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Analysis of the Complete Mitochondrial DNA Sequence of the Brachiopod Terebratulina Retusa Places Brachiopoda Within the Protostomes

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Analysis of the Complete Mitochondrial DNA Sequence of the Brachiopod Terebratulina Retusa Places Brachiopoda Within the Protostomes See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/12415870 Analysis of the complete mitochondrial DNA sequence of the brachiopod Terebratulina retusa places Brachiopoda within the protostomes Article in Proceedings of the Royal Society B: Biological Sciences · November 1999 DOI: 10.1098/rspb.1999.0885 · Source: PubMed CITATIONS READS 83 50 2 authors, including: Martin Schlegel University of Leipzig 151 PUBLICATIONS 2,931 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Rare for a reason? Scale-dependence of factors influencing rarity and diversity of xylobiont beetles View project Bat diversity and vertical niche activity in the fluvial flood forest Leipzig View project All content following this page was uploaded by Martin Schlegel on 22 May 2014. The user has requested enhancement of the downloaded file. Analysis of the complete mitochondrial DNA sequence of the brachiopod Terebratulina retusa places Brachiopoda within the protostomes Alexandra Stechmann* and Martin Schlegel UniversitÌt Leipzig, Institut fÏr Zoologie/Spezielle Zoologie,Talstr. 33, 04103 Leipzig, Germany Brachiopod phylogeny is still a controversial subject. Analyses using nuclear 18SrRNA and mitochondrial 12SrDNA sequences place them within the protostomes but some recent interpretations of morphological data support a relationship with deuterostomes. In order to investigate brachiopod a¤nities within the metazoa further,we compared the gene arrangement on the brachiopod mitochondrial genome with several metazoan taxa. The complete (15 451bp) mitochondrial DNA (mtDNA) sequence of the articulate brachiopod Terebratulina retusa was determined from two overlapping long polymerase chain reaction products. All the genes are encoded on the same strand and gene order comparisons showed that only one major rearrangement is required to interconvert the T.retusa and Katharina tunicata (Mollusca: Polyplaco- phora) mitochondrial genomes. The partial mtDNA sequence of the prosobranch mollusc Littorina saxatilis shows complete congruence with the T.retusa gene arrangement with regard to the ribosomal and protein coding genes. This high similarity in gene arrangement is the ¢rst to be reported within the protostomes. Sequence analyses of mitochondrial protein coding genes also support a close relationship of the brachiopod with molluscs and annelids,thus supporting the clade Lophotrochozoa. Though being highly informative,sequence analyses of the mitochondrial protein coding genes failed to resolve the branching order within the lophotrochozoa. Keywords: brachiopod phylogeny; mitochondrial genome; gene order; sequence analysis; Lophotrochozoa share a common ancestry with those fossil Halkieriids, 1. INTRODUCTION implying an ancestral metamerous body plan for both of Brachiopods are a group of marine invertebrates them. Segmentation must then have been secondarily lost comprising around 350 extant and 12 000 fossil species. in brachiopods,but so far there is no clear evidence for Their fossil record dates back to the Lower Cambrian. any segmentation in brachiopods. Together with the Phoronida and Bryozoa they have been With the ¢rst partial brachiopod 18SrRNA (small classi¢ed as Tentaculata (or Lophophorata) because they subunit ribosomal RNA) sequence (Field et al. 1988) used possess a similar suspension feeding apparatus,the lopho- in a molecular analysis of di¡erent metazoan taxa,new phore,which is a horseshoe-shaped structure surrounding emphasis was put on the idea of a protostome a¤nity of the mouth with ciliated tentacles arranged on it (Emig the Lophophorata. Although the method and interpreta- 1976). Because they show both protostome and deutero- tion of this work was criticized,a reanalysis led to the stome features,the Lophophorata have been seen as same result (Lake 1990). Analyses of complete 18SrRNA members of the protostomes,as deuterostomes or as inter- sequences from di¡erent lophophorate taxa demonstrated mediates. More recently the lophophorates have been that all three groups (Phoronida,Bryozoa and Brachio- classi¢ed as deuterostomes on the basis of morphological poda) always cluster within the protostomes along with and larval features (Salvini-Plawen 1982; Emig 1984; molluscs and annelids (Conway-Morris 1995; Halanych et Brusca & Brusca 1990; Eernisse et al. 1992; Backeljau et al. al. 1995; Conway-Morris et al. 1996; Mackey et al.1996; 1993; Nielsen 1995). Evidence from the fossil record gave Cohen & Gawthrop 1997) in a clade named Lophotro- rise to speculations about protostome a¤nities of the chozoa (Halanych et