MicroRNA loci support conspecificity of gyrodactylus salaris and gyrodactylus thymalli (Platyhelminthes: Monogenea)

International Journal for Parasitology

Volumn 44, Issue 11, 2014, Pages 787-793

  Fromm, Bastian ^a   Burow, Susann ^a   Hahn, Christoph ^a   Bachmann, Lutz ^a  

^a UNIVERSITY OF OSLO   (Norway)

Author keywords

Flatworm; Gyrodactylosis; Speciation; Species identification; Synonymization; Taxonomy

Indexed keywords

MICRORNA; HELMINTH RNA;

FLATWORM; GENETIC DIFFERENTIATION; MORPHOLOGY; PATHOGEN; RNA; SPECIATION (CHEMISTRY);

ARTICLE; CLUSTER ANALYSIS; CONTROLLED STUDY; DNA FLANKING REGION; DNA HAIRPIN; GENE AMPLIFICATION; GENE LOCUS; GENE SEQUENCE; GENETIC VARIABILITY; GENOME ANALYSIS; GYRODACTYLUS; GYRODACTYLUS SALARIS; GYRODACTYLUS THYMALLI; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES COMPARISON; SPECIES DIFFERENCE; STRAIN IDENTIFICATION; SYNONYMIZATION; TAXONOMIC IDENTIFICATION; TAXONOMY; ANIMAL; ANIMAL DISPERSAL; GENETICS; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TREMATODE;

NORWAY;

GYRODACTYLUS SALARIS; GYRODACTYLUS THYMALLI; MONOGENEA; PLATYHELMINTHES;

ANIMAL DISTRIBUTION; ANIMALS; GENETIC VARIATION; MICRORNAS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA, HELMINTH; SPECIES SPECIFICITY; TREMATODA;

EID: 84908502706     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2014.05.010     Document Type: Article

References (47)

