Comprehensive phylogenetic analysis of evolutionarily conserved rRNA adenine dimethyltransferase suggests diverse bacterial contributions to the nucleus-encoded plastid proteome

Molecular Phylogenetics and Evolution

Volumn 50, Issue 2, 2009, Pages 282-289

  Park, Ae Kyung ^a   Kim, Ho ^a   Jin, Hyung Jong ^b  

^a Seoul National University   (South Korea)

^b Suwon University   (South Korea)

Author keywords

Dim1; Endosymbiosis; KsgA; Lateral gene transfer; Mitochondrial transcription factor B; Phylogenetic analysis; Plastid targeted proteins; rRNA adenine dimethyltransferase

Indexed keywords

METHYLTRANSFERASE; PROTEOME; RIBOSOME RNA; RRNA(ADENINE N6) METHYLTRANSFERASE; RRNA(ADENINE-N6)-METHYLTRANSFERASE;

AMINO ACID SEQUENCE; ANIMAL; ARCHAEBACTERIUM; ARTICLE; BACTERIAL GENE; BACTERIUM; BAYES THEOREM; EVOLUTION; GENETICS; HORIZONTAL GENE TRANSFER; HUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASTID; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STATISTICAL MODEL;

AMINO ACID SEQUENCE; ANIMALS; ARCHAEA; BACTERIA; BAYES THEOREM; CONSERVED SEQUENCE; EVOLUTION; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; HUMANS; LIKELIHOOD FUNCTIONS; METHYLTRANSFERASES; PHYLOGENY; PLASTIDS; PROTEOME; RNA, RIBOSOMAL; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN;

ALGAE; ARCHAEA; BACTERIA (MICROORGANISMS); CHLAMYDIAE; CYANOBACTERIA; EUKARYOTA; PROTEOBACTERIA;

EID: 58049138212     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2008.10.020     Document Type: Article

References (51)

