Home LiteratureArticle Details
PMID: 15342554 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Comparative analysis of apicomplexa and genomic diversity in eukaryotes.

Genome research ·Vol. 14 ·No. 9 ·2004-09-00 ·Pages 1686-95

Templeton TJ, Iyer LM, Anantharaman V, Enomoto S, Abrahante JE, Subramanian GM, Hoffman SL, Abrahamsen MS, Aravind L

Abstract

The apicomplexans Plasmodium and Cryptosporidium have developed distinctive adaptations via lineage-specific gene loss and gene innovation in the process of diverging from a common parasitic ancestor. The two lineages have acquired distinct but overlapping sets of surface protein adhesion domains typical of animal proteins, but in no case do they share multidomain architectures identical to animals. Cryptosporidium, but not Plasmodium, possesses an animal-type O-linked glycosylation pathway, along with >30 predicted surface proteins having mucin-like segments. The two parasites have notable qualitative differences in conserved protein architectures associated with chromatin dynamics and transcription. Cryptosporidium shows considerable reduction in the number of introns and a concomitant loss of spliceosomal machinery components. We also describe additional molecular characteristics distinguishing Apicomplexa from other eukaryotes for which complete genome sequences are available.

MeSH Terms
Animals Apicomplexa/classification,genetics,pathogenicity Cell Adhesion Chromatin Cryptosporidium/classification,genetics,pathogenicity Eukaryotic Cells/physiology Evolution, Molecular Genes, Protozoan Genetic Variation Genome Glycosylation Introns Membrane Proteins/genetics,metabolism Phylogeny Plasmodium/classification,genetics,pathogenicity Signal Transduction Transcription, Genetic/genetics
Chemicals
Chromatin Membrane Proteins
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Templeton Thomas J
Department of Microbiology and Immunology, Weill Medical College and the Program in Immunology and Microbial Pathogenesis, Weill Graduate School of Medical Sciences of Cornell University, New York, New York 10021, USA. [email protected]
Iyer Lakshminarayan M
Anantharaman Vivek
Enomoto Shinichiro
Abrahante Juan E
Subramanian G M
Hoffman Stephen L
Abrahamsen Mitchell S
Aravind L
References (48)
48 references, click to expand
  1. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.
    J Mol Biol. 2001 Jan 19;305(3):567-80 PMID: 11152613
  2. A kingdom-level phylogeny of eukaryotes based on combined protein data.
    Science. 2000 Nov 3;290(5493):972-7 PMID: 11062127
  3. Initial sequencing and analysis of the human genome.
    Nature. 2001 Feb 15;409(6822):860-921 PMID: 11237011
  4. Characterization of the subpellicular network, a filamentous membrane skeletal component in the parasite Toxoplasma gondii.
    Mol Biochem Parasitol. 2001 Jul;115(2):257-68 PMID: 11420112
  5. MEGA2: molecular evolutionary genetics analysis software.
    Bioinformatics. 2001 Dec;17(12):1244-5 PMID: 11751241
  6. The Pfam protein families database.
    Nucleic Acids Res. 2002 Jan 1;30(1):276-80 PMID: 11752314
  7. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing.
    Bioinformatics. 2002 Mar;18(3):502-4 PMID: 11934758
  8. The starch-related R1 protein is an alpha -glucan, water dikinase.
    Proc Natl Acad Sci U S A. 2002 May 14;99(10):7166-71 PMID: 12011472
  9. The role of lineage-specific gene family expansion in the evolution of eukaryotes.
    Genome Res. 2002 Jul;12(7):1048-59 PMID: 12097341
  10. The SWIRM domain: a conserved module found in chromosomal proteins points to novel chromatin-modifying activities.
    Genome Biol. 2002 Jul 24;3(8):RESEARCH0039 PMID: 12186646
  11. Genome sequence of the human malaria parasite Plasmodium falciparum.
    Nature. 2002 Oct 3;419(6906):498-511 PMID: 12368864
  12. MrBayes 3: Bayesian phylogenetic inference under mixed models.
    Bioinformatics. 2003 Aug 12;19(12):1572-4 PMID: 12912839
  13. The eukaryotic DNMT2 genes encode a new class of cytosine-5 DNA methyltransferases.
    J Biol Chem. 2003 Sep 5;278(36):33613-6 PMID: 12819212
  14. Discovery of gene function by expression profiling of the malaria parasite life cycle.
    Science. 2003 Sep 12;301(5639):1503-8 PMID: 12893887
  15. Plasmodium biology: genomic gleanings.
    Cell. 2003 Dec 26;115(7):771-85 PMID: 14697197
  16. The Cryptosporidium oocyst wall protein is a member of a multigene family and has a homolog in Toxoplasma.
    Infect Immun. 2004 Feb;72(2):980-7 PMID: 14742544
  17. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum.
    PLoS Biol. 2003 Oct;1(1):E5 PMID: 12929205
