatafora R Vilgalys 2006 Reconstructing the early evolution of fungi using a six-gene phylogeny Nature 443 818 822 1:CAS:528:DC%2BD28XhtVyktbjN 10.1038/nature05110 17051209 (Pubitemid 44622687)
43. MD Katinka S Duprat E Cornillot G Metenier F Thomarat G Prensier V Barbe E Peyretaillade P Brottier P Wincker F Delbac H El Alaoui P Peyret W Saurin M Gouy J Weissenbach CP Vivares 2001 Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi Nature 414 450 453 1:CAS:528:DC%2BD3MXovFamsbo%3D 10.1038/35106579 11719806 (Pubitemid 34173726)
44. PJ Keeling NM Fast JS Law BA Williams CH Slamovits 2005 Comparative genomics of microsporidia Folia Parasitol (Praha) 52 8 14
45. M Kimura 1980 A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences J Mol Evol 16 111 120 1:CAS:528:DyaL3MXmtFSktg%3D%3D 10.1007/BF01731581 7463489 (Pubitemid 11166431)
46. DJ Kliebenstein RA Monde RL Last 1998 Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization Plant Physiol 118 637 650 1:CAS:528:DyaK1cXmslyqtb0%3D 10.1104/pp.118.2.637 9765550
47. S Knapp S Kardinahl N Hellgren G Tibbelin G Sch fer R Ladenstein 1999 Refined crystal structure of a superoxide dismutase from the hyperthermophilic archaeon Sulfolobus acidocaldarius at 2.2 resolution. J Mol Biol 285 689 702 1:CAS:528:DyaK1MXnslSntw%3D%3D 10.1006/jmbi.1998.2344 9878438 (Pubitemid 29041801)
48. MS Lah MM Dixon KA Pattridge WC Stallings JA Fee ML Ludwig 1995 Structure-function in Escherichia coli iron superoxide dismutase: comparisons with the manganese enzyme from Thermus thermophilus Biochemistry 34 1646 1660 1:CAS:528:DyaK2MXjtlOgur8%3D 10.1021/bi00005a021 7849024
49. C Lamarre JD LeMay N Deslauriers Y Bourbonnais 2001 Candida albicans expresses an unusual cytoplasmic manganese-containing superoxide dismutase (SOD3 gene product) upon the entry and during the stationary phase J Biol Chem 276 43784 43791 1:CAS:528:DC%2BD3MXos12nt7o%3D 10.1074/jbc.M108095200 11562375
50. JH Lim YG Yu YS Han S Cho BY Ahn SH Kim Y Cho 1997 The crystal structure of an Fe-superoxide dismutase from the hyperthermophile Aquifex pyrophilus at 1.9 resolution: structural basis for thermostability1 J Mol Biol 270 259 274 1:CAS:528:DyaK2sXkvVWrsL8%3D 10.1006/jmbi.1997.1105 9236127 (Pubitemid 27296686)
51. M Lynch H Kuramitsu 2000 Expression and role of superoxide dismutases (SOD) in pathogenic bacteria Microbes Infect 2 1245 1255 1:CAS:528: DC%2BD3cXntlSgtLc%3D 10.1016/S1286-4579(00)01278-8 11008114
52. SL Marklund 1984 Extracellular superoxide dismutase and other superoxide dismutase isoenzymes in tissues from nine mammalian species Biochem J 222 649 655 1:CAS:528:DyaL2cXls1Oru7o%3D 6487268
53. ME Martin BR Byers MO Olson ML Salin JE Arceneaux C Tolbert 1986 A Streptococcus mutans superoxide dismutase that is active with either manganese or iron as a cofactor J Biol Chem 261 9361 9367 1:STN:280:DyaL283ltVyrtA%3D%3D 3722201
54. JM McCord I Fridovich 1969 Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) J Biol Chem 244 6049 6055 1:CAS:528:DyaE3cXmsVU%3D 5389100
55. K Nakai P Horton 1999 PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization Trends Biochem Sci 24 34 35 1:CAS:528:DyaK1MXks12qtLk%3D 10.1016/S0968-0004(98)01336-X 10087920 (Pubitemid 29074461)
56. Natvig DO, Sylvester K, Dvorachek WH, Baldwin JL (1996) Superoxide dismutases and catalases. In: Brambl R, Marzluf GA (eds) Biochemistry and molecular biology. Springer-Verlag, Berlin
57. Ohno S (1970) Evolution by gene duplication. Springer-Verlag, New York
58. JM Palma E Lopez-Huertas FJ Corpas LM Sandalio M Gomez LA del Rio 1998 Peroxisomal manganese superoxide dismutase: purification and properties of the isozyme from pea leaves Physiol Plant 104 720 726 1:CAS:528:DyaK1MXhtFOrsrk%3D 10.1034/j.1399-3054.1998.1040429.x (Pubitemid 29096695)
