title: A novel minicollagen gene links cnidarians and myxozoans.
abstract: Myxozoans are enigmatic endoparasitic organisms sharing morphological features with bilateria, protists and cnidarians. This, coupled with their highly divergent gene sequences, has greatly obscured their phylogenetic affinities. Here we report the sequencing and characterization of a minicollagen homologue (designated Tb-Ncol-1) in the myxozoan Tetracapsuloides bryosalmonae. Minicollagens are phylum-specific genes encoding cnidarian nematocyst proteins. Sequence analysis revealed a cysteine-rich domain (CRD) architecture and genomic organization similar to group 1 minicollagens. Homology modelling predicted similar three-dimensional structures to Hydra CRDs despite deviations from the canonical pattern of group 1 minicollagens. The discovery of this minicollagen gene strongly supports myxozoans as cnidarians that have radiated as endoparasites of freshwater, marine and terrestrial hosts. It also reveals novel protein sequence variation of relevance to understanding the evolution of nematocyst complexity, and indicates a molecular/morphological link between myxozoan polar capsules and cnidarian nematocysts. Our study is the first to illustrate the power of using genes related to a taxon-specific novelty for phylogenetic inference within the Metazoa, and it exemplifies how the evolutionary relationships of other metazoans characterized by extreme sequence divergence could be similarly resolved.
authors.affiliation: Scottish Fish Immunology Research Centre, Aberdeen University, , Aberdeen AB24 2TZ, UK. j.holland@abdn.ac.uk
authors.forename: Jason W
authors.initials: JW
authors.lastname: Holland
authors.forename: Beth
authors.initials: B
authors.lastname: Okamura
authors.forename: Hanna
authors.initials: H
authors.lastname: Hartikainen
authors.forename: Chris J
authors.initials: CJ
authors.lastname: Secombes
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D003063:Cnidaria / Q000145:classification* / Q000235:genetics*; D003094:Collagen / Q000737:chemistry / Q000235:genetics*; D019143:Evolution, Molecular; D008969:Molecular Sequence Data; D055764:Myxozoa / Q000145:classification* / Q000235:genetics* / Q000648:ultrastructure; D058894:Nematocyst / Q000378:metabolism / Q000648:ultrastructure; D010802:Phylogeny; D017510:Protein Folding; D011506:Proteins / Q000235:genetics / Q000378:metabolism
chemical_list: D011506:Proteins; D003094:Collagen
references.citation: Int Rev Cytol. 1978;52:197-276
references.pmid: 418022
references.citation: EMBO J. 2001 Jun 15;20(12):3063-73
references.pmid: 11406583
references.citation: Bioessays. 2007 Nov;29(11):1095-104
references.pmid: 17935152
references.citation: Methods Enzymol. 1990;183:252-78
references.pmid: 2314278
references.citation: Bioinformatics. 2003 Aug 12;19(12):1572-4
references.pmid: 12912839
references.citation: Adv Parasitol. 2004;56:43-131
references.pmid: 14710996
references.citation: Nucleic Acids Res. 1994 Nov 11;22(22):4673-80
references.pmid: 7984417
references.citation: Genome Res. 1998 Sep;8(9):967-74
references.pmid: 9750195
references.citation: Science. 2007 Jul 6;317(5834):86-94
references.pmid: 17615350
references.citation: Nature. 2008 Apr 10;452(7188):745-9
references.pmid: 18322464
references.citation: Science. 1995 Mar 17;267(5204):1641-3
references.pmid: 7886451
references.citation: Bioinformatics. 2002 Sep;18(9):1250-6
references.pmid: 12217917
references.citation: J Biol Chem. 2002 Dec 20;277(51):49200-4
references.pmid: 12368276
references.citation: Science. 2009 Apr 10;324(5924):203-7
references.pmid: 19359577
references.citation: Trends Genet. 2008 Sep;24(9):431-8
references.pmid: 18676050
references.citation: J Mol Biol. 2004 Jul 16;340(4):783-95
references.pmid: 15223320
references.citation: Genome Biol. 2009;10(1):R8
references.pmid: 19161630
references.citation: Science. 1994 Sep 16;265(5179):1719-21
references.pmid: 8085160
references.citation: J Mol Biol. 2008 Feb 29;376(4):1008-20
references.pmid: 18206162
references.citation: Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444-8
references.pmid: 3162770
references.citation: Biosystems. 1992;28(1-3):195-201
references.pmid: 1292663
references.citation: Nature. 1997 May 29;387(6632):489-93
references.pmid: 9168109
references.citation: BMC Evol Biol. 2008 May 09;8:139
references.pmid: 18471296
references.citation: EMBO J. 1986 Apr;5(4):823-6
references.pmid: 3709526
references.citation: Mol Biol Evol. 2010 Dec;27(12):2733-46
references.pmid: 20576761
references.citation: Nature. 1998 Mar 26;392(6674):346-7
references.pmid: 9537319
references.citation: Nucleic Acids Res. 2006 Jan 1;34(Database issue):D257-60
references.pmid: 16381859
references.citation: Biosystems. 1993;29(1):49-58
references.pmid: 8100457
references.citation: Curr Biol. 2007 Jan 23;17(2):173-8
references.pmid: 17240343
references.citation: Comput Appl Biosci. 1994 Apr;10(2):189-91
references.pmid: 8019868
references.citation: Parasitology. 2002 Feb;124(Pt 2):215-23
references.pmid: 11860036
references.citation: Science. 2007 Jul 6;317(5834):116-8
references.pmid: 17615357
references.citation: Curr Biol. 2009 Apr 28;19(8):706-12
references.pmid: 19345102
references.citation: Syst Biol. 2003 Oct;52(5):696-704
references.pmid: 14530136
references.citation: Nucleic Acids Res. 2000 Jan 1;28(1):231-4
references.pmid: 10592234
references.citation: J Mol Biol. 2005 Dec 2;354(3):591-600
references.pmid: 16257007
references.citation: Folia Parasitol (Praha). 2006 Mar;53(1):1-36
references.pmid: 16696428
references.citation: Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
references.pmid: 9254694
references.citation: Proc Biol Sci. 2009 Dec 22;276(1677):4261-70
references.pmid: 19759036
references.citation: BMC Bioinformatics. 2003 Jul 10;4:29
references.pmid: 12854978
references.citation: J Biol Chem. 2004 Jul 16;279(29):30395-401
references.pmid: 15123641
references.citation: Nucleic Acids Res. 2007 Jan;35(Database issue):D298-300
references.pmid: 17135201
references.citation: J Mol Biol. 1990 Oct 5;215(3):403-10
references.pmid: 2231712
references.citation: J Exp Zool B Mol Dev Evol. 2008 Jan 15;310(1):5-14
references.pmid: 17219369