The enigmatic mitochondrial genome of Rhabdopleura compacta (Pterobranchia) reveals insights into selection of an efficient tRNA system and supports monophyly of Ambulacraria

BMC Evolutionary Biology

Detlef Bernhard⁴  Martin Schlegel¹  Peter F Stadler⁵  Matthias Bernt²  Joerg Hetmank⁴  Marleen Perseke³ 

[1] Interdisciplinary Center for Bioinformatics, University of Leipzig, Härtelstr, 16-18, 04107 Leipzig, Germany;Parallel Computing and Complex Systems Group, University of Leipzig, Johannisgasse, 26, 04103 Leipzig, Germany;Laboratory of Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Science, 164 West Xingang Road, 510301 Guangzhou, PR China;Molecular Evolution and Animal Systematics, University of Leipzig, Talstr. 33, 04103 Leipzig, Germany;Department of Theoretical Chemistry, University of Vienna, Währingerstrasse 17, 1090 Wien, Austria

关键词: codon-anticodon adaptation;    codon reassignment;    deuterostome evolution;    Pterobranchia;    Hemichordata;   

Others  :  1144287
DOI  :  10.1186/1471-2148-11-134

 received in 2011-03-07, accepted in 2011-05-20,  发布年份 2011

【 摘 要 】

Background

The Hemichordata comprises solitary-living Enteropneusta and colonial-living Pterobranchia, sharing morphological features with both Chordata and Echinodermata. Despite their key role for understanding deuterostome evolution, hemichordate phylogeny is controversial and only few molecular data are available for phylogenetic analysis. Furthermore, mitochondrial sequences are completely lacking for pterobranchs. Therefore, we determined and analyzed the complete mitochondrial genome of the pterobranch Rhabdopleura compacta to elucidate deuterostome evolution. Thereby, we also gained important insights in mitochondrial tRNA evolution.

Results

The mitochondrial DNA of Rhabdopleura compacta corresponds in size and gene content to typical mitochondrial genomes of metazoans, but shows the strongest known strand-specific mutational bias in the nucleotide composition among deuterostomes with a very GT-rich main-coding strand. The order of the protein-coding genes in R. compacta is similar to that of the deuterostome ground pattern. However, the protein-coding genes have been highly affected by a strand-specific mutational pressure showing unusual codon frequency and amino acid composition. This composition caused extremely long branches in phylogenetic analyses. The unusual codon frequency points to a selection pressure on the tRNA translation system to codon-anticodon sequences of highest versatility instead of showing adaptations in anticodon sequences to the most frequent codons. Furthermore, an assignment of the codon AGG to Lysine has been detected in the mitochondrial genome of R. compacta, which is otherwise observed only in the mitogenomes of some arthropods. The genomes of these arthropods do not have such a strong strand-specific bias as found in R. compacta but possess an identical mutation in the anticodon sequence of the tRNA_Lys.

Conclusion

A strong reversed asymmetrical mutational constraint in the mitochondrial genome of Rhabdopleura compacta may have arisen by an inversion of the replication direction and adaptation to this bias in the protein sequences leading to an enigmatic mitochondrial genome. Although, phylogenetic analyses of protein coding sequences are hampered, features of the tRNA system of R. compacta support the monophyly of Ambulacraria. The identical reassignment of AGG to Lysine in two distinct groups may have occurred by convergent evolution in the anticodon sequence of the tRNA_Lys.

