The mitochondrial genome of Paragyrodactylus variegatus (Platyhelminthes: Monogenea): differences in major non-coding region and gene order compared to Gyrodactylus

Particle and Fibre Toxicology

Ping You²  David K Cone³  Stanley D King¹  Fei Ye² 

[1] Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4 J1, Canada;Co-Innovation Center for Qinba regions’ sustainable development, College of Life Science, Shaanxi Normal University, Xi’an 710062, China;Department of Biology, Saint Mary’s University, Halifax, Nova Scotia B3H 3C3, Canada

关键词: China;    Homatula variegata;    Monogenea;    Gyrodactylidae;    Gyrodactylus;    Mitochondrial genome;    Paragyrodactylus variegatus;   

Others  :  1181859
DOI  :  10.1186/1756-3305-7-377

 received in 2014-05-06, accepted in 2014-08-04,  发布年份 2014

【 摘 要 】

Background

Paragyrodactylus Gvosdev and Martechov, 1953, a viviparous genus of ectoparasite within the Gyrodactylidae, contains three nominal species all of which infect Asian river loaches. The group is suspected to be a basal lineage within Gyrodactylus Nordmann, 1832 sensu lato although this remains unclear. Further molecular study, beyond characterization of the standard Internal Transcribed Spacer region, is needed to clarify the evolutionary relationships within the family and the placement of this genus.

Methods

The mitochondrial genome of Paragyrodactylus variegatus You, King, Ye and Cone, 2014 was amplified in six parts from a single worm, sequenced using primer walking, annotated and analyzed using bioinformatic tools.

Results

The mitochondrial genome of P. variegatus is 14,517 bp, containing 12 protein-coding genes (PCGs), 22 transfer RNA (tRNA) genes, two ribosomal RNA (rRNA) genes and a major non-coding region (NCR). The overall A + T content of the mitochondrial genome is 76.3%, which is higher than all reported mitochondrial genomes of monogeneans. All of the 22 tRNAs have the typical cloverleaf secondary structure, except tRNA^Cys, tRNA^Ser1 and tRNA^Ser2 that lack the dihydrouridine (DHU) arm. There are six domains (domain III is absent) and three domains in the inferred secondary structures of the large ribosomal subunit (rrnL) and small ribosomal subunit (rrnS), respectively. The NCR includes six 40 bp tandem repeat units and has the double identical poly-T stretches, stem-loop structure and some surrounding structure elements. The gene order (tRNA^Gln, tRNA^Met and NCR) differs in arrangement compared to the mitochondrial genomes reported from Gyrodactylus spp.

Conclusion

The Duplication and Random Loss Model and Recombination Model together are the most plausible explanations for the variation in gene order. Both morphological characters and characteristics of the mitochondrial genome support Paragyrodactylus as a distinct genus from Gyrodactylus. Considering their specific distribution and known hosts, we believe that Paragyrodactylus is a relict freshwater lineage of viviparous monogenean isolated in the high plateaus of central Asia on closely related river loaches.

