Hidden diversity and evolutionary trends in malacosporean parasites (Cnidaria: Myxozoa) identified using molecular phylogenetics

International Journal for Parasitology

Volumn 44, Issue 8, 2014, Pages 565-577

  Bartosova Sojkova, Pavla ^a   Hrabcová, Martina ^b   Pecková, Hana ^a   Patra, Sneha ^a,b   Kodádková, Alena ^a,b   Jurajda, Pavel ^c   Tyml, Tomáš ^a,b   Holzer, Astrid Sibylle ^a  

^a INSTITUTE OF PARASITOLOGY   (Czech Republic)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^c INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

Author keywords

Bryozoa; Buddenbrockia; Cryptic; Diversity; Fish; Phylogeny; Tetracapsuloides; Worm

Indexed keywords

ELONGATION FACTOR 2; RIBOSOME DNA; PROTOZOAL DNA; RIBOSOME RNA; RNA 18S; RNA, RIBOSOMAL, 26S;

BIODIVERSITY; BRYOZOAN; FISH; HABITAT SELECTION; HOST PREFERENCE; LIFE CYCLE; PARASITE; PARASITE PREVALENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; SPATIAL DISTRIBUTION;

ARTICLE; BIODIVERSITY; BUDDENBROCKIA; BUDDENBROCKIA PLUMATELLAE; CONTROLLED STUDY; FISH; GEOGRAPHIC DISTRIBUTION; HABITAT SELECTION; HOST PARASITE INTERACTION; LIFE CYCLE STAGE; MARINE ENVIRONMENT; MICROBIAL DIVERSITY; MICROBIAL IDENTIFICATION; MICROBIAL MORPHOLOGY; MIXED INFECTION; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MYXOZOA; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE PREVALENCE; POLYMERASE CHAIN REACTION; SPECIES DISTRIBUTION; SPECIES RICHNESS; TETRACAPSULOIDE; ANIMAL; CHEMISTRY; CLASSIFICATION; CYTOLOGY; DNA SEQUENCE; EVOLUTION; GENETICS; MOLECULAR GENETICS; PARASITOLOGY;

BRYOZOA; BUDDENBROCKIA; BUDDENBROCKIA PLUMATELLAE; CNIDARIA; CYPRINIDAE; MALACOSPOREA; MYXOZOA; TETRACAPSULOIDES;

ANIMALS; BIODIVERSITY; BIOLOGICAL EVOLUTION; DNA, PROTOZOAN; DNA, RIBOSOMAL; FISHES; MOLECULAR SEQUENCE DATA; MYXOZOA; PEPTIDE ELONGATION FACTOR 2; RNA, RIBOSOMAL; RNA, RIBOSOMAL, 18S; SEQUENCE ANALYSIS, DNA;

EID: 84902777482     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2014.04.005     Document Type: Article

References (70)

