Home LiteratureArticle Details
PMID: 15875012 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The genome of the social amoeba Dictyostelium discoideum.

Nature ·Vol. 435 ·No. 7038 ·2005-05-05 ·Pages 43-57

Eichinger L, Pachebat JA, Glöckner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny D, Mourier T, Pain A, Lu M, Harper D, Lindsay R, Hauser H, James K, Quiles M, Madan Babu M, Saito T, Buchrieser C, Wardroper A, Felder M, Thangavelu M, Johnson D, Knights A, Loulseged H, Mungall K, Oliver K, Price C, Quail MA, Urushihara H, Hernandez J, Rabbinowitsch E, Steffen D, Sanders M, Ma J, Kohara Y, Sharp S, Simmonds M, Spiegler S, Tivey A, Sugano S, White B, Walker D, Woodward J, Winckler T, Tanaka Y, Shaulsky G, Schleicher M, Weinstock G, Rosenthal A, Cox EC, Chisholm RL, Gibbs R, Loomis WF, Platzer M, Kay RR, Williams J, Dear PH, Noegel AA, Barrell B, Kuspa A

Abstract

The social amoebae are exceptional in their ability to alternate between unicellular and multicellular forms. Here we describe the genome of the best-studied member of this group, Dictyostelium discoideum. The gene-dense chromosomes of this organism encode approximately 12,500 predicted proteins, a high proportion of which have long, repetitive amino acid tracts. There are many genes for polyketide synthases and ABC transporters, suggesting an extensive secondary metabolism for producing and exporting small molecules. The genome is rich in complex repeats, one class of which is clustered and may serve as centromeres. Partial copies of the extrachromosomal ribosomal DNA (rDNA) element are found at the ends of each chromosome, suggesting a novel telomere structure and the use of a common mechanism to maintain both the rDNA and chromosomal termini. A proteome-based phylogeny shows that the amoebozoa diverged from the animal-fungal lineage after the plant-animal split, but Dictyostelium seems to have retained more of the diversity of the ancestral genome than have plants, animals or fungi.

MeSH Terms
ATP-Binding Cassette Transporters/genetics Animals Base Composition Cell Adhesion/genetics Cell Movement/genetics Centromere/genetics Conserved Sequence/genetics DNA Transposable Elements/genetics DNA, Ribosomal/genetics Dictyostelium/cytology,enzymology,genetics,metabolism Eukaryotic Cells/metabolism Gene Duplication Gene Transfer, Horizontal/genetics Genome Genomics Humans Molecular Sequence Data Phylogeny Proteome Protozoan Proteins/chemistry,genetics RNA, Transfer/genetics Repetitive Sequences, Nucleic Acid/genetics Sequence Analysis, DNA Signal Transduction/genetics Social Behavior Telomere/genetics
Chemicals
ATP-Binding Cassette Transporters DNA Transposable Elements DNA, Ribosomal Proteome Protozoan Proteins RNA, Transfer
Authors & Affiliations
97 authors, click to expand affiliations / ORCID
Eichinger L
Center for Biochemistry and Center for Molecular Medicine Cologne, University of Cologne, Joseph-Stelzmann-Str. 52, 50931 Cologne, Germany.
Pachebat J A
Glöckner G
Rajandream M-A
Sucgang R
Berriman M
Song J
Olsen R
Szafranski K
Xu Q
Tunggal B
Kummerfeld S
Madera M
Konfortov B A
Rivero F
Bankier A T
Lehmann R
Hamlin N
Davies R
Gaudet P
Fey P
Pilcher K
Chen G
Saunders D
Sodergren E
Davis P
Kerhornou A
Nie X
Hall N
Anjard C
Hemphill L
Bason N
Farbrother P
Desany B
Just E
Morio T
Rost R
Churcher C
Cooper J
Haydock S
van Driessche N
Cronin A
Goodhead I
Muzny D
Mourier T
Pain A
Lu M
Harper D
Lindsay R
Hauser H
James K
Quiles M
Madan Babu M
Saito T
Buchrieser C
Wardroper A
Felder M
Thangavelu M
Johnson D
Knights A
Loulseged H
Mungall K
Oliver K
Price C
Quail M A
Urushihara H
Hernandez J
Rabbinowitsch E
Steffen D
Sanders M
Ma J
Kohara Y
Sharp S
Simmonds M
Spiegler S
Tivey A
Sugano S
White B
Walker D
Woodward J
Winckler T
Tanaka Y
Shaulsky G
Schleicher M
Weinstock G
Rosenthal A
Cox E C
Chisholm R L
Gibbs R
Loomis W F
Platzer M
Kay R R
Williams J
Dear P H
Noegel A A
Barrell B
Kuspa A
References (92)