【 授权许可】

   
2011 Perseke et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Benito J, Pardos F: Hemichordata. In Microscopic Anatomy of Invertebrates. Volume 15. Edited by Harrison MA. Wiley Liss. New York; 1997::15-101.
• [2]Sato T: Vorläufige Mitteilungen über Atubaria heterolopba gen. nov. sp. nov., einen in freiem Zustand aufgefundenen Pterobranchier aus dem Stillen Ozean. Zool Anz 1936, 115:97-106.
• [3]Hyman LH: Smaller Coelomate Groups: Hemichordata. In The Invertebrates. Volume 5. New York: McGraw-Hill Book Company; 1959::72-207.
• [4]Halanych KM: The phylogenetic position of the pterobranch hemichordates based on 18S rDNA sequence data. Mol Phyl Evol 1995, 4:72-76.
• [5]Cameron CB, Garey JR, Swalla BJ: Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci USA 2000, 97:4469-4474.
• [6]Winchell CJ, Sullivan J, Cameron CB, Swalla BJ, Mallatt J: Evaluating hypotheses of deuterostome phylogeny and chordate evolution with new LSU and SSU ribosomal DNA data. Mol Biol Evol 2002, 19:762-776.
• [7]Metschnikoff VE: Über die systematische Stellung von Balanoglossus. Zool Anz 1881, 4:139-157.
• [8]Lavrov DV, Lang BF: Poriferan mtDNA and animal phylogeny based on mitochondrial gene arrangements. Systematic Biol 2005, 54:651-659.
• [9]Nohara M, Nishida M, Miya M, Nishikawa T: Evolution of the mitochondrial genome in cephalochordata as inferred from complete nucleotide sequences from two Epigonichthys species. J Mol Biol 2005, 60:526-537.
• [10]Perseke M, Hankeln T, Weich B, Fritzsch G, Stadler PF, Israelsson O, Bernhard D, Schlegel M: The mitochondrial DNA of Xenoturbella bocki: genomic architecture and phylogenetic analysis. Theory of Biosci 2007, 126:35-42.
• [11]Perseke M, Bernhard D, Fritzsch G, Brümmer F, Stadler PF, Schlegel M: Mitochondrial genome evolution in Ophiuroides, Echinoidea, and Holthuroidea: Insights in phylogenetic relationships of Echinodermata. Mol Phyl Evol 2010, 56(1):201-211.
• [12]Boore JL: Animal mitochondrial genomes. Nucleic Acids Res 1999, 27:1767-1780.
• [13]Stach T, Braband A, Podsiadlowski L: Erosion of phylogenetic signal in tunicate mitochondrial genomes on different levels of analysis. Mol Phylogenet Evol 2010, 55:860-870.
• [14]Bourlat SJ, Rota-Stabelli O, Lanfear R, Telford MJ: The mitochondrial genome structure of Xenoturbella bocki (phylum Xenoturbellida) is ancestral within the deuterostomes. BMC Evol Biol 2009, 9:107. BioMed Central Full Text
• [15]Carullo M, Xia X: An Extensive Study of Mutation and Selection on the Wobble Nucleotide in tRNA Anticodons in Fungal Mitochondrial Genomes. J Mol Evol 2008, 66:484-493.
• [16]Xia X: The cost of wobble translation in fungal mitochondrial genomes: integration of two traditional hypotheses. BMC Evol Biol 2008, 8:211. BioMed Central Full Text
• [17]Xia X: Mutation and selection on the anticodon of tRNA genes in vertebrate mitochondrial genomes. Gene 2005, 345:13-20.
• [18]Tong KL, Wong JT: Anticodon and wobble evolution. Gene 2004, 333:169-177.
• [19]Yokobori S, Suzuki T, Watanabe K: Genetic code variations in mitochondria: tRNA as a major determinant of genetic code plasticity. J Mol Evol 2001, 53:314-326.
• [20]Yokoyama S, Nishimura S: Modified nucleotides and codon recognition. In tRNA: Structure, Biosynthesis and Function. Edited by Soll D, RajBhandary U. Washington, MA: ASM Press; 1995:207-223.
• [21]Bulmer M: The selection-mutation-drift theory of synonymous codon usage. Genetics 1991, 129:897-907.
• [22]Bulmer M: Coevolution of codon usage and transfer RNA abundance. Nature 1987, 325(6106):728-730.