【 授权许可】

   
2014 Ye et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

【 参考文献 】

• [1]Johnsen BO, Jensen AJ: The Gyrodactylus story in Norway. Aquaculture 1991, 98:289-302.
• [2]Mo TA, Norheim K: The surveillance and control programme for Gyrodactylus salaris in Atlantic salmon and rainbow trout in Norway. In Annual Report 2004. Oslo, Norway: National Veterinary Institute; 2005:137-139.
• [3]Bakke TA, Cable J, Harris PD: The biology of gyrodactylid monogeneans: the “Russian Doll-killers”. Adv Parasitol 2007, 64:161-376.
• [4]Ziętara MS, Huyse T, Lumme J, Volckaert FA: Deep divergence among subgenera of Gyrodactylus inferred from rDNA ITS region. Parasitology 2002, 124:39-52.
• [5]Matejusová I, Gelnar M, Verneau O, Cunningham CO, Littlewood DTJ: Molecular phylogenetic analysis of the genus Gyrodactylus (Platyhelminthes : Monogenea) inferred from rDNA ITS region: subgenera versus species groups. Parasitology 2003, 127:603-611.
• [6]Vanhove MPM, Tessens B, Schoelinck C, Jondelius U, Littlewood DTJ, Artois T, Huyse T: Problematic barcoding in flatworms: A case-study on monogeneans and rhabdocoels (Platyhelminthes). Zookeys 2013, 365:355-379.
• [7]Bueno-Silva M, Boeger WA: Neotropical Monogenoidea. 58. Three new species of Gyrodactylus (Gyrodactylidae) from Scleromystax spp. (Callichthyidae) and the proposal of COII gene as an additional fragment for barcoding gyrodactylids. Folia Parasitol 2014, 61:213-222.
• [8]You P, King SD, Ye F, Cone DK: Paragyrodactylus variegatus n. sp. (Gyrodactylidae) from Homatula variegata (Dabry de Thiersant, 1874) (Nemacheilidae) in central China. J Parasitol 2014, 100:350-355.
• [9]Kritsky DC, Boeger WA: Phylogeny of the Gyrodactylidae and the phylogenetic status of Gyrodactylus Nordmann, 1832 (Platyhelminthes: Monogenoidea). In Taxonomy, ecology and evolution of metazoan parasites (Livre hommage à Louis Euzet). Edited by Tome II, Combes C, Jourdane J. Perpignan, France: Presses Universitaire Perpignan; 2003:37-58.
• [10]Elson JL, Lightowlers RN: Mitochondrial DNA clonality in the dock: can surveillance swing the case? Trends Genet 2006, 22:603-607.
• [11]Gissi C, Iannelli F, Pesole G: Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity 2008, 101:301-320.
• [12]Lavrov DV, Lang BF: Poriferan mtDNA and animal phylogeny based on mitochondrial gene arrangements. Syst Biol 2005, 54:651-659.
• [13]Boore JL, Brown WM: Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Curr Opin Genet Dev 1998, 8:668-674.
• [14]Staden R, Beal KF, Bonfield JK: The Staden package, 1998. Methods in Molecular Biology. In Bioinformatics Methods and Protocols. Edited by Misener S, Krawetz SA. Totowa, NJ: The Humana Press Inc; 1998:115-130.
• [15]Sakai M, Sakaizumi M: The complete mitochondrial genome of Dugesia japonica (Platyhelminthes; Order Tricladida). Zoolog Sci 2012, 29:672-680.
• [16]Lowe TM, Eddy SR: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964.
• [17]Huyse T, Plaisance L, Webster BL, Mo TA, Bakke TA, Bachmann L, Littlewood DTJ: The mitochondrial genome of Gyrodactylus salaris (Platyhelminthes: Monogenea), a pathogen of Atlantic salmon (Salmo salar). Parasitology 2007, 134:739-747.
• [18]Plaisance L, Huyse T, Littlewood DTJ, Bakke TA, Bachmann L: The complete mitochondrial DNA sequence of the monogenean Gyrodactylus thymalli (Platyhelminthes: Monogenea), a parasite of grayling (Thymallus thymallus). Mol Biochem Parasitol 2007, 154:190-194.
• [19]Benson G: Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999, 27:573-580.
• [20]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [21]Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J: KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics 2006, 4:259-263.
• [22]Le TH, Humair PF, Blair D, Agatsuma T, Littlewood DTJ, McManus DP: Mitochondrial gene content, arrangement and composition compared in African and Asian schistosomes. Mol Biochem Parasitol 2001, 117:61-71.
• [23]Le TH, Blair D, McManus DP: Mitochondrial genomes of parasitic flatworms. Trends Parasitol 2002, 18:206-213.
• [24]Huyse T, Buchmann K, Littlewood DTJ: The mitochondrial genome of Gyrodactylus derjavinoides (Platyhelminthes: Monogenea) - a mitogenomic approach for Gyrodactylus species and strain identification. Gene 2008, 417:27-34.
• [25]Park JK, Kim KH, Kang S, Kim W, Eom KS, Littlewood DTJ: A common origin of complex life cycles in parasitic flatworms: evidence from the complete mitochondrial genome of Microcotyle sebastis (Monogenea: Platyhelminthes). BMC Evol Biol 2007, 7:11. BioMed Central Full Text
• [26]Zhang J, Wu X, Xie M, Li A: The complete mitochondrial genome of Pseudochauhanea macrorchis (Monogenea: Chauhaneidae) revealed a highly repetitive region and a gene rearrangement hot spot in Polyopisthocotylea. Mol Biol Rep 2012, 39:8115-8125.
• [27]Goddard JM, Wolstenholme DR: Origin and direction of replication in mitochondrial DNA molecules from the genus Drosophila. Nucleic Acids Res 1980, 8:741-757.
• [28]Zhang DX, Szymura JM, Hewitt GM: Evolution and structure conservation of the control region of insect mitochondrial DNA. J Mol Evol 1995, 40:382-391.
• [29]Zhang DX, Hewitt GM: Insect mitochondrial control region: a review of its structure, evolution and usefulness in evolutionary studies. Biochem Syst Ecol 1997, 25:99-120.
• [30]Wei SJ, Shi M, Chen XX, Sharkey MJ, Achterberg CV, Ye GY, He JH: New views on strand asymmetry in insect mitochondrial genomes. PLoS One 2010, 5:e12708.
• [31]Moritz C, Brown WM: Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc Natl Acad Sci USA 1987, 84:7183-7187.
• [32]Boore JL: The duplication/random loss model for gene rearrangement exemplified by mitochondrial genomes of deuterostome animals. In Computational biology series. Vol. 1. Dordrecht (The Netherlands). Edited by Sankoff D, Nadeau J. Dordrecht, Boston, and London: Kluwer Academic Publishers; 2000:133-147.
• [33]Lavrov DV, Boore JL, Brown WM: Complete mtDNA sequences of two millipedes suggest a new model for mitochondrial gene rearrangement: duplication and nonrandom loss. Mol Biol Evol 2002, 19:163-169.
• [34]Dowton M, Campbell NJH: Intramitochondrial recombination - is it why some mitochondrial genes sleep around? Trends Ecol Evol 2001, 16:269-271.
• [35]Thyagarajan B, Padua RA, Campbell C: Mammalian mitochondria possess homologous DNA recombination activity. J Biol Chem 1996, 271:27536-27543.
• [36]Lunt DF, Hyman BC: Animal mitochondrial DNA recombination. Nature 1997, 387:247.
• [37]Rawson PD: Nonhomologous recombination between the large unassigned region of the male and female mitochondrial genomes in the mussel, Mytilus trossulus. J Mol Evol 2005, 61:717-732.
• [38]Tsaousis AD, Martin DP, Ladoukakis ED, Posada D, Zouros E: Widespread recombination in published animal mtDNA sequences. Mol Biol Evol 2005, 22:925-933.
• [39]Chen WJ, Bu Y, Carapelli A, Dallai R, Li S, Yin WY, Luan YX: The mitochondrial genome of Sinentomon erythranum (Arthropoda: Hexapoda: Protura): an example of highly divergent evolution. BMC Evol Biol 2011, 11:246. BioMed Central Full Text
• [40]Kurabayashi A, Sumida M, Yonekawa H, Glaw F, Vences M, Hasegawa M: Phylogeny, recombination, and mechanisms of stepwise mitochondrial genome reorganization in mantellid frogs from Madagascar. Mol Biol Evol 2008, 25:874-891.