Home LiteratureArticle Details
PMID: 20686567 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

The Amphimedon queenslandica genome and the evolution of animal complexity.

Nature ·Vol. 466 ·No. 7307 ·2010-08-05 ·Pages 720-6

Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS

Abstract

Sponges are an ancient group of animals that diverged from other metazoans over 600 million years ago. Here we present the draft genome sequence of Amphimedon queenslandica, a demosponge from the Great Barrier Reef, and show that it is remarkably similar to other animal genomes in content, structure and organization. Comparative analysis enabled by the sequencing of the sponge genome reveals genomic events linked to the origin and early evolution of animals, including the appearance, expansion and diversification of pan-metazoan transcription factor, signalling pathway and structural genes. This diverse 'toolkit' of genes correlates with critical aspects of all metazoan body plans, and comprises cell cycle control and growth, development, somatic- and germ-cell specification, cell adhesion, innate immunity and allorecognition. Notably, many of the genes associated with the emergence of animals are also implicated in cancer, which arises from defects in basic processes associated with metazoan multicellularity.

MeSH Terms
Animals Apoptosis/genetics Cell Adhesion/genetics Cell Cycle/genetics Cell Polarity/genetics Cell Proliferation Evolution, Molecular Genes/genetics Genome/genetics Genomics Humans Immunity, Innate/genetics Models, Biological Neurons/metabolism Phosphotransferases/chemistry,genetics Phylogeny Porifera/anatomy & histology,cytology,genetics,immunology Sequence Analysis, DNA Signal Transduction/genetics
Chemicals
Phosphotransferases
Authors & Affiliations
33 authors, click to expand affiliations / ORCID
Srivastava Mansi
Center for Integrative Genomics and Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, USA. mansi@wi.mit.edu
Simakov Oleg
Chapman Jarrod
Fahey Bryony
Gauthier Marie E A
Mitros Therese
Richards Gemma S
Conaco Cecilia
Dacre Michael
Hellsten Uffe
Larroux Claire
Putnam Nicholas H
Stanke Mario
Adamska Maja
Darling Aaron
Degnan Sandie M
Oakley Todd H
Plachetzki David C
Zhai Yufeng
Adamski Marcin
Calcino Andrew
Cummins Scott F
Goodstein David M
Harris Christina
Jackson Daniel J
Leys Sally P
Shu Shengqiang
Woodcroft Ben J
Vervoort Michel
Kosik Kenneth S
Manning Gerard
Degnan Bernard M
Rokhsar Daniel S
References (59)
59 references, click to expand
  1. The Trichoplax genome and the nature of placozoans.
    Nature. 2008 Aug 21;454(7207):955-60 PMID: 18719581
  2. Sponge homologs of vertebrate protein tyrosine kinases and frequent domain shufflings in the early evolution of animals before the parazoan-eumetazoan split.
    Gene. 2001 Dec 12;280(1-2):195-201 PMID: 11738833
  3. Early evolution of animal cell signaling and adhesion genes.
    Proc Natl Acad Sci U S A. 2006 Aug 15;103(33):12451-6 PMID: 16891419
  4. The NK homeobox gene cluster predates the origin of Hox genes.
    Curr Biol. 2007 Apr 17;17(8):706-10 PMID: 17379523
  5. Cytological basis of photoresponsive behavior in a sponge larva.
    Biol Bull. 2001 Dec;201(3):323-38 PMID: 11751245
  6. Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa.
    Mol Biol Evol. 2009 Oct;26(10):2261-74 PMID: 19597161
  7. Early evolution of the LIM homeobox gene family.
    BMC Biol. 2010 Jan 18;8:4 PMID: 20082688
  8. Wnt and TGF-beta expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning.
    PLoS One. 2007 Oct 10;2(10):e1031 PMID: 17925879
  9. The zootype and the phylotypic stage.
    Nature. 1993 Feb 11;361(6412):490-2 PMID: 8094230