59. SM Pan JS Ye RS Hseu 1997 Purification and characterization of manganese superoxide dismutase from Ganoderma microsporum Biochem Mol Biol Int 42 1035 1043 1:CAS:528:DyaK2sXnt1antr8%3D 9285072
60. MW Parker CC Blake 1988 Iron- and manganese-containing superoxide dismutases can be distinguished by analysis of their primary structures FEBS Lett 229 377 382 1:CAS:528:DyaL1cXhs1Cjt74%3D 10.1016/0014-5793(88)81160-8 3345848 (Pubitemid 18070424)
61. MW Parker CC Blake D Barra F Bossa ME Schinina WH Bannister JV Bannister 1987 Structural identity between the iron- and manganese-containing superoxide dismutases Protein Eng 1 393 397 1:CAS:528:DyaL1cXptVyqsQ%3D%3D 10.1093/protein/1.5.393 3508288
62. G Regelsberger W Atzenhofer F Ruker GA Peschek C Jakopitsch M Paumann PG Furtmuller C Obinger 2002 Biochemical characterization of a membrane-bound manganese-containing superoxide dismutase from the cyanobacterium Anabaena PCC 7120 J Biol Chem 277 43615 43622 1:CAS:528:DC%2BD38XpsFClsrk%3D 10.1074/jbc.M207691200 12215453 (Pubitemid 36157776)
63. M Robinson-Rechavi D Huchon 2000 RRTree: relative-rate tests between groups of sequences on a phylogenetic tree Bioinformatics 16 296 1:CAS:528:DC%2BD3cXksFaisr4%3D 10.1093/bioinformatics/16.3.296 10869026
64. JG Scandalios 1993 Oxygen stress and superoxide dismutases Plant Physiol 101 7 12 1:CAS:528:DyaK3sXpvVSisQ%3D%3D 12231660
65. M Schmidt 1999 Manipulating the coordination mumber of the ferric iron within the cambialistic superoxide dismutase of Propionibacterium shermanii by changing the pH-value. A crystallographic analysis Eur J Biochem 262 117 127 1:CAS:528:DyaK1MXjsVyqtrc%3D 10.1046/j.1432-1327.1999.00359.x 10231372 (Pubitemid 29242617)
66. ME Siddall MF Whiting 1999 Long-branch abstractions Cladistics 15 9 24 10.1111/j.1096-0031.1999.tb00391.x
67. MW Smith RF Doolittle 1992 A comparison of evolutionary rates of the two major kinds of superoxide dismutase J Mol Evol 34 175 184 1:CAS:528: DyaK38Xhs1yru7g%3D 1556751
68. Snowden KF (2004) Zoonotic microsporidia from animals and arthropods with a discussion of human infections. In: Lindsay DS, Weiss LM (eds) World class parasites. Kluwer Academic Press, Boston
69. WC Stallings KA Pattridge RK Strong ML Ludwig 1984 Manganese and iron superoxide dismutases are structural homologs J Biol Chem 259 10695 10699 1:CAS:528:DyaL2cXls1Khtrc%3D 6381489
70. S Sugio BY Hiraoka F Yamakura 2003 Crystal structure of cambialistic superoxide dismutase from Porphyromonas gingivalis Eur J Biochem 267 3487 3495 10.1046/j.1432-1327.2000.01373.x
71. JA Tainer ED Getzoff KM Beem JS Richardson DC Richardson 1982 Determination and analysis of the 2 A-structure of copper, zinc superoxide dismutase J Mol Biol 160 181 217 1:CAS:528:DyaL38XlvFGisLk%3D 10.1016/0022-2836(82)90174-7 7175933 (Pubitemid 13239300)
72. M Takao A Yasui A Oikawa 1991 Unique characteristics of superoxide dismutase of a strictly anaerobic archaebacterium Methanobacterium thermoautotrophicum J Biol Chem 266 14151 14154 1:CAS:528:DyaK3MXlslOqs7Y%3D 1907270
73. F Thomarat CP Vivares M Gouy 2004 Phylogenetic analysis of the complete genome sequence of Encephalitozoon cuniculi supports the fungal origin of microsporidia and reveals a high frequency of fast-evolving genes J Mol Evol 59 780 791 1:CAS:528:DC%2BD2cXhtVKrurvJ 10.1007/s00239-004-2673-0 15599510 (Pubitemid 40100874)
74. A Tomitani AH Knoll CM Cavanaugh T Ohno 2006 The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives Proc Natl Acad Sci USA 103 5442 5447 1:CAS:528:DC%2BD28Xjslejsr8%3D 10.1073/pnas.0600999103 16569695