1. Bakke T.A., Cable J., Harris P.D. The biology of gyrodactylid monogeneans: the "Russian-doll killers". Adv. Parasitol. 2007, 64:161-376.
2. Bakke T.A., Harris P.D., Cable J. Host specificity dynamics: observations on gyrodactylid monogeneans. Int. J. Parasitol. 2002, 32:281-308.
3. Bakke T.A., Jansen P.A., Kennedy C.R. The host specificity of Gyrodactylus salaris Malmberg (Platyhelminthes, Monogenea): susceptibility of Oncovhynchus mykiss (Walbaum) under experimental conditions. J. Fish Biol. 1991, 39:45-57.
4. Bakke T.A., MacKenzie K. Comparative susceptibility of native Scottish and Norwegian stocks of Atlantic salmon, Salmo salar L., to Gyrodactylus salaris Malmberg: laboratory experiments. Fisheries Res. 1993, 17:69-85.
5. Buchmann K., Lindenstrøm T., Nielsen M.E., Bresciani J. Diagnosis and occurrence of ectoparasite infections (Gyrodactylus spp.) in Danish salmonids. Dansk Veterinærtidsskrift 2000, 83:15-19.
6. Cunningham C.O. Species variation within the internal transcribed spacer (ITS) region of Gyrodactylus (Monogenea:Gyrodactylidae) ribosomal RNA genes. J. Parasitol. 1997, 83:215-219.
7. Cunningham C.O., Collins C.M., Malmberg G., Mo T.A. Analysis of ribosomal RNA intergenic spacer (IGS) sequences in species and populations of Gyrodactylus (Platyhelminthes: Monogenea) from salmonid fish in Northern Europe. Dis. Aquatic Org. 2003, 57:237-246.
8. Faria P., Lazarus C., Oosterhout C., Harris P., Cable J. First polymorphic microsatellites for the gyrodactylids (Monogenea), an important group of fish pathogens. Conserv. Genet Resour. 2011, 3:177-180.
9. Fromm B., Harris P.D., Bachmann L. MicroRNA preparations from individual monogenean Gyrodactylus salaris-a comparison of six commercially available totalRNA extraction kits. BMC Res. Notes 2011, 4:217.
10. Fromm B., Worren M.M., Hahn C., Hovig E., Bachmann L. Substantial loss of conserved and gain of novel MicroRNA families in flatworms. Mol. Biol. Evol. 2013, 30:2619-2628.
11. Hahn C., Bachmann L., Chevreux B. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads-a baiting and iterative mapping approach. Nucleic Acids Res. 2013, 41:e129.
12. Hahn C., Fromm B., Bachmann L. Comparative genomics of flatworms (Platyhelminthes) reveals shared genomic features of Ecto- and Endoparastic Neodermata. Genome Biol. Evol. 2014, 6:1105-1117.
13. Hansen H., Bachmann L., Bakke T.A. Mitochondrial DNA variation of Gyrodactylus spp (Monogenea, Gyrodactylidae) populations infecting Atlantic salmon, grayling, and rainbow trout in Norway and Sweden. Int. J. Parasitol. 2003, 33:1471-1478.
14. Hansen H., Bakke T.A., Bachmann L. Mitochondrial haplotype diversity of Gyrodactylus thymalli (Platyhelminthes; Monogenea): extended geographic sampling in United Kingdom, Poland, and Norway reveals further lineages. Parasitol. Res. 2007, 100:1389-1394.
15. Hansen H., Martinsen L., Bakke T.A., Bachmann L. The incongruence of nuclear and mitochondrial DNA variation supports conspecificity of the monogenean parasites Gyrodactylus salaris and G. thymalli. Parasitology 2006, 133:639-650.
16. Harris P.D., Bachmann L., Bakke T.A. Freshwater charr (Salvelinus alpinus) as hosts for Gyrodactylus salaris: implications for management. Vet. Record 2011, 168:161.
17. Hebert P.D.N., Cywinska A., Ball S.L., deWaard J.R. Biological identifications through DNA barcodes. Proc. R. Soc. London. Series B: Biol. Sci. 2003, 270:313-321.
18. Huyse T., Plaisance L., Webster B.L., Mo T.A., Bakke T.A., Bachmann L., Littlewood D.T. The mitochondrial genome of Gyrodactylus salaris (Platyhelminthes: Monogenea), a pathogen of Atlantic salmon (Salmo salar). Parasitology 2007, 134:739-747.
19. Kozomara A., Griffiths-Jones S. MiRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011, 39:D152-D157.
20. Kuusela J., Holopainen R., Meinilä M., Anttila P., Koski P., Zietara M.S., Veselov A., Primmer C.R., Lumme J. Clonal structure of salmon parasite Gyrodactylus salaris on a coevolutionary gradient on fennoscandian salmon (Salmo salar). Ann. Zool. Fenn. 2009, 46:21-33.
21. Kuusela J., Zietara M.S., Lumme J. Hybrid origin of Baltic salmon-specific parasite Gyrodactylus salaris: a model for speciation by host switch for hemiclonal organisms. Mol. Ecol. 2007, 16:5234-5245.
22. Lindenstrom T., Collins C.M., Bresciani J., Cunningham C.O., Buchmann K. Characterization of a Gyrodactylus salaris variant: infection biology, morphology and molecular genetics. Parasitology 2003, 127:165-177.
23. Malmberg G. The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv för zoologi 1970, 23:1-235.
24. Malmberg G., Malmberg M. Species of Gyrodactylus (Platyhelminthes, Monogenea) on salmonids in Sweden. Fish. Res. 1993, 17:59-68.