  10. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.
    Syst Biol. 2003 Oct;52(5):696-704 PMID: 14530136
  11. Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model.
    BMC Evol Biol. 2007 Feb 08;7 Suppl 1:S4 PMID: 17288577
  12. The genomic underpinnings of apoptosis in Strongylocentrotus purpuratus.
    Dev Biol. 2006 Dec 1;300(1):321-34 PMID: 17010332
  13. CONSEL: for assessing the confidence of phylogenetic tree selection.
    Bioinformatics. 2001 Dec;17(12):1246-7 PMID: 11751242
  14. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.
    Mol Biol Evol. 2000 Apr;17(4):540-52 PMID: 10742046
  15. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization.
    Science. 2007 Jul 6;317(5834):86-94 PMID: 17615350
  16. PANTHER: a browsable database of gene products organized by biological function, using curated protein family and subfamily classification.
    Nucleic Acids Res. 2003 Jan 1;31(1):334-41 PMID: 12520017
  17. Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics.
    BMC Evol Biol. 2007 Mar 02;7:33 PMID: 17335570
  18. Broad phylogenomic sampling improves resolution of the animal tree of life.
    Nature. 2008 Apr 10;452(7188):745-9 PMID: 18322464
  19. The Pfam protein families database.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D138-41 PMID: 14681378
  20. Innate immune defense of the sponge Suberites domuncula against bacteria involves a MyD88-dependent signaling pathway. Induction of a perforin-like molecule.
    J Biol Chem. 2005 Jul 29;280(30):27949-59 PMID: 15923643
  21. Type IV collagen in sponges, the missing link in basement membrane ubiquity.
    Biol Cell. 1996;88(1-2):37-44 PMID: 9175266
  22. MRBAYES: Bayesian inference of phylogenetic trees.
    Bioinformatics. 2001 Aug;17(8):754-5 PMID: 11524383
  23. Concatenated analysis sheds light on early metazoan evolution and fuels a modern "urmetazoon" hypothesis.
    PLoS Biol. 2009 Jan 27;7(1):e20 PMID: 19175291
  24. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing.
    Bioinformatics. 2002 Mar;18(3):502-4 PMID: 11934758
  25. Circular proteoglycans from sponges: first members of the spongican family.
    Cell Mol Life Sci. 2003 Jan;60(1):88-112 PMID: 12613660
  26. Late Precambrian bilaterians: grades and clades.
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6751-7 PMID: 8041693
  27. Origin of the metazoan immune system: identification of the molecules and their functions in sponges.
    Integr Comp Biol. 2003 Apr;43(2):281-92 PMID: 21680435
  28. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process.
    Mol Biol Evol. 2004 Jun;21(6):1095-109 PMID: 15014145
  29. The amphioxus genome and the evolution of the chordate karyotype.
    Nature. 2008 Jun 19;453(7198):1064-71 PMID: 18563158
  30. Demosponge and sea anemone fibrillar collagen diversity reveals the early emergence of A/C clades and the maintenance of the modular structure of type V/XI collagens from sponge to human.
    J Biol Chem. 2008 Oct 17;283(42):28226-35 PMID: 18697744
  31. Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity.
    Evol Dev. 2006 Mar-Apr;8(2):150-73 PMID: 16509894
  32. Computational inference of homologous gene structures in the human genome.
    Genome Res. 2001 May;11(5):803-16 PMID: 11337476
  33. Bauplan of urmetazoa: basis for genetic complexity of metazoa.
    Int Rev Cytol. 2004;235:53-92 PMID: 15219781
  34. Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity.
    Genome Res. 2008 Jul;18(7):1112-26 PMID: 18562681
  35. The premetazoan ancestry of cadherins.
    Science. 2008 Feb 15;319(5865):946-8 PMID: 18276888
  36. MrBayes 3: Bayesian phylogenetic inference under mixed models.