• [23]Hassanin A, Léger N, Deutsch J: Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of Metazoa, and consequences for phylogenetic inferences. Syst Biol 2005, 54:277-298.
• [24]Krishnan NM, Seligmann H, Raina SZ, Pollock DD: Detecting gradients of asymmetry in site-specific substitutions in mitochondrial genomes. DNA Cell Biol 2004, 23:707-714.
• [25]Reyes A, Gissi C, Pesole G, Saccone C: Asymmetrical directional mutation pressure in the mitochondrial genome of mammals. Mol Biol Evol 1998, 15:957-966.
• [26]Grigoriev A: Analyzing genomes with cumulative skew diagrams. Nucleic Acids Res 1998, 26:2286-2290.
• [27]Francino MP, Ochman H: Strand asymmetries in DNA evolution. Trends Genet 1997, 13:240-245.
• [28]Frederico LA, Kunkel TA, Shaw BR: A sensitive genetic assay for the detection of cytosine deamination: determination of rate constants and the activation energy. Biochemistry 1990, 29:2532-2537.
• [29]Scouras A, Smith JM: The complete mitochondrial genomes of the sea lily Gymnocrinus richeri and the feather star Phanogenia gracilis: signature nucleotide bias and unique nad4L gene rearrangement within crinoids. Mol Phylogenet Evol 2006, 39:323-334.
• [30]Castresana J, Feldmaier-Fuchs G, Yokobori S, Satoh N, Päabo S: The mitochondrial genome of the hemichordata Balanoglossus carnosus and the evolution of deuterostome mitochondria. Genetics 1998, 150:1115-1123.
• [31]Castresana J, Feldmaier-Fuchs G, Päabo S: Codon reassignment and amino acid composition in hemichordate mitochondria. Proc Natl Acad Sci USA 1998, 95:3703-3707.
• [32]Ojala D, Montoya DJ, Attardi G: tRNA punctuation model of RNA processing in human mitochondria. Nature 1981, 290:470-474.
• [33]Brown TA, Cecconi C, Tkachuk AN: Replication of mitochondrial DNA occurs by strand displacement with alternative light-strand origins, not via a strand-coupled mechanism. Genes Dev 2005, 19:2466-2476.
• [34]Pikó L, Bulpitt KJ, Meyer R: Structural and replicative forms of mitochondrial DNA in tissues from adult and senescent BALB/c mice and Fischer 344 rats. Mech. Ageing Dev 1984, 26:113-131.
• [35]Koike K, Wolstenholme DR: Evidence for discontinuous replication of circular mitochondrial DNA molecules from Novikoff rat ascites hepatoma cells. J. Cell Biol 1974, 61:14-25.
• [36]Holt IJ, Jacobs HT: Response: The mitochondrial DNA replication bubble has not burst. Trends Biochem. Sci 2003, 28:355-356.
• [37]Yang MY, Bowmaker M, Reyes A, Vergani L, Angeli P, Gringeri E, Jacobs HT, Holt IJ: Biased incorporation of ribonucleotides on the mitochondrial L-strand accounts for apparent strand-asymmetric DNA replication. Cell 2002, 111:495-505.
• [38]Holt IJ, Lorimer HE, Jacobs HT: Coupled leading and lagging-strand synthesis of mammalian mitochondrial DNA. Cell 2000, 100:515-524.
• [39]Yasukawa T, Yang MY, Jacobs HT, Holt IJ: A bidirectional origin of replication maps to the major noncoding region of human mitochondrial DNA. Mol. Cell 2005, 18:651-662.
• [40]Bowmaker M, Yang MY, Yasukawa T, Reyes A, Jacobs HT, Huberman JA, Holt IJ: Mammalian mitochondrial DNA replicates bidirectionally from an initiation zone. J. Biol. Chem 2003, 278:50961-50969.
• [41]Abascal F, Zardoya R, Posada D: GenDecoder: genetic code prediction for metazoan mitochondria. Nucleic Acids Res 2006, 34:389-393.
• [42]Matsuyama S, Ueda T, Crain PF, McCloskey JA, Watanabe K: A novel wobble rule found in starfish mitochondria. J Biol Chem 1998, 273:3363-3368.
