Evolutionary diversification and characterization of the eubacterial gene family encoding DXR type II, an alternative isoprenoid biosynthetic enzyme

BMC Evolutionary Biology

Volumn 13, Issue 1, 2013, Pages

  Carretero Paulet, Lorenzo ^a,b   Lipska, Agnieszka ^a   Pérez Gil, Jordi ^c   Sangari, Félix J ^d   Albert, Victor A ^a   Rodríguez Concepción, Manuel ^c  

^a Ciudad Politécnica de la Innovación   (Spain)

^b UNIVERSITY AT BUFFALO   (United States)

^c CSIC   (Spain)

^d UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

DXR II; Functional divergence; Gene loss; Horizontal gene transfer; Isoprenoid metabolism

Indexed keywords

ADAPTATION; AMINO ACID; ANTIMICROBIAL ACTIVITY; BACTERIUM; COMPARATIVE STUDY; DIVERGENCE; DRUG; GENE TRANSFER; ISOPRENOID; PATHOGENICITY; PHOSPHATE; PHYLOGENETICS; PROTEOMICS; TAXONOMY;

ALPHAPROTEOBACTERIA; ANIMALIA; BACTERIA (MICROORGANISMS); FIRMICUTES;

1-DEOXY-D-XYLULOSE 5-PHOSPHATE REDUCTOISOMERASE; ISOMERASE; MULTIENZYME COMPLEX; OXIDOREDUCTASE; TERPENE; 1 DEOXY D XYLULOSE 5 PHOSPHATE REDUCTOISOMERASE;

BACTERIA; CHEMISTRY; CLASSIFICATION; ENZYMOLOGY; EVOLUTION; GENETICS; HORIZONTAL GENE TRANSFER; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; 1-DEOXY-D-XYLULOSE 5-PHOSPHATE REDUCTOISOMERASE; ARTICLE; BACTERIUM;

ALDOSE-KETOSE ISOMERASES; BACTERIA; BIOLOGICAL EVOLUTION; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; MULTIENZYME COMPLEXES; OXIDOREDUCTASES; PHYLOGENY; TERPENES;

EID: 84883277128     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-13-180     Document Type: Article

References (70)