    Bioinformatics. 2003 Aug 12;19(12):1572-4 PMID: 12912839
  37. Genesis and expansion of metazoan transcription factor gene classes.
    Mol Biol Evol. 2008 May;25(5):980-96 PMID: 18296413
  38. A high percentage of introns in human genes were present early in animal evolution: evidence from the basal metazoan Nematostella vectensis.
    Genome Inform. 2006;17(1):219-29 PMID: 17503371
  39. The evolutionary origin of hedgehog proteins.
    Curr Biol. 2007 Oct 9;17(19):R836-7 PMID: 17925209
  40. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes.
    Science. 2002 Aug 23;297(5585):1301-10 PMID: 12142439
  41. Origin of metazoan adhesion molecules and adhesion receptors as deduced from cDNA analyses in the marine sponge Geodia cydonium: a review.
    Cell Tissue Res. 1997 Sep;289(3):383-95 PMID: 9232818
  42. The hallmarks of cancer.
    Cell. 2000 Jan 7;100(1):57-70 PMID: 10647931
  43. Characterization of the receptor protein-tyrosine kinase gene from the marine sponge Geodia cydonium.
    Prog Mol Subcell Biol. 1996;17:183-208 PMID: 8822805
  44. Multiple dicer genes in the early-diverging metazoa.
    Mol Biol Evol. 2009 Jun;26(6):1333-40 PMID: 19276153
  45. NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges.
    Dev Genes Evol. 2008 Sep;218(9):479-89 PMID: 18704494
  46. Origin of insulin receptor-like tyrosine kinases in marine sponges.
    Biol Bull. 1999 Oct;197(2):198-206 PMID: 10573839
  47. A post-synaptic scaffold at the origin of the animal kingdom.
    PLoS One. 2007 Jun 06;2(6):e506 PMID: 17551586
  48. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals.
    Nature. 2008 Oct 30;455(7217):1193-7 PMID: 18830242
  49. PANTHER: a library of protein families and subfamilies indexed by function.
    Genome Res. 2003 Sep;13(9):2129-41 PMID: 12952881
  50. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  51. Cadherins in embryonic and neural morphogenesis.
    Nat Rev Mol Cell Biol. 2000 Nov;1(2):91-100 PMID: 11253370
  52. The Demosponge Amphimedon queenslandica: Reconstructing the Ancestral Metazoan Genome and Deciphering the Origin of Animal Multicellularity.
    CSH Protoc. 2008 Dec 01;2008:pdb.emo108 PMID: 21356734
  53. The protist, Monosiga brevicollis, has a tyrosine kinase signaling network more elaborate and diverse than found in any known metazoan.
    Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9674-9 PMID: 18621719
  54. AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome.
    Genome Biol. 2006;7 Suppl 1:S11.1-8 PMID: 16925833
  55. Gene finding in novel genomes.
    BMC Bioinformatics. 2004 May 14;5:59 PMID: 15144565
  56. Multi-component complement system of Cnidaria: C3, Bf, and MASP genes expressed in the endodermal tissues of a sea anemone, Nematostella vectensis.
    Immunobiology. 2009;214(3):165-78 PMID: 19195737
  57. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans.
    Nature. 2008 Feb 14;451(7180):783-8 PMID: 18273011
  58. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships.
    Mol Biol Evol. 2010 Sep;27(9):1983-7 PMID: 20378579
  59. Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit.
    Curr Biol. 2008 Aug 5;18(15):1156-61 PMID: 18674909
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
DOI
10.1038/nature09201
Email
mansi@wi.mit.edu
Published
2010-08-05
Pages
720-6
Language
English
Region
England
NLM ID
0410462
PMCID
PMC3130542
Subset
IM
Grants
NHGRI NIH HHS · R01 HG004164 · United States
NHGRI NIH HHS · R01 HG004164-03 · United States
NHGRI NIH HHS · R01 HG004164-04 · United States
External Links
PubMed source DOI: 10.1038/nature09201 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2