92 references, click to expand
  1. A high-resolution HAPPY map of Dictyostelium discoideum chromosome 6.
    Genome Res. 2000 Nov;10(11):1737-42 PMID: 11076859
  2. A transcriptional profile of multicellular development in Dictyostelium discoideum.
    Development. 2002 Apr;129(7):1543-52 PMID: 11923193
  3. Structure of an activated Dictyostelium STAT in its DNA-unbound form.
    Mol Cell. 2004 Mar 26;13(6):791-804 PMID: 15053873
  4. Evolution of key cell signaling and adhesion protein families predates animal origins.
    Science. 2003 Jul 18;301(5631):361-3 PMID: 12869759
  5. Analyses of cDNAs from growth and slug stages of Dictyostelium discoideum.
    Nucleic Acids Res. 2004;32(5):1647-53 PMID: 15010511
  6. Transcriptional transitions during Dictyostelium spore germination.
    Eukaryot Cell. 2004 Oct;3(5):1101-10 PMID: 15470238
  7. Leading the way: Directional sensing through phosphatidylinositol 3-kinase and other signaling pathways.
    J Cell Sci. 2003 Sep 1;116(Pt 17):3471-8 PMID: 12893811
  8. Happy mapping: linkage mapping using a physical analogue of meiosis.
    Nucleic Acids Res. 1993 Jan 11;21(1):13-20 PMID: 8441608
  9. A cell-adhesion pathway regulates intercellular communication during Dictyostelium development.
    Dev Biol. 2003 Dec 15;264(2):506-21 PMID: 14651934
  10. Signal transduction pathways leading to spore differentiation in Dictyostelium discoideum.
    Dev Biol. 1998 Jan 15;193(2):146-55 PMID: 9473320
  11. TagA, a putative serine protease/ABC transporter of Dictyostelium that is required for cell fate determination at the onset of development.
    Development. 2003 Jul;130(13):2953-65 PMID: 12756178
  12. SH2 signaling in a lower eukaryote: a STAT protein that regulates stalk cell differentiation in dictyostelium.
    Cell. 1997 Jun 13;89(6):909-16 PMID: 9200609
  13. Genome-wide expression analyses of gene regulation during early development of Dictyostelium discoideum.
    Eukaryot Cell. 2003 Aug;2(4):664-70 PMID: 12912885
  14. A specific glycoprotein as the target site of adhesion blocking Fab in aggregating Dictyostelium cells.
    Nature. 1978 Aug 3;274(5670):445-9 PMID: 566857
  15. AmpA, a modular protein containing disintegrin and ornatin domains, has multiple effects on cell adhesion and cell fate specification.
    J Muscle Res Cell Motil. 2002;23(7-8):817-28 PMID: 12952080
  16. The actin cytoskeleton of Dictyostelium: a story told by mutants.
    J Cell Sci. 2000 Mar;113 ( Pt 5):759-66 PMID: 10671366
  17. Horizontal gene transfer and the evolution of parasitic protozoa.
    Protist. 2003 Apr;154(1):17-32 PMID: 12812367
  18. Molecular tinkering of G protein-coupled receptors: an evolutionary success.
    EMBO J. 1999 Apr 1;18(7):1723-9 PMID: 10202136
  19. Glutamine repeats and neurodegeneration.
    Annu Rev Neurosci. 2000;23:217-47 PMID: 10845064
  20. A molecular clock based on the expansion of gene families.
    Nucleic Acids Res. 1996 Mar 15;24(6):995-9 PMID: 8604358
  21. The mitochondrial DNA of Dictyostelium discoideum: complete sequence, gene content and genome organization.
    Mol Gen Genet. 2000 Apr;263(3):514-9 PMID: 10821186
  22. Cbl: many adaptations to regulate protein tyrosine kinases.
    Nat Rev Mol Cell Biol. 2001 Apr;2(4):294-307 PMID: 11283727
  23. Template jumping by a LINE reverse transcriptase has created a SINE-like 5S rRNA retropseudogene in Dictyostelium.
    Mol Genet Genomics. 2004 Feb;271(1):98-102 PMID: 14652739
  24. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium.