1. Secondary Metabolites. Croteau R, Kutchan TM, Lewis NG, Biochemistry & Molecular Biology of Plants, American Society of Plant Physiologists, Buchanan WG B, Jones R, 2000 1250 1318 24015374
2. Genes and enzymes involved in bacterial isoprenoid biosynthesis. Daum M, Herrmann S, Wilkinson B, Bechthold A, Curr Opin Chem Biol 2009 13 2 180 188 10.1016/j.cbpa.2009.02.029 19318289
3. Diversity of the biosynthesis of the isoprene units. Kuzuyama T, Seto H, Nat Prod Rep 2003 20 2 171 183 10.1039/b109860h 12735695
4. Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Rodríguez-Concepción M, Boronat A, Plant Physiol 2002 130 1079 1089 10.1104/pp.007138 12427975
5. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Lange BM, Rujan T, Martin W, Croteau R, Proc Natl Acad Sci U S A 2000 97 24 13172 13177 10.1073/pnas.240454797 11078528
6. The interplay between classical and alternative isoprenoid biosynthesis controls gammadelta T cell bioactivity of Listeria monocytogenes. Begley M, Gahan CG, Kollas AK, Hintz M, Hill C, Jomaa H, Eberl M, FEBS Lett 2004 561 1-3 99 104 15013758
7. Biochemical characterization of Bacillus subtilis type II isopentenyl diphosphate isomerase, and phylogenetic distribution of isoprenoid biosynthesis pathways. Laupitz R, Hecht S, Amslinger S, Zepeck F, Kaiser J, Richter G, Schramek N, Steinbacher S, Huber R, Arigoni D, et al. Eur J Biochem 2004 271 13 2658 2669 10.1111/j.1432-1033.2004.04194.x 15206931
8. The role of lateral gene transfer in the evolution of isoprenoid biosynthesis pathways. Boucher Y, Doolittle WF, Mol Microbiol 2000 37 703 716 10.1046/j.1365-2958.2000.02004.x 10972794
9. The plastidial MEP pathway: unified nomenclature and resources. Phillips MA, Leon P, Boronat A, Rodriguez-Concepcion M, Trends Plant Sci 2008 13 12 619 623 10.1016/j.tplants.2008.09.003 18948055
10. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Jomaa H, Wiesner J, Sanderbrand S, Altincicek B, Weidemeyer C, Hintz M, Turbachova I, Eberl M, Zeidler J, Lichtenthaler HK, et al. Science 1999 285 5433 1573 1576 10.1126/science.285.5433.1573 10477522
11. Two distinct pathways for essential metabolic precursors for isoprenoid biosynthesis. Kuzuyama T, Seto H, Proc Jpn Acad Ser B Phys Biol Sci 2012 88 3 41 52 10.2183/pjab.88.41 22450534
12. The 1-Deoxy-D-Xylulose-5-Phosphate pathway of Isoprenoid Biosynthesis in plants. Lichtenthaler HK, Annu Rev Plant Physiol Plant Mol Biol 1999 50 47 65 10.1146/annurev.arplant.50.1.47 15012203
13. Isoprenoid biosynthesis in prokaryotic organisms. Rodríguez- Concepción M, Boronat A, Isoprenoid Synthesis in Plants and Microorganisms New York: Springer, Bach TJ, Rohmer M, 2013 1 16
14. The MEP pathway: a new target for the development of herbicides, antibiotics and antimalarial drugs. Rodriguez-Concepcion M, Curr Pharm Des 2004 10 19 2391 2400 10.2174/1381612043384006 15279616
15. Isoprenoid biosynthetic pathways as anti-infective drug targets. Rohdich F, Bacher A, Eisenreich W, Biochem Soc Trans 2005 33 Pt 4 785 791 16042599
16. Biogenesis, molecular regulation and function of plant isoprenoids. Bouvier F, Rahier A, Camara B, Prog Lipid Res 2005 44 6 357 429 10.1016/j.plipres.2005.09.003 16289312
17. Metabolic plasticity for isoprenoid biosynthesis in bacteria. Perez-Gil J, Rodriguez-Concepcion M, Biochem J 2013 452 1 19 25 23614721
18. Bacterial origin for the isoprenoid biosynthesis enzyme HMG-CoA reductase of the archaeal orders thermoplasmatales and archaeoglobales. Boucher Y, Huber H, L'Haridon S, Stetter KO, Doolittle WF, Mol Biol Evol 2001 18 7 1378 1388 10.1093/oxfordjournals.molbev.a003922 11420376
19. Complex histories of genes encoding 3-hydroxy-3-methylglutaryl-CoenzymeA reductase. Gophna U, Thompson JR, Boucher Y, Doolittle WF, Mol Biol Evol 2006 23 1 168 178 16162862
20. An unusual isopentenyl diphosphate isomerase found in the mevalonate pathway gene cluster from Streptomyces sp. strain CL190. Kaneda K, Kuzuyama T, Takagi M, Hayakawa Y, Seto H, Proc Natl Acad Sci USA 2001 98 3 932 937 10.1073/pnas.98.3.932 11158573
21. Identification of an Archaeal type II isopentenyl diphosphate isomerase in methanothermobacter thermautotrophicus. Barkley SJ, Cornish RM, Poulter CD, J Bacteriol 2004 186 6 1811 1817 10.1128/JB.186.6.1811-1817.2004 14996812