25. Matejusova I., Gelnar M., McBeath A.J., Collins C.M., Cunningham C.O. Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). Int. J. Parasitol. 2001, 31:738-745.
26. McHugh E.S., Shinn A.P., Kay J.W. Discrimination of the notifiable pathogen Gyrodactylus salaris from G. thymalli (Monogenea) using statistical classifiers applied to morphometric data. Parasitology 2000, 121(Pt 3):315-323.
27. Meinila M., Kuusela J., Zietara M.S., Lumme J. Initial steps of speciation by geographic isolation and host switch in salmonid pathogen Gyrodactylus salaris (Monogenea: Gyrodactylidae). Int. J. Parasitol. 2004, 34:515-526.
28. Olstad K., Robertsen G., Bachmann L., Bakke T.A. Variation in host preference within Gyrodactylus salaris (Monogenea): an experimental approach. Parasitology 2007, 134:589-597.
29. Olstad K., Shinn A.P., Bachmann L., Bakke T.A. Host-based identification is not supported by morphometrics in natural populations of Gyrodactylus salaris and G. thymalli (Platyhelminthes, Monogenea). Parasitology 2007, 134:2041-2052.
30. Plaisance L., Huyse T., Littlewood D.T., Bakke T.A., 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.
31. Robertsen G., Hansen H., Bachmann L., Bakke T.A. Arctic charr (Salvelinus alpinus) is a suitable host for Gyrodactylus salaris (Monogenea, Gyrodactylidae) in Norway. Parasitology 2007, 134:257-267.
32. Shinn A.P., Collins C., Garcia-Vasquez A., Snow M., Matejusova I., Paladini G., Longshaw M., Lindenstrom T., Stone D.M., Turnbull J.F., Picon-Camacho S.M., Rivera C.V., Duguid R.A., Mo T.A., Hansen H., Olstad K., Cable J., Harris P.D., Kerr R., Graham D., Monaghan S.J., Yoon G.H., Buchmann K., Taylor N.G., Bakke T.A., Raynard R., Irving S., Bron J.E. Multi-centre testing and validation of current protocols for the identification of Gyrodactylus salaris (Monogenea). Int. J. Parasitol. 2010, 40:1455-1467.
33. Shinn A.P., Hansen H., Olstad K., Bachmann L., Bakke T.A. The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. thymalli (Monogenea). Folia Parasitol. 2004, 51:239-252.
34. Shinn A.P., Kay J.W., Sommerville C. The use of statistical classifiers for the discrimination of species of the genus Gyrodactylus (Monogenea) parasitizing salmonids. Parasitology 2000, 120(Pt 3):261-269.
35. Soleng A., Bakke T.A. The susceptibility of grayling (Thymallus thymallus) to experimental infections with the monogenean Gyrodactylus salaris. Int. J. Parasitol. 2001, 31:793-797.
36. Sperling E.A., Vinther J., Moy V.N., Wheeler B.M., Semon M., Briggs D.E., Peterson K.J. MicroRNAs resolve an apparent conflict between annelid systematics and their fossil record. Proceedings. Biolo. Sci. R. Soc. 2009, 276:4315-4322.
37. Stentiford G.D., Feist S.W., Stone D.M., Peeler E.J., Bass D. Policy, phylogeny, and the parasite. Trends Parasitol. 2014, 30(6):274-281.
38. Sterud E., Mo T.A., Collins C.M., Cunningham C.O. The use of host specificity, pathogenicity, and molecular markers to differentiate between Gyrodactylus salaris Malmberg, 1957 and G. thymalli Zitnan, 1960 (Monogenea: Gyrodactylidae). Parasitology 2002, 124:203-213.
39. 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.
40. Tarver, J.E., Sperling, E.A., Nailor, A., Heimberg, A.M., Robinson, J.M., King, B.L., Pisani, D., Donoghue, P.C.J., Peterson, K.J., 2013. miRNAs: Small Genes with Big Potential in Metazoan Phylogenetics. Mole. Biol. Evol.
41. Untergasser A., Cutcutache I., Koressaar T., Ye J., Faircloth B.C., Remm M., Rozen S.G. Primer3-new capabilities and interfaces. Nucleic Acids Res. 2012, 40:e115.
42. Wheeler B., Heimberg A., Moy V., Sperling E., Holstein T., Heber S., Peterson K. The deep evolution of metazoan microRNAs. Evol. Dev. 2009, 11:50-68.
43. Winger A.C., Kristoffersen R., Siikavuopio S.I., Knudsen R. Experiments to test if allopatric Salvelinus alpinus are suitable year-round hosts of Gyrodactylus salaris (Monogenea). J. Fish Biol. 2009, 74:1476-1486.
44. Zietara M., Rokicka M., Stojanovski S., Lumme J. Introgression of distant mitochondria into the genome of Gyrodactylus salaris: nuclear and mitochondrial markers are necessary to identify parasite strains. Acta Parasit. 2010, 55:20-28.
45. Zietara M.S., Kuusela J., Lumme J. Escape from an evolutionary dead end: a triploid clone of Gyrodactylus salaris is able to revert to sex and switch host (Platyhelminthes, Monogenea, Gyrodactylidae). Hereditas 2006, 143:84-90.
46. Zietara M.S., Lumme J. Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evol. Int. J. Org. Evol. 2002, 56:2445-2458.
47. Zietara M.S., Lumme J. Comparison of molecular phylogeny and morphological systematics in fish parasite genus Gyrodactylus Nordmann, 1832 (Monogenea, Gyrodactylidae). Zool. Poloniae 2004, 49:5-28.