    Annu Rev Cell Biol. 1988;4:649-86 PMID: 2848555
  25. The Production of Homozygous Deficient Tissues with Mutant Characteristics by Means of the Aberrant Mitotic Behavior of Ring-Shaped Chromosomes.
    Genetics. 1938 Jul;23(4):315-76 PMID: 17246891
  26. Electrophoretic karyotype for Dictyostelium discoideum.
    Proc Natl Acad Sci U S A. 1990 Nov;87(21):8247-51 PMID: 2236037
  27. An orderly retreat: Dedifferentiation is a regulated process.
    Proc Natl Acad Sci U S A. 2004 May 4;101(18):7005-10 PMID: 15103019
  28. Evolutionary analyses of ABC transporters of Dictyostelium discoideum.
    Eukaryot Cell. 2002 Aug;1(4):643-52 PMID: 12456012
  29. Sequence and analysis of chromosome 2 of Dictyostelium discoideum.
    Nature. 2002 Jul 4;418(6893):79-85 PMID: 12097910
  30. A multidrug resistance transporter/serine protease gene is required for prestalk specialization in Dictyostelium.
    Genes Dev. 1995 May 1;9(9):1111-22 PMID: 7744252
  31. Sequence of Dictyostelium DIRS-1: an apparent retrotransposon with inverted terminal repeats and an internal circle junction sequence.
    Cell. 1985 Nov;43(1):105-15 PMID: 2416457
  32. Disruption of the gene encoding the EcmA, extracellular matrix protein of Dictyostelium alters slug morphology.
    Dev Biol. 1994 Jun;163(2):457-66 PMID: 8200481
  33. An intersection of the cAMP/PKA and two-component signal transduction systems in Dictyostelium.
    EMBO J. 1998 May 15;17(10):2838-45 PMID: 9582277
  34. Alanine tracts: the expanding story of human illness and trinucleotide repeats.
    Trends Genet. 2004 Jan;20(1):51-8 PMID: 14698619
  35. An alternative flavin-dependent mechanism for thymidylate synthesis.
    Science. 2002 Jul 5;297(5578):105-7 PMID: 12029065
  36. Evolution of cell-cell signaling in animals: did late horizontal gene transfer from bacteria have a role?
    Trends Genet. 2004 Jul;20(7):292-9 PMID: 15219393
  37. Genome evolution in yeasts.
    Nature. 2004 Jul 1;430(6995):35-44 PMID: 15229592
  38. Gdt2 regulates the transition of Dictyostelium cells from growth to differentiation.
    BMC Dev Biol. 2004 Jul 5;4:8 PMID: 15236669
  39. The complex repeats of Dictyostelium discoideum.
    Genome Res. 2001 Apr;11(4):585-94 PMID: 11282973
  40. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae.
    Nature. 2004 Apr 8;428(6983):617-24 PMID: 15004568
  41. Developmental regulation of Dictyostelium discoideum actin gene fusions carried on low-copy and high-copy transformation vectors.
    Mol Cell Biol. 1986 Nov;6(11):3973-83 PMID: 3025622
  42. Alignment of BLAST high-scoring segment pairs based on the longest increasing subsequence algorithm.
    Bioinformatics. 2003 Jul 22;19(11):1391-6 PMID: 12874051
  43. Origin and evolution of the slime molds (Mycetozoa)
    Proc Natl Acad Sci U S A. 1997 Oct 28;94(22):12007-12 PMID: 9342353
  44. Whole genome amplification from a single cell: implications for genetic analysis.
    Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5847-51 PMID: 1631067
  45. Genome sequence of the human malaria parasite Plasmodium falciparum.
    Nature. 2002 Oct 3;419(6906):498-511 PMID: 12368864
  46. Expression patterns of cell-type-specific genes in Dictyostelium.
    Mol Biol Cell. 2001 Sep;12(9):2590-600 PMID: 11553701
  47. The membrane glycoprotein gp150 is encoded by the lagC gene and mediates cell-cell adhesion by heterophilic binding during Dictyostelium development.