1. Abascal F., Zardoya R., and Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21 (2005) 2104-2105
2. Archibald J.M., and Keeling P.J. Recycled plastids: a 'green movement' in eukaryotic evolution. Trends Genet. 18 (2002) 577-584
3. Archibald J.M., Rogers M.B., Toop M., Ishida K., and Keeling P.J. Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc. Natl. Acad. Sci. USA 100 (2003) 7678-7683
4. Arthur M., Brisson-Noel A., and Courvalin P. Origin and evolution of genes specifying resistance to macrolide, lincosamide and streptogramin antibiotics: data and hypotheses. J. Antimicrob. Chemother. 20 (1987) 783-802
5. Balashov S.P., Imasheva E.S., Boichenko V.A., Anton J., Wang J.M., and Lanyi J.K. Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 309 (2005) 2061-2064
6. Baughn A.D., and Malamy M.H. A mitochondrial-like aconitase in the bacterium Bacteroides fragilis: implications for the evolution of the mitochondrial Krebs cycle. Proc. Natl. Acad. Sci. USA 99 (2002) 4662-4667
7. Becker B., Hoef-Emden K., and Melkonian M. Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes. BMC Evol. Biol. 8 (2008) 203
8. Brinkman F.S., Blanchard J.L., Cherkasov A., Av-Gay Y., Brunham R.C., Fernandez R.C., Finlay B.B., Otto S.P., Ouellette B.F., Keeling P.J., Rose A.M., Hancock R.E., Jones S.J., and Greberg H. Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast. Genome Res. 12 (2002) 1159-1167
9. Cotney J., and Shadel G.S. Evidence for an early gene duplication event in the evolution of the mitochondrial transcription factor B family and maintenance of rRNA methyltransferase activity in human mtTFB1 and mtTFB2. J. Mol. Evol. 63 (2006) 707-717
10. Douglas S.E. Plastid evolution: origins, diversity, trends. Curr. Opin. Genet. Dev. 8 (1998) 655-661
11. Falkenberg M., Gaspari M., Rantanen A., Trifunovic A., Larsson N.G., and Gustafsson C.M. Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat. Genet. 31 (2002) 289-294
12. Fan J., Schnare M.N., and Lee R.W. Characterization of fragmented mitochondrial ribosomal RNAs of the colorless green alga Polytomella parva. Nucleic Acids Res. 31 (2003) 769-778
13. Fichera M.E., and Roos D.S. A plastid organelle as a drug target in apicomplexan parasites. Nature 390 (1997) 407-409
14. Gaspari M., Larsson N.G., and Gustafsson C.M. The transcription machinery in mammalian mitochondria. Biochim. Biophys. Acta 1659 (2004) 148-152
15. Grauvogel C., Brinkmann H., and Petersen J. Evolution of the glucose-6-phosphate isomerase: the plasticity of primary metabolism in photosynthetic eukaryotes. Mol. Biol. Evol. 24 (2007) 1611-1621
16. Greub G., and Raoult D. History of the ADP/ATP-translocase-encoding gene, a parasitism gene transferred from a Chlamydiales ancestor to plants 1 billion years ago. Appl. Environ. Microbiol. 69 (2003) 5530-5535
17. Guindon S., and Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52 (2003) 696-704
18. Helser T.L., Davies J.E., and Dahlberg J.E. Change in methylation of 16S ribosomal RNA associated with mutation to kasugamycin resistance in Escherichia coli. Nat. New Biol. 233 (1971) 12-14
19. Horn M., Collingro A., Schmitz-Esser S., Beier C.L., Purkhold U., Fartmann B., Brandt P., Nyakatura G.J., Droege M., Frishman D., Rattei T., Mewes H.W., and Wagner M. Illuminating the evolutionary history of chlamydiae. Science 304 (2004) 728-730
20. Huang J., and Gogarten J.P. Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids?. Genome Biol. 8 (2007) R99
21. Huelsenbeck J.P., and Ronquist F. MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17 (2001) 754-755
22. Kalman S., Mitchell W., Marathe R., Lammel C., Fan J., Hyman R.W., Olinger L., Grimwood J., Davis R.W., and Stephens R.S. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat. Genet. 21 (1999) 385-389
23. Keeling P.J. A brief history of plastids and their hosts. Protist 155 (2004) 3-7
24. Keeling P.J. Diversity and evolutionary history of plastids and their hosts. Am. J. Bot. 91 (2004) 1481-1493
25. Klootwijk J., Klein I., and Grivell L.A. Minimal post-transcriptional modification of yeast mitochondrial ribosomal RNA. J. Mol. Biol. 97 (1975) 337-350
26. Lafontaine D., Delcour J., Glasser A.L., Desgres J., and Vandenhaute J. The DIM1 gene responsible for the conserved m6(2)Am6(2)A dimethylation in the 3′-terminal loop of 18S rRNA is essential in yeast. J. Mol. Biol. 241 (1994) 492-497
27. Lafontaine D., Vandenhaute J., and Tollervey D. The 18S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast. Genes Dev. 9 (1995) 2470-2481
28. Lister D.L., Bateman J.M., Purton S., and Howe C.J. DNA transfer from chloroplast to nucleus is much rarer in Chlamydomonas than in tobacco. Gene 316 (2003) 33-38
