The Capsaspora genome reveals a complex unicellular prehistory of animals

Nature Communications

Volumn 4, Issue , 2013, Pages

  Suga, Hiroshi ^a   Chen, Zehua ^b   De Mendoza, Alex ^a   Sebé Pedrós, Arnau ^a   Brown, Matthew W ^c   Kramer, Eric ^d   Carr, Martin ^e   Kerner, Pierre ^f   Vervoort, Michel ^f   Sánchez Pons, Núria ^a   Torruella, Guifré ^a   Derelle, Romain ^g   Manning, Gerard ^d   Lang, B Franz ^h   Russ, Carsten ^b   Haas, Brian J ^b   Roger, Andrew J ^c   Nusbaum, Chad ^b   Ruiz Trillo, Iñaki ^a,i,j  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c DALHOUSIE UNIVERSITY   (Canada)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^e UNIVERSITY OF HUDDERSFIELD   (United Kingdom)

^f INSTITUT JACQUES MONOD   (France)

^g CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^h Universite de Montreal   (Canada)

ⁱ UNIVERSITY OF BARCELONA   (Spain)

^j INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; ANCESTRY; ANIMAL; CYTOLOGY; EUKARYOTE; EVOLUTIONARY BIOLOGY; FLAGELLATE; FUNCTIONAL ROLE; GENETIC ANALYSIS; GENOME; METAZOAN; PROTEIN;

AMOEBA (LIFE CYCLE STAGE); ARTICLE; CAPSASPORA OWCZARZAKI; CELL ADHESION; CELL CYCLE REGULATION; CHOANOFLAGELLATE; ENDOSYMBIONT; GENOME; NONHUMAN; TRANSCRIPTION REGULATION;

ANIMALS; APOPTOSIS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; CELL ADHESION; CHOANOFLAGELLATA; EVOLUTION, MOLECULAR; GENOME; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MESOMYCETOZOEA; MITOCHONDRIA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84883125088     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3325     Document Type: Article

References (52)