    Dev Biol. 2000 Nov 15;227(2):734-45 PMID: 11071787
  48. Structure of the amino-terminal domain of Cbl complexed to its binding site on ZAP-70 kinase.
    Nature. 1999 Mar 4;398(6722):84-90 PMID: 10078535
  49. The mitochondrial DNA of the amoeboid protozoon, Acanthamoeba castellanii: complete sequence, gene content and genome organization.
    J Mol Biol. 1995 Feb 3;245(5):522-37 PMID: 7844823
  50. Integrated maps of the chromosomes in Dictyostelium discoideum.
    Genetics. 1995 Sep;141(1):147-57 PMID: 8536963
  51. Sequence and structure of the extrachromosomal palindrome encoding the ribosomal RNA genes in Dictyostelium.
    Nucleic Acids Res. 2003 May 1;31(9):2361-8 PMID: 12711681
  52. Distinct centromere domain structures with separate functions demonstrated in live fission yeast cells.
    J Cell Sci. 2003 Oct 1;116(Pt 19):4035-42 PMID: 12928332
  53. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  54. Eukaryotic signal transduction via histidine-aspartate phosphorelay.
    J Cell Sci. 2000 Sep;113 ( Pt 18):3141-50 PMID: 10954413
  55. ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans.
    J Mol Biol. 1999 Oct 22;293(2):381-99 PMID: 10529352
  56. A computational analysis of whole-genome expression data reveals chromosomal domains of gene expression.
    Nat Genet. 2000 Oct;26(2):183-6 PMID: 11017073
  57. Harnessing the biosynthetic code: combinations, permutations, and mutations.
    Science. 1998 Oct 2;282(5386):63-8 PMID: 9756477
  58. Periodic signaling controlled by an oscillatory circuit that includes protein kinases ERK2 and PKA.
    Science. 2004 May 7;304(5672):875-8 PMID: 15131307
  59. Lack of 5-methylcytosine in Dictyostelium discoideum DNA.
    Biochem J. 1991 Jul 1;277 ( Pt 1):273-5 PMID: 1713034
  60. How cellular slime molds evade nematodes.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):4857-61 PMID: 8643493
  61. Codon--anticodon pairing: the wobble hypothesis.
    J Mol Biol. 1966 Aug;19(2):548-55 PMID: 5969078
  62. The regulation of Dictyostelium development by transmembrane signalling.
    J Eukaryot Microbiol. 1995 May-Jun;42(3):200-5 PMID: 7496377
  63. Evidence that a cell-type-specific efflux pump regulates cell differentiation in Dictyostelium.
    Dev Biol. 2000 Apr 1;220(1):53-61 PMID: 10720430
  64. An efficient algorithm for large-scale detection of protein families.
    Nucleic Acids Res. 2002 Apr 1;30(7):1575-84 PMID: 11917018
  65. Comparative genomics of the eukaryotes.
    Science. 2000 Mar 24;287(5461):2204-15 PMID: 10731134
  66. Fungal ABC transporters and microbial interactions in natural environments.
    Mol Plant Microbe Interact. 2002 Nov;15(11):1165-72 PMID: 12423022
  67. The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba.
    Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1414-9 PMID: 11830664
  68. The cellulose synthase gene of Dictyostelium.
    Proc Natl Acad Sci U S A. 2000 Feb 29;97(5):2391-6 PMID: 10681463
  69. Spore coat formation and timely sporulation depend on cellulose in Dictyostelium.
    Differentiation. 2001 Mar;67(3):72-9 PMID: 11428129
  70. Intracellular growth of Legionella pneumophila in Dictyostelium discoideum, a system for genetic analysis of host-pathogen interactions.