  18. Complete genome sequence of the apicomplexan, Cryptosporidium parvum.
    Science. 2004 Apr 16;304(5669):441-5 PMID: 15044751
  19. A multidomain adhesion protein family expressed in Plasmodium falciparum is essential for transmission to the mosquito.
    J Exp Med. 2004 Jun 7;199(11):1533-44 PMID: 15184503
  20. Plasmodium falciparum: evidence for a DNA methylation pattern.
    Exp Parasitol. 1991 May;72(4):339-44 PMID: 1851101
  21. On the maximum likelihood method in molecular phylogenetics.
    J Mol Evol. 1991 May;32(5):443-5 PMID: 1904100
  22. Evidence for N-linked glycosylation in Toxoplasma gondii.
    Biochem J. 1993 May 1;291 ( Pt 3):713-21 PMID: 8489499
  23. TopPred II: an improved software for membrane protein structure predictions.
    Comput Appl Biosci. 1994 Dec;10(6):685-6 PMID: 7704669
  24. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes.
    Cell. 1995 Jul 14;82(1):101-10 PMID: 7606775
  25. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes.
    Cell. 1995 Jul 14;82(1):77-87 PMID: 7541722
  26. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes.
    Cell. 1995 Jul 14;82(1):89-100 PMID: 7606788
  27. Isolation of multiple sequences from the Plasmodium falciparum genome that encode conserved domains homologous to those in erythrocyte-binding proteins.
    Proc Natl Acad Sci U S A. 1995 Jul 18;92(15):7100-4 PMID: 7624377
  28. Sexual-stage-specific RNA expression of a new Plasmodium falciparum gene detected by in situ hybridisation.
    Mol Biochem Parasitol. 1995 Jun;72(1-2):193-201 PMID: 8538689
  29. Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods.
    Methods Enzymol. 1996;266:418-27 PMID: 8743697
  30. Topology prediction for helical transmembrane proteins at 86% accuracy.
    Protein Sci. 1996 Aug;5(8):1704-18 PMID: 8844859
  31. Bacterial polysaccharide synthesis and gene nomenclature.
    Trends Microbiol. 1996 Dec;4(12):495-503 PMID: 9004408
  32. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites.
    Protein Eng. 1997 Jan;10(1):1-6 PMID: 9051728
  33. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  34. Crystal structure of a Hedgehog autoprocessing domain: homology between Hedgehog and self-splicing proteins.
    Cell. 1997 Oct 3;91(1):85-97 PMID: 9335337
  35. Chromosome 2 sequence of the human malaria parasite Plasmodium falciparum.
    Science. 1998 Nov 6;282(5391):1126-32 PMID: 9804551
  36. Cloning, sequencing, and expression of the gene encoding cyclic 2, 3-diphosphoglycerate synthetase, the key enzyme of cyclic 2, 3-diphosphoglycerate metabolism in Methanothermus fervidus.
    J Bacteriol. 1998 Nov;180(22):5997-6004 PMID: 9811660
  37. Comparison of the complete protein sets of worm and yeast: orthology and divergence.
    Science. 1998 Dec 11;282(5396):2022-8 PMID: 9851918
  38. stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens.
    Mol Biochem Parasitol. 1998 Nov 30;97(1-2):161-76 PMID: 9879895
  39. Profile hidden Markov models.
    Bioinformatics. 1998;14(9):755-63 PMID: 9918945
  40. Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer.
    J Mol Biol. 1999 Jun 18;289(4):729-45 PMID: 10369758
  41. Cryptosporidium is more closely related to the gregarines than to coccidia as shown by phylogenetic analysis of apicomplexan parasites inferred using small-subunit ribosomal RNA gene sequences.
    Parasitol Res. 1999 Nov;85(11):899-904 PMID: 10540950
  42. Origin of multicellular eukaryotes - insights from proteome comparisons.
    Curr Opin Genet Dev. 1999 Dec;9(6):688-94 PMID: 10607613
  43. Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction.
    Mol Biol Evol. 2000 Jan;17(1):189-97 PMID: 10666718
  44. Comparative genome analysis of the pathogenic spirochetes Borrelia burgdorferi and Treponema pallidum.
    Infect Immun. 2000 Mar;68(3):1633-48 PMID: 10678983
  45. What is the phylogenetic position of Cryptosporidium?
    Int J Syst Evol Microbiol. 2000 Jul;50 Pt 4:1673-81 PMID: 10939675
  46. T-Coffee: A novel method for fast and accurate multiple sequence alignment.
    J Mol Biol. 2000 Sep 8;302(1):205-17 PMID: 10964570
  47. Lineage-specific loss and divergence of functionally linked genes in eukaryotes.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11319-24 PMID: 11016957
  48. Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes.
    Nucleic Acids Res. 2001 Feb 1;29(3):850-3 PMID: 11160909
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1088-9051
Published
2004-09-00
Pages
1686-95
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC515313
Subset
IM
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]