22. Type II isopentenyl diphosphate isomerase from synechocystis sp. strain PCC 6803. Barkley SJ, Desai SB, Poulter CD, J Bacteriol 2004 186 23 8156 8158 10.1128/JB.186.23.8156-8158.2004 15547291
23. A new family of enzymes catalyzing the first committed step of the methylerythritol 4-phosphate (MEP) pathway for isoprenoid biosynthesis in bacteria. Sangari FJ, Perez-Gil J, Carretero-Paulet L, Garcia-Lobo JM, Rodriguez-Concepcion M, Proc Natl Acad Sci U S A 2010 107 32 14081 14086 10.1073/pnas.1001962107 20660776
24. Lateral gene transfer and the origins of prokaryotic groups. Boucher Y, Douady CJ, Papke RT, Walsh DA, Boudreau MER, Nesbø CL, Case RJ, Doolittle WF, Annu Rev Genet 2003 37 283 328 10.1146/annurev.genet.37.050503.084247 14616063
25. Choosing BLAST options for better detection of orthologs as reciprocal best hits. Moreno-Hagelsieb G, Latimer K, Bioinformatics 2008 24 3 319 324 10.1093/bioinformatics/btm585 18042555
26. Crystal structure of brucella abortus deoxyxylulose-5-phosphate reductoisomerase-like (DRL) enzyme involved in isoprenoid biosynthesis. Perez-Gil J, Calisto BM, Behrendt C, Kurz T, Fita I, Rodriguez-Concepcion M, J Biol Chem 2012 287 19 15803 15809 10.1074/jbc.M112.354811 22442144
27. Statistical methods for testing functional divergence after gene duplication. Gu X, Mol Biol Evol 1999 16 12 1664 1674 10.1093/oxfordjournals. molbev.a026080 10605109
28. A simple statistical method for estimating type-II (cluster-specific) functional divergence of protein sequences. Gu X, Mol Biol Evol 2006 23 10 1937 1945 10.1093/molbev/msl056 16864604
29. VMD: visual molecular dynamics. Humphrey W, Dalke A, Schulten K, J Mol Graph 1996 14 1 33 38 27-38 10.1016/0263-7855(96)00018-5 8744570
30. A robust species tree for the alphaproteobacteria. Williams KP, Sobral BW, Dickerman AW, J Bacteriol 2007 189 13 4578 4586 10.1128/JB.00269-07 17483224
31. Complete genome sequence of the metabolically versatile photosynthetic bacterium rhodopseudomonas palustris. Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S, Do L, Land ML, Pelletier DA, Beatty JT, Lang AS, et al. Nat Biotechnol 2004 22 1 55 61 10.1038/nbt923 14704707
32. Parallel evolution and horizontal gene transfer of the pst operon in firmicutes from oligotrophic environments. Moreno-Letelier A, Olmedo G, Eguiarte LE, Martinez-Castilla L, Souza V, Int J Evol Biol 2011 2011 781642 21461370
33. On the origin and evolution of biosynthetic pathways: integrating microarray data with structure and organization of the common pathway genes. Fondi M, Brilli M, Fani R, BMC bioinformatics 2007 8 Suppl 1 12 10.1186/1471-2105-8-S1-S12 18047711
34. Amelioration of bacterial genomes: rates of change and exchange. Lawrence JG, Ochman H, J Mol Evol 1997 44 4 383 397 10.1007/PL00006158 9089078
35. Molecular archaeology of the Escherichia coli genome. Lawrence JG, Ochman H, Proc Natl Acad Sci U S A 1998 95 16 9413 9417 10.1073/pnas.95.16.9413 9689094
36. Dinucleotide relative abundance extremes: a genomic signature. Karlin S, Burge C, Trends Genet 1995 11 7 283 290 10.1016/S0168-9525(00)89076-9 7482779
37. Detection of genes with atypical nucleotide sequence in microbial genomes. Hooper SD, Berg OG, J Mol Evol 2002 54 3 365 375 11847562
38. Coenzyme a biosynthesis: reconstruction of the pathway in archaea and an evolutionary scenario based on comparative genomics. Genschel U, Mol Biol Evol 2004 21 7 1242 1251 10.1093/molbev/msh119 15014152
39. Convergent evolution of enzyme active sites is not a rare phenomenon. Gherardini PF, Wass MN, Helmer-Citterich M, Sternberg MJ, J Mol Biol 2007 372 3 817 845 10.1016/j.jmb.2007.06.017 17681532
40. Xylanase II from an alkaliphilic thermophilic Bacillus with a distinctly different structure from other xylanases: evolutionary relationship to alkaliphilic xylanases. Kulkarni N, Lakshmikumaran M, Rao M, Biochem Biophys Res Commun 1999 263 3 640 645 10.1006/bbrc.1999.1420 10512731
41. alpha-ketoglutaric semialdehyde dehydrogenase isozymes involved in metabolic pathways of D-glucarate, D-galactarate, and hydroxy-L-proline. Molecular and metabolic convergent evolution. Watanabe S, Yamada M, Ohtsu I, Makino K, J Biol Chem 2007 282 9 6685 6695 17202142