75. T Ursby BS Adinolfi S Al-Karadaghi E De Vendittis V Bocchini 1999 Iron superoxide dismutase from the archaeon Sulfolobus solfataricus: analysis of structure and thermostability J Mol Biol 286 189 205 1:CAS:528: DyaK1MXhtV2hu7s%3D 10.1006/jmbi.1998.2471 9931259 (Pubitemid 29078405)
76. W Van Camp D Inze M Van Montagu 1997 The regulation and function of tobacco superoxide dismutases Free Radic Biol Med 23 515 520 10.1016/S0891-5849(97)00112-3 9214590 (Pubitemid 27276791)
77. CR Vossbrinck CR Woese 1986 Eukaryotic ribosomes that lack a 5.8S RNA Nature 320 287 288 1:CAS:528:DyaL28XhsVCitLg%3D 10.1038/320287a0 3083262
78. CR Vossbrinck JV Maddox S Friedman BA Debrunner-Vossbrinck CR Woese 1987 Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes Nature 326 411 414 1:CAS:528:DyaL2sXktVWrsr4%3D 10.1038/326411a0 3550472 (Pubitemid 17053774)
79. UG Wagner KA Pattridge ML Ludwig WC Stallings MM Werber C Oefner F Frolow JL Sussman 1993 Comparison of the crystal structures of genetically engineered human manganese superoxide dismutase and manganese superoxide dismutase from Thermus thermophilus: differences in dimer-dimer interaction Protein Sci 2 814 825 1:CAS:528:DyaK3sXkvFSjt7Y%3D 10.1002/pro.5560020511 8495200
80. J Wang GKS Wong P Ni Y Han X Huang J Zhang C Ye Y Zhang J Hu K Zhang 2002 RePS: a sequence assembler that masks exact repeats identified from the shotgun data Genome Res 12 824 831 1:CAS:528:DC%2BD38XjvFSgtLc%3D 10.1101/gr.165102 11997349 (Pubitemid 34546470)
81. RA Weisiger I Fridovich 1973 Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization J Biol Chem 248 4793 4796 1:CAS:528:DyaE3sXks1ehtr0%3D 4578091
82. BA Williams RP Hirt JM Lucocq TM Embley 2002 A mitochondrial remnant in the microsporidian Trachipleistophora hominis Nature 418 865 869 1:CAS:528:DC%2BD38XmtlWlt7o%3D 10.1038/nature00949 12192407 (Pubitemid 34966303)
83. R Wintjens C Noel AC May D Gerbod F Dufernez M Capron E Viscogliosi M Rooman 2004 Specificity and phenetic relationships of iron- and manganese-containing superoxide dismutases on the basis of structure and sequence comparisons J Biol Chem 279 9248 9254 1:CAS:528:DC%2BD2cXhs1OmsL8%3D 10.1074/jbc.M312329200 14672935 (Pubitemid 38295988)
84. CR Woese O Kandler ML Wheelis 1990 Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya Proc Natl Acad Sci USA 87 4576 4579 1:STN:280:DyaK3c3otVCiug%3D%3D 10.1073/pnas.87.12.4576 2112744 (Pubitemid 20204145)
85. S Woodcock JP Mornon B Henrissat 1992 Detection of secondary structure elements in proteins by hydrophobic cluster analysis Protein Eng 5 629 635 1:CAS:528:DyaK3sXhvVyhsA%3D%3D 10.1093/protein/5.7.629 1480617
86. J Xu G Pan L Fang J Li X Tian T Li Z Zhou Z Xiang 2006 The varying microsporidian genome: existence of long-terminal repeat retrotransposon in domesticated silkworm parasite Nosema bombycis Int J Parasitol 36 1049 1056 1:CAS:528:DC%2BD28Xns12ltL4%3D 10.1016/j.ijpara.2006.04.010 16797019 (Pubitemid 44164330)
87. Z Yang 1997 PAML: a program package for phylogenetic analysis by maximum likelihood Comput Bioinformatics 13 555 556 1:CAS:528:DyaK2sXntlGnu7s%3D 10.1093/bioinformatics/13.5.555
88. O Zhaxybayeva JP Gogarten RL Charlebois WF Doolittle RT Papke 2006 Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events Genome Res 16 1099 1108 1:CAS:528:DC%2BD28XpsFelsrs%3D 10.1101/gr.5322306 16899658 (Pubitemid 44320397)
89. D Zhu JG Scandalios 1993 Maize mitochondrial manganese superoxide dismutases are encoded by a differentially expressed multigene family Proc Natl Acad Sci USA 90 9310 9314 1:CAS:528:DyaK2cXisVKjtw%3D%3D 10.1073/pnas.90.20.9310 8415698 (Pubitemid 23315773)