• [43]Tomita K, Ueda T, Watanabe K: 7-Methylguanosine at the anticodon wobble position of squid mitochondrial tRNA(Ser)GCU: Molecular basis for assignment of AGA/AGG codons as serine in invertebrate mitochondria. Biochim Biophys Acta 1998, 1399:78-82.
• [44]Kondow A, Suzuki T, Yokobori S, Ueda T, Watanabe K: An extra tRNAGly(U*CU) found in ascidian mitochondria responsible for decoding non-universal codons AGA/AGG as glycine. Nucleic Acids Res 1999, 27:2554-2559.
• [45]Ivanov V, Beniaminov A, Mikheyev A, Minyat E: A mechanism for stop codon recognition by the ribosome: A bioinformatic approach. RNA 2001, 7:1683-1692.
• [46]Osawa S, Jukes ST, Watanabe K, Muto A: Recent evidence for evolution of the genetic code. Microbiol Rev 1992, 56:229-264.
• [47]Abascal F, Posada D, Knight RD, Zardoya R: Parallel evolution of the genetic code in arthropod mitochondrial genomes. PLOS Biol 2006, 4:e127.
• [48]Asakawa S, Himeno H, Miura K, Watanabe K: Nucleotide sequence and gene organization of the starfish Asterina pectinifera mitochondrial genome. Genetics 1995, 140:1047-1060.
• [49]Schultz DW, Yarus M: Transfer RNA mutation and the malleability of the genetic code. J Mol Biol 1994, 235:1377-1380.
• [50]Schultz DW, Yarus M: On malleability in the genetic code. J Mol Evol 1996, 42:597-601.
• [51]Massey SE, Moura G, Beltrao P, Almeida R, Garey JR, Tuite MF, Santos MAS: Comparative evolutionary genomics unveils the molecular mechanism of reassignment of the CTG codon in Candida spp. Genome Res 2003, 13:544-557.
• [52]Jukes TH, Osawa S: Further Comments on Codon Reassignment. J Mol Evol 1997, 45:1-8.
• [53]Zhang Z, Yu J: Modeling compositional dynamics based on GC and purine contents of protein-coding sequences. Biology Direct 2010, 5:63. BioMed Central Full Text
• [54]Perseke M, Fritzsch G, Ramsch K, Bernt M, Merkle D, Middendorf M, Bernhard D, Stadler PF, Schlegel M: Evolution of mitochondrial gene orders in echinoderms. Mol Phylogenet Evol 2008, 47:855-864.
• [55]Scouras A, Beckenbach K, Arndt A, Smith JM: Complete mitochondrial genome DNA sequence for two ophiuroids and a holothuroid: the utility of protein gene sequence and gene maps in the analyses of deep deuterostome phylogeny. Mol. Phylogenet. Evol 2004, 31:50-65.
• [56]Lowe TM, Eddy SR: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964.
• [57]Lobry JR: Properties of a general model of DNA evolution under no-strand bias conditions. J Mol Evol 1995, 40:326-330.
• [58]Pruitt KD, Tatusova T, Maglott DR: NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 2007, 35:D61-D65.
• [59]Bernt M, Merkle D, Ramsch K, Fritzsch G, Perseke M, Bernhard D, Schlegel M, Stadler PF, Middendorf M: CREx: inferring genomic rearrangements based on common intervals. Bioinformatics 2007, 23(21):2957-2958.
• [60]Park JK, Kim KH, Kang SH, Kim JH, Eom KS, Littlewood DTJ: A common origin of complex life cycles in parasitic flatworms: evidence from the complete mitochondrial genome of Microcotyle sebastis. BMC Evol Biol 2007, 7:11. BioMed Central Full Text
• [61]He Y, Jones J, Armstrong M, Lamberti F, Moens M: The mitochondrial genome of Xiphinema americanum sensu stricto (Nematoda: enoplea): Considerable economization in the length and structural features of encoded genes. J Mol Evol 2005, 61:819-833.
• [62]Notredame C, Higgins D, Heringa J: T-Coffee: a novel method for multiple sequence alignments. J Mol Biol 2000, 302:205-217.
• [63]Guindon S, Gascuel O: A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 2003, 52:696-704.
• [64]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.