42. Archean molecular fossils and the early rise of eukaryotes. Brocks JJ, Logan GA, Buick R, Summons RE, Science 1999 285 5430 1033 1036 10.1126/science.285.5430.1033 10446042
43. Studies on new phosphonic acid antibiotics. II. Taxonomic studies on producing organisms of the phosphonic acid and related compounds. Iguchi E, Okuhara M, Kohsaka M, Aoki H, Imanaka H, J Antibiot (Tokyo) 1980 33 1 19 23
44. Bartonellosis. Guptill L, Vet Microbiol 2010 140 3-4 347 359 20018462
45. Listeriosis: a resurgent foodborne infection. Allerberger F, Wagner M, Clin Microbiol Infect 2010 16 1 16 23 10.1111/j.1469-0691.2009.03109.x 20002687
46. Internal affairs: investigating the brucella intracellular lifestyle. von Bargen K, Gorvel JP, Salcedo SP, FEMS Microbiol Rev 2012 36 3 533 562 10.1111/j.1574-6976.2012.00334.x 22373010
47. Clostridia: sporeforming anaerobic bacilli. Wells CL, Wilkins TD, Medical Microbiology Galveston (TX), Baron S, 4 1996
48. Lateral gene transfer and the nature of bacterial innovation. Ochman H, Lawrence JG, Groisman EA, Nature 2000 405 6784 299 304 10.1038/35012500 10830951
49. The balance of driving forces during genome evolution in prokaryotes. Kunin V, Ouzounis CA, Genome Res 2003 13 7 1589 1594 10.1101/gr.1092603 12840037
50. Horizontal gene transfer: a critical view. Kurland CG, Canback B, Berg OG, Proc Natl Acad Sci U S A 2003 100 17 9658 9662 10.1073/pnas.1632870100 12902542
51. Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes. Mirkin BG, Fenner TI, Galperin MY, Koonin EV, BMC Evol Biol 2003 3 2 10.1186/1471-2148-3-2 12515582
52. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ, Nucleic Acids Res 1997 25 17 3389 3402 10.1093/nar/25.17.3389 9254694
53. 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
54. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O, Syst Biol 2010 59 3 307 321 10.1093/sysbio/syq010 20525638
55. An improved general amino acid replacement matrix. Le SQ, Gascuel O, Mol Biol Evol 2008 25 7 1307 1320 10.1093/molbev/msn067 18367465
56. ProtTest: selection of best-fit models of protein evolution. Abascal F, Zardoya R, Posada D, Bioinformatics 2005 21 9 2104 2105 10.1093/bioinformatics/ bti263 15647292
57. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Anisimova M, Gascuel O, Syst Biol 2006 55 4 539 552 10.1080/10635150600755453 16785212
58. MrBayes 3: Bayesian phylogenetic inference under mixed models. Ronquist F, Huelsenbeck JP, Bioinformatics 2003 19 12 1572 1574 10.1093/bioinformatics/ btg180 12912839
59. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Whelan S, Goldman N, Mol Biol Evol 2001 18 5 691 699 10.1093/oxfordjournals.molbev.a003851 11319253
60. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Tamura K, Dudley J, Nei M, Kumar S, Mol Biol Evol 2007 24 8 1596 1599 10.1093/molbev/msm092 17488738
61. DIVERGE: phylogeny-based analysis for functional-structural divergence of a protein family. Gu X, Vander Velden K, Bioinformatics 2002 18 3 500 501 10.1093/bioinformatics/18.3.500 11934757
62. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Goldman N, Yang Z, Mol Biol Evol 1994 11 5 725 736 7968486
63. The codon Adaptation Index-a measure of directional synonymous codon usage bias, and its potential applications. Sharp PM, Li WH, Nucleic Acids Res 1987 15 3 1281 1295 10.1093/nar/15.3.1281 3547335
64. An improved implementation of codon adaptation index. Xia X, Evol Bioinform Online 2007 3 53 58 19461982
65. DAMBE: software package for data analysis in molecular biology and evolution. Xia X, Xie Z, J Hered 2001 92 4 371 373 10.1093/jhered/92.4.371 11535656
66. Horizontal gene transfer in bacterial and archaeal complete genomes. Garcia-Vallve S, Romeu A, Palau J, Genome Res 2000 10 11 1719 1725 10.1101/gr.130000 11076857
67. Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes. Karlin S, Trends Microbiol 2001 9 7 335 343 10.1016/S0966-842X(01)02079-0 11435108
68. The proof and measurement of association between Two things. Spearman C, Am J Psychol 1904 15 1 72 101 10.2307/1412159
69. A new measure of rank correlation. Kendall MG, Biometrika 1938 30 1-2 81 93
70. Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Sharp PM, Tuohy TM, Mosurski KR, Nucleic Acids Res 1986 14 13 5125 5143 10.1093/nar/14.13.5125 3526280