al. 1995). Analyses using partial brachiopods. It has been suggested that the setae of mitochondrial 12SrDNA (small subunit ribosomal RNA) brachiopods are derived from the sclerites of the fossil sequences (Cohen et al. 1998b) con¢rmed the clustering of Halkieriids,which are equivalent to the setae of annelids brachiopods within the protostomes. (Conway-Morris 1995,1998; Conway-Morris & Peel Toaddress the question of brachiopod a¤nity within the 1995). This would mean that brachiopods and annelids metazoa further,we determined the complete mitochon- drial DNA (mtDNA) sequence of Terebratulina retusa.Inthe *Author for correspondence ([email protected]). last few years mitochondrial gene order comparisons have Proc. R. Soc. Lond. B(1999)266,2043^2052 2043 & 1999 The Royal Society Received 28 June 1999 Accepted 23 July 1999 2044 A. Stechmann and M. Schlegel Mitochondrial genome of the brachiopod T. retusa become a promising new tool for investigating phylo- overlapping mode. The 5'- and 3'-ends of this 4.7 kb fragment genetic relationships within the major metazoan groups were identical to the COI and 16SrRNA genes of Terebratulina that (see Boore & Brown 1998; Boore 1999). Several features of had been obtained previously. From this 4.7 kb sequence the mitochondrial genomes support the idea of investigating following two primers were designed to amplify the remaining deep level phylogenies in the metazoa. The gene content of mitochondrial genome: 5'-GTATCGTCGAGGTATCCCTCC- metazoan mtDNA is almost invariant,thus a comparable TA ATCCTAG -3 ' (Tr/LCOX) and 5'- CGA ATA AGGAGATTG - data set is available for all taxa (Moritz et al. 1987; Wolsten- CGACCTCGATGTTGG-3' (Tr/L16S). Both primers were used holme 1992). Stable structural gene rearrangements are in a long PCR with a combination of Taq- and Pwo-poly- rare events due to the fact that functional genomes have to merases (ExpandTM Long Template PCR System,Boehringer, be maintained. It is rather unlikely that two or more taxa Mannheim,Germany) and cycling conditions as recommended will independently converge on the same gene order,thus by the manufacturer. Electrophoretic analysis of the reaction an identical gene order strongly supports a common showed a single product of ca. 11.5 kb length. This product was ancestry of those taxa. Furthermore,reversals of gene digested with the following restriction enzymes to generate over- order are presumed to be unlikely. Thus,there is little lapping fragments: ApaI, BamHI, EcoRI, HindIII, PstI, SacI, danger of homoplastic events hiding the true phylogeny SmaIandXbaI. Double digests were carried out to create (Smith et al. 1993;Boore&Brown1994a,b;Booreet al. smaller fragments if necessary. All restriction fragments were 1995; Lee & Kocher 1995). Studies on the complete cloned into the vectors pUC18,pUC19 (Boehringer,Mannheim, mtDNA of T.retusa have already been carried out byJacobs Germany) and pBluescript SK + (Stratagene,Amsterdam,The et al. (1988) using blot hybridizations to determine the rela- Netherlands). Sequencing was performed as already described tive positions of three genes on the mitochondrial genome. for the 4.7 kb fragment. Cohen et al. (1991) investigated the population genetic structure between Scottish and Canadian Terebratulina (b) Sequence analysis and phylogenetic populations using,among other methods,restriction frag- reconstruction ment length polymorphism (RFLP) analysis of the Gene sequences were identi¢ed as follows. Ribosomal genes mtDNA. However,the complete mtDNA sequence was not were determined by their similarity to corresponding genes in determined in any of these works. alignments with other metazoan mtDNAs. Open reading frames (ORFs) were determined with the program DNASIS for Windows,v. 2 using the genetic code for invertebrate mtDNA. 2. MATERIAL AND METHODS ORFs were identi¢ed according to the sequence similarity of (a) DNA extraction, cloning, polymerase chain their inferred amino-acid sequence in alignments using reaction and sequencing BLASTX (Altschul et al. 1995). In the case of ND4L and ND6 Single specimens of T.retusa (Linne 1758) were collected by (NADH dehydrogenase subunits 4L and 6) and AT P 8 (ATP divers in the Gullmarnfjord near Kristineberg,Sweden. Five synthetase subunit 8),which show only weak amino-acid specimens were shipped alive in cold seawater to Leipzig, sequence similarities,hydropathy pro¢les (Kyte & Doolittle Germany. Total genomic DNA was isolated from the gonads 1982) were calculated and compared with Katharina tunicata and muscles of a single specimen using standard phenol/chloro- (Boore & Brown 1994b), Drosophila yakuba (Clary & Wolsten- form protocols (Sambrook et al. 1989). The entire mtDNA was holme 1985), Lumbricus terrestris (Boore & Brown 1995) and Bala- ampli¢ed by two overlapping polymerase chain reactions noglossus carnosus (Castresana et al. 1998) (data not
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