29. Martin W., Stoebe B., Goremykin V., Hapsmann S., Hasegawa M., and Kowallik K.V. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393 (1998) 162-165
30. Mongodin E.F., Nelson K.E., Daugherty S., Deboy R.T., Wister J., Khouri H., Weidman J., Walsh D.A., Papke R.T., Sanchez Perez G., Sharma A.K., Nesbo C.L., MacLeod D., Bapteste E., Doolittle W.F., Charlebois R.L., Legault B., and Rodriguez-Valera F. The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc. Natl. Acad. Sci. USA 102 (2005) 18147-18152
31. Moustafa A., Reyes-Prieto A., and Bhattacharya D. Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions. Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions (2008) e2205
32. Noon K.R., Bruenger E., and McCloskey J.A. Posttranscriptional modifications in 16S and 23S rRNAs of the archaeal hyperthermophile Sulfolobus solfataricus. J. Bacteriol. 180 (1998) 2883-2888
33. Nosenko T., Lidie K.L., Van Dolah F.M., Lindquist E., Cheng J.F., and Bhattacharya D. Chimeric plastid proteome in the Florida "red tide" dinoflagellate Karenia brevis. Mol. Biol. Evol. 23 (2006) 2026-2038
34. O'Farrell H.C., Pulicherla N., Desai P.M., and Rife J.P. Recognition of a complex substrate by the KsgA/Dim1 family of enzymes has been conserved throughout evolution. RNA 12 (2006) 725-733
35. O'Farrell H.C., Scarsdale J.N., and Rife J.P. Crystal structure of KsgA, a universally conserved rRNA adenine dimethyltransferase in Escherichia coli. J. Mol. Biol. 339 (2004) 337-353
36. Patron N.J., Waller R.F., Archibald J.M., and Keeling P.J. Complex protein targeting to dinoflagellate plastids. J. Mol. Biol. 348 (2005) 1015-1024
37. Richly E., and Leister D. An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329 (2004) 11-16
38. Rogers M., Watkins R., Harper J., Durnford D., Gray M., and Keeling P. A complex and punctate distribution of three eukaryotic genes derived by lateral gene transfer. BMC Evol. Biol. 7 (2007) 89
39. Schmitz-Esser S., Linka N., Collingro A., Beier C.L., Neuhaus H.E., Wagner M., and Horn M. ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to Chlamydiae and Rickettsiae. J. Bacteriol. 186 (2004) 683-691
40. Schnare M.N., Heinonen T.Y., Young P.G., and Gray M.W. A discontinuous small subunit ribosomal RNA in Tetrahymena pyriformis mitochondria. J. Biol. Chem. 261 (1986) 5187-5193
41. Schubot F.D., Chen C.J., Rose J.P., Dailey T.A., Dailey H.A., and Wang B.C. Crystal structure of the transcription factor sc-mtTFB offers insights into mitochondrial transcription. Protein Sci. 10 (2001) 1980-1988
42. Seidel-Rogol B.L., McCulloch V., and Shadel G.S. Human mitochondrial transcription factor B1 methylates ribosomal RNA at a conserved stem-loop. Nat. Genet. 33 (2003) 23-24
43. Shadel G.S., and Clayton D.A. A Saccharomyces cerevisiae mitochondrial transcription factor, sc-mtTFB, shares features with sigma factors but is functionally distinct. Mol. Cell. Biol. 15 (1995) 2101-2108
44. Shutt T.E., and Gray M.W. Homologs of mitochondrial transcription factor B, sparsely distributed within the eukaryotic radiation, are likely derived from the dimethyladenosine methyltransferase of the mitochondrial endosymbiont. Mol. Biol. Evol. 23 (2006) 1169-1179
45. Stephens R.S., Kalman S., Lammel C., Fan J., Marathe R., Aravind L., Mitchell W., Olinger L., Tatusov R.L., Zhao Q., Koonin E.V., and Davis R.W. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282 (1998) 754-759
46. Teich R., Zauner S., Baurain D., Brinkmann H., and Petersen J. Origin and distribution of Calvin cycle fructose and sedoheptulose bisphosphatases in plantae and complex algae: a single secondary origin of complex red plastids and subsequent propagation via tertiary endosymbioses. Protist 158 (2007) 263-276
47. Timmis J.N., Ayliffe M.A., Huang C.Y., and Martin W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5 (2004) 123-135
48. Tokuhisa J.G., Vijayan P., Feldmann K.A., and Browse J.A. Chloroplast development at low temperatures requires a homolog of DIM1, a yeast gene encoding the 18S rRNA dimethylase. Plant Cell 10 (1998) 699-711
49. Tyra H.M., Linka M., Weber A.P., and Bhattacharya D. Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol. 8 (2007) R212
50. Van Buul C.P., Hamersma M., Visser W., and Van Knippenberg P.H. Partial methylation of two adjacent adenosines in ribosomes from Euglena gracilis chloroplasts suggests evolutionary loss of an intermediate stage in the methyl-transfer reaction. Nucleic Acids Res. 12 (1984) 9205-9208
51. Van Knippenberg P.H., Van Kimmenade J.M., and Heus H.A. Phylogeny of the conserved 3′ terminal structure of the RNA of small ribosomal subunits. Nucleic Acids Res. 12 (1984) 2595-2604