1. Putnam, N. et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86-94 (2007). (Pubitemid 47056460)
2. Srivastava, M. et al. The Trichoplax genome and the nature of Placozoans. Nature 454, 955-960 (2008).
3. Srivastava, M. et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466, 720-726 (2010).
4. Chapman, J. et al. The dynamic genome of Hydra. Nature 464, 592-596 (2010).
5. Lang, B. F., O'Kelly, C., Nerad, T., Gray, M. W. & Burger, G. The closest unicellular relatives of animals. Curr. Biol. 12, 1773-1778 (2002). (Pubitemid 35169794)
6. Ruiz-Trillo, I., Roger, A., Burger, G., Gray, M. & Lang, B. A phylogenomic investigation into the origin of metazoa. Mol. Biol. Evol. 25, 664-672 (2008). (Pubitemid 351398321)
7. Shalchian-Tabrizi, K. et al. Multigene phylogeny of choanozoa and the origin of animals. PLoS One 3, e2098 (2008).
8. Torruella, G. et al. Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single-copy protein domains. Mol. Biol. Evol. 29, 531-544 (2012).
9. King, N. et al. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451, 783-788 (2008). (Pubitemid 351253174)
10. Manning, G., Young, S., Miller, W. & Zhai, Y. The protist, Monosiga brevicollis, has a tyrosine kinase signaling network more elaborate and diverse than found in any known metazoan. Proc. Natl Acad. Sci. USA 105, 9674-9679 (2008). (Pubitemid 352031359)
11. Pincus, D., Letunic, I., Bork, P. & Lim, W. Evolution of the phospho-tyrosine signaling machinery in premetazoan lineages. Proc. Natl Acad. Sci. USA 105, 9680-9684 (2008). (Pubitemid 352031360)
12. Rokas, A. The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu. Rev. Genet. 42, 235-251 (2008).
13. Fairclough, S. R. et al. Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol. 14, R15 (2013).
14. Zmasek, C. & Godzik, A. Strong functional patterns in the evolution of eukaryotic genomes revealed by the reconstruction of ancestral protein domain repertoires. Genome Biol. 12, R4 (2011).
15. Hertel, L., Bayne, C. & Loker, E. The symbiont Capsaspora owczarzaki, nov. gen. nov. sp., isolated from three strains of the pulmonate snail Biomphalaria glabrata is related to members of the Mesomycetozoea. Int. J. Parasitol. 32, 1183-1191 (2002). (Pubitemid 34761912)
16. Sebe-Pedros, A., Roger, A., Lang, F., King, N. & Ruiz-Trillo, I. Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc. Natl Acad. Sci. USA 107, 10142-10147 (2010).
17. Sebe-Pedros, A., de Mendoza, A., Lang, B., Degnan, B. & Ruiz-Trillo, I. Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol. Biol. Evol. 28, 1241-1254 (2011).
18. Young, S. et al. Premetazoan ancestry of the Myc-Max network. Mol. Biol. Evol. 28, 2961-2971 (2011).
19. Sebe-Pedros, A., Zheng, Y., Ruiz-Trillo, I. & Pan, D. Premetazoan origin of the hippo signaling pathway. Cell Rep. 1, 13-20 (2012).
20. Suga, H. et al. Genomic survey of premetazoans shows deep conservation of cytoplasmic tyrosine kinases and multiple radiations of receptor tyrosine kinases. Sci. Signal. 5, ra35 (2012).
21. Nichols, S. A., Roberts, B. W., Richter, D. J., Fairclough, S. R. & King, N. Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/beta-catenin complex. Proc. Natl Acad. Sci. USA 109, 13046-13051 (2012).
22. Carr, M., Nelson, M., Leadbeater, B. & Baldauf, S. Three families of LTR retrotransposons are present in the genome of the choanoflagellate Monosiga brevicollis. Protist 159, 579-590 (2008).
23. Kim, J., Vanguri, S., Boeke, J., Gabriel, A. & Voytas, D. Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 8, 464-478 (1998). (Pubitemid 28256796)
24. Ohno, S. Evolution by Gene Duplication 160 (Springer, 1970).
25. Hunter, S. et al. InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res. 40, D306-D312 (2012).
26. Wickstead, B. & Gull, K. The evolution of the cytoskeleton. J. Cell Biol. 194, 513-525 (2011).
27. Nichols, S. A., Dirks, W., Pearse, J. S. & King, N. Early evolution of animal cell signaling and adhesion genes. Proc. Natl Acad. Sci. USA 103, 1251-1256 (2006).
28. Degnan, B., Vervoort, M., Larroux, C. & Richards, G. Early evolution of metazoan transcription factors. Curr. Opin. Genet. Dev. 19, 591-599 (2009).
29. Burger, G., Lavrov, D., Forget, L. & Lang, B. Sequencing complete mitochondrial and plastid genomes. Nat. Protoc. 2, 603-614 (2007). (Pubitemid 47044695)
30. Jaffe, D. et al. Whole-genome sequence assembly for mammalian genomes: Arachne 2. Genome Res. 13, 91-96 (2003).
31. Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 9, R7 (2008).
32. Lomsadze, A., Ter-Hovhannisyan, V., Chernoff, Y. O. & Borodovsky, M. Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res. 33, 6494-6506 (2005). (Pubitemid 41806413)
33. Stanke, M. & Waack, S. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19(Suppl 2): ii215-ii225 (2003). (Pubitemid 41296659)
34. Majoros, W. H., Pertea, M. & Salzberg, S. L. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878-2879 (2004). (Pubitemid 39530188)
35. Birney, E., Clamp, M. & Durbin, R. GeneWise and Genomewise. Genome Res. 14, 988-995 (2004). (Pubitemid 38660520)
36. Haas, B. J. et al. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 5654-5666 (2003). (Pubitemid 37441936)
37. Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644-652 (2011).
38. Haas, B. J., Delcher, A. L., Wortman, J. R. & Salzberg, S. L. DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics 20, 3643-3646 (2004). (Pubitemid 40136803)
39. Li, L., Stoeckert, Jr. C. J. & Roos, D. S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189 (2003). (Pubitemid 37161775)
40. Katoh, K., Kuma, K., Toh, H. & Miyata, T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511-518 (2005). (Pubitemid 40360980)
41. Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552 (2000). (Pubitemid 30210700)
42. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 22, 2688-2690 (2006). (Pubitemid 44642609)
43. Lartillot, N., Lepage, T. & Blanquart, S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25, 2286-2288 (2009).
44. Lartillot, N. & Philippe, H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol. Biol. Evol. 21, 1095-1109 (2004). (Pubitemid 38658218)
45. Eddy, S. R. A new generation of homology search tools based on probabilistic inference. Genome. Inform. 23, 205-211 (2009).
46. Bauer, S., Grossmann, S., Vingron, M. & Robinson, P. N. Ontologizer 2.0-a multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics 24, 1650-1651 (2008). (Pubitemid 351966169)
47. Alexa, A., Rahnenfuhrer, J. & Lengauer, T. Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22, 1600-1607 (2006). (Pubitemid 43985293)
48. Quevillon, E. et al. InterProScan: protein domains identifier. Nucleic Acids Res. 33, W116-W120 (2005). (Pubitemid 44529891)
49. Gentleman, R. C. et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004).
50. Blake, J. A. & Harris, M. A. The Gene Ontology (GO) project: structured vocabularies for molecular biology and their application to genome and expression analysis. Curr. Protoc. Bioinformatics. Chapter 7, Unit 7.2 (2008).
51. Conesa, A. et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676 (2005). (Pubitemid 41264107)
52. Burge, S. et al. Manual GO annotation of predictive protein signatures: the InterPro approach to GO curation. Database (Oxford) 2012, bar068 (2012).