    Infect Immun. 2000 May;68(5):2939-47 PMID: 10768992
  71. Evolutionary implications of the mosaic pyrimidine-biosynthetic pathway in eukaryotes.
    Gene. 2000 Oct 31;257(2):209-22 PMID: 11080587
  72. Horizontal gene transfer in microbial genome evolution.
    Theor Popul Biol. 2002 Jun;61(4):489-95 PMID: 12167368
  73. Physical mapping of genes to specific chromosomes in Dictyostelium discoideum.
    Genomics. 1992 May;13(1):49-61 PMID: 1577493
  74. Dictyostelium transposable element DIRS-1 preferentially inserts into DIRS-1 sequences.
    Mol Cell Biol. 1984 Oct;4(10):2207-13 PMID: 6095047
  75. Consensus phylogeny of Dictyostelium.
    Experientia. 1995 Dec 18;51(12):1110-5 PMID: 8536798
  76. Multiple LTR-retrotransposon families in the asexual yeast Candida albicans.
    Genome Res. 2000 Feb;10(2):174-91 PMID: 10673276
  77. Cellulose-binding modules from extracellular matrix proteins of Dictyostelium discoideum stalk and sheath.
    Eur J Biochem. 2001 Aug;268(15):4334-45 PMID: 11488929
  78. A survey of human disease gene counterparts in the Drosophila genome.
    J Cell Biol. 2000 Jul 24;150(2):F23-30 PMID: 10908582
  79. Changing patterns of gene expression in dictyostelium prestalk cell subtypes recognized by in situ hybridization with genes from microarray analyses.
    Eukaryot Cell. 2003 Jun;2(3):627-37 PMID: 12796308
  80. Adherens junctions and beta-catenin-mediated cell signalling in a non-metazoan organism.
    Nature. 2000 Dec 7;408(6813):727-31 PMID: 11130075
  81. The role of ABC transporters in antibiotic-producing organisms: drug secretion and resistance mechanisms.
    Res Microbiol. 2001 Apr-May;152(3-4):341-50 PMID: 11421281
  82. The role of ABC transporters from Aspergillus nidulans in protection against cytotoxic agents and in antibiotic production.
    Mol Gen Genet. 2000 Jul;263(6):966-77 PMID: 10954082
  83. Structural dynamics of eukaryotic chromosome evolution.
    Science. 2003 Aug 8;301(5634):793-7 PMID: 12907789
  84. The acrasin activity of adenosine-3',5'-cyclic phosphate.
    Proc Natl Acad Sci U S A. 1967 Sep;58(3):1152-4 PMID: 4861307
  85. A cAMP receptor-like G protein-coupled receptor with roles in growth regulation and development.
    Dev Biol. 2004 Jan 15;265(2):433-45 PMID: 14732403
  86. Various bacterial pathogens and symbionts infect the amoeba Dictyostelium discoideum.
    Int J Med Microbiol. 2002 Mar;291(8):615-24 PMID: 12008915
  87. Chemical analysis of stalk components of Dictostelium discoideum.
    Biochim Biophys Acta. 1978 Apr 3;539(4):529-37 PMID: 565220
  88. Outside-in signaling of cellulose synthesis by a spore coat protein in Dictyostelium.
    Eukaryot Cell. 2002 Apr;1(2):281-92 PMID: 12455962
  89. Signal transduction pathways regulated by Rho GTPases in Dictyostelium.
    J Muscle Res Cell Motil. 2002;23(7-8):737-49 PMID: 12952072
  90. Chemical structure of the morphogen differentiation inducing factor from Dictyostelium discoideum.
    Nature. 1987 Aug 27-Sep 2;328(6133):811-4 PMID: 3627228
  91. Initial sequencing and analysis of the human genome.
    Nature. 2001 Feb 15;409(6822):860-921 PMID: 11237011
  92. LagC is required for cell-cell interactions that are essential for cell-type differentiation in Dictyostelium.
    Genes Dev. 1994 Apr 15;8(8):948-58 PMID: 7926779
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
DOI
10.1038/nature03481
Published
2005-05-05
Pages
43-57
Language
English
Region
England
NLM ID
0410462
PMCID
PMC1352341
Subset
IM
Grants
NICHD NIH HHS · R01 HD035925 · United States
Databases
GENBANK
CM000150, CM000151, CM000152, CM000153, CM000154, CM000155
External Links
PubMed source DOI: 10.1038/nature03481 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: [email protected]

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