1. Abd-Elfattah A., Fontes I., Kumar G., Soliman H., Hartikainen H., Okamura B., El-Matbouli M. Vertical transmission of Tetracapsuloides bryosalmonae (Myxozoa), the causative agent of salmonid proliferative kidney disease. Parasitology 2014, 141:482-490.
2. Anderson C.L., Canning E.U., Okamura B. Molecular data implicate bryozoans as hosts for PKX (Phylum Myxozoa) and identify a clade of bryozoan parasites within the Myxozoa. Parasitology 1999, 119:555-561.
3. Balakrishnan R. Species concepts, species boundaries and species identification: a view from the tropics. Syst. Biol. 2005, 54:689-693.
4. Ballard J.W., Whitlock M.C. The incomplete natural history of mitochondria. Mol. Ecol. 2004, 13:729-744.
5. Bartošová P., Fiala I. Molecular evidence for the existence of cryptic species assemblages of several myxosporeans (Myxozoa). Parasitol. Res. 2011, 108:573-583.
6. Bartošová P., Fiala I., Hypša V. Concatenated SSU and LSU rDNA data confirm the main evolutionary trends within myxosporeans (Myxozoa: Myxosporea) and provide an effective tool for their molecular phylogenetics. Mol. Phylogenet. Evol. 2009, 64:81-93.
7. Bartošová P., Fiala I., Jirků M., Cinková M., Caffara M., Fioravanti M.L., Atkinson S.D., Bartholomew J.L., Holzer A.S. Sphaerospora sensu stricto: taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa). Mol. Phylogenet. Evol. 2013, 68:93-105.
8. Boore J.L., Brown W.M. Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol. Biol. Evol. 2000, 17:87-106.
9. Bucke D., Feist S.W., Clifton-Hadley R.S. The occurrence of proliferative kidney disease (PKD) in cultured and wild fish: further investigations. J. Fish Dis. 1991, 14:583-588.
10. Canning E.U., Okamura B. Biodiversity and evolution of the Myxozoa. Adv. Parasitol. 2004, 56:43-131.
11. Canning E.U., Curry A., Hill S.L.L., Okamura B. Ultrastructure of Buddenbrockia allmani n. sp. (Myxozoa, Malacosporea), a parasite of Lophopus crystallinus (Bryozoa, Phylactolaemata). J. Eukaryot. Microbiol. 2007, 54:247-262.
12. Canning E.U., Curry A., Feist S.W., Longshaw M., Okamura B. Tetracapsula bryosalmonae n.sp. for PKX organism, the cause of PKD in salmonid fish. Bull. Eur. Assoc. Fish Pathol. 1999, 19:203-206.
13. Canning E.U., Tops S., Curry A., Wood T.S., Okamura B. Ecology, development and pathogenicity of Buddenbrockia plumatellae Schröder, 1910 (Myxozoa, Malacosporea) (syn. Tetracapsula bryozoides) and establishment of Tetracapsuloides n. gen. for Tetracapsula bryosalmonae. J. Eukaryot. Microbiol. 2002, 49:280-295.
14. Collins A.G. Recent insights into cnidarian phylogeny. Smithson. Contrib. Mar. Sci. 2009, 38:139-149.
15. Evans N.M., Holder M.T., Barbeitos M.S., Okamura B., Cartwright P. The phylogenetic position of Myxozoa: exploring conflicting signals in phylogenomic and ribosomal data sets. Mol. Biol. Evol. 2010, 27:2733-2746.
16. Feist S.W., Longshaw M., Canning E.U., Okamura B. Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae. Dis. Aquat. Organ. 2001, 45:61-68.
17. Ferguson J.A., Atkinson S.D., Whipps C.M., Kent M.L. Molecular and morphological analysis of Myxobolus spp. of salmonid fishes with the description of a new Myxobolus species. J. Parasitol. 2008, 94:1322-1334.
18. Fiala I. The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int. J. Parasitol. 2006, 36:1521-1534.
19. Fiala I., Bartošová P. History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evol. Biol. 2010, 10:228.
20. Froese, R., Pauly, D., 2013. FishBase. World Wide Web electronic publication. <>, version (04/2014). http://www.fishbase.org.
21. Gil R., Silva F.J., Zientz E., Delmotte F., González-Candelas F., Latorre A., Rausell C., Kamerbeek J., Gadau J., Hölldobler B., van Ham R.C., Gross R., Moya A. The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc. Natl. Acad. Sci. USA 2003, 100:9388-9393.
22. Gordon, D.P., 1999. Bryozoan diversity in New Zealand and Australia. In: Ponder, W., Lunney D. (Eds). The Other 99%: The Conservation and Biodiversity of Invertebrates. TRZS NSW, Mosman, New South Wales, pp. 199-204.
23. Grabner D.S., El-Matbouli M. Experimental transmission of malacosporean parasites from bryozoans to common carp (Cyprinus carpio) and minnow (Phoxinus phoxinus). Parasitology 2010, 137:629-639.
24. Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. 41. Nucleic Acids Symp. Ser. No. 41, 95-98.
25. Hartigan A., Fiala I., Dyková I., Jirků M., Okimoto B., Rose K., Phalen D.N., Šlapeta J. A suspected parasite spill-back of two novel Myxidium spp. (Myxosporea) causing disease in Australian endemic frogs found in the invasive Cane Toad. PLoS One 2011, 6:e18871.
26. Hastings A.B. Polyzoa (Bryozoa). 1. Scrupocellariidae, Epistomiidae, Farciminariidae, Bicellariellidae, Aeteidae, Scrupariidae. Discov. Rep. 1943, 32:301-510.
27. Hebert P.D.N., Stoeckle M.Y., Zemlak T.S., Francis C.M. Identification of birds through DNA barcodes. PLoS Biol. 2004, 2:e312.
28. Hedrick R.P., Baxa D.V., De Kinkelin P., Okamura B. Malacosporean-like spores in urine of rainbow trout react with antibody and DNA probes to Tetracapsuloides bryosalmonae. Parasitol. Res. 2004, 92:81-88.
29. Henderson M., Okamura B. The phylogeography of salmonid proliferative kidney disease in Europe and North America. Proc. Biol. Sci. 2004, 271:1729-1736.
30. Hesselberth J.R. Lives that introns lead after splicing. Wiley Interdiscip. Rev. RNA 2013, 4:677-691.
31. Hill S.L.L., Okamura B. Endoparasitism in colonial hosts: patterns and processes. Parasitology 2007, 134:841-852.
32. Holland J.W., Okamura B., Hartikainen H., Secombes C.J. A novel minicollagen gene links cnidarians and myxozoans. Proc. Biol. Sci. 2011, 278:546-553.
33. Holzer A.S., Bartošová P., Pecková H., Tyml T., Atkinson S., Bartholomew J., Sipos D., Eszterbauer E., Dyková I. 'Who's who' in renal sphaerosporids (Bivalvulida: Myxozoa) from common carp, Prussian carp and goldfish - molecular identification of cryptic species, blood stages and new members of Sphaerospora sensu stricto. Parasitology 2013, 140:46-60.
34. Holzer A.S., Stewart S., Tildesley A., Wootten R., Sommerville C. Infection dynamics of two renal myxozoans in hatchery reared fry and juvenile Atlantic cod Gadus morhua L. Parasitology 2010, 137:1501-1513.
35. Jackson J.A. Analysis of parasite host-switching: limitations on the use of phylogenies. Parasitology 1999, 119:S111-S123.
36. Jiménez-Guri E., Okamura B., Holland P.W.H. Origin and evolution of a myxozoan worm. Integr. Comp. Biol. 2007, 47:752-758.
37. Jiménez-Guri E., Philippe H., Okamura B., Holland P.W.H. Buddenbrockia is a cnidarian worm. Science 2007, 317:116-118.
38. Jirků M., Fiala I., Modrý D. Tracing the genus Sphaerospora: rediscovery, redescription and phylogeny of the Sphaerospora ranae (Morelle, 1929) n.comb. (Myxosporea, Sphaerosporidae), with emendation of the genus Sphaerospora. Parasitology 2007, 134:1727-1739.
39. Kallert D.M., Bauer W., Haas W., El-Matbouli M. No shot in the dark: myxozoans chemically detect fresh fish. Int. J. Parasitol. 2011, 41:271-276.
40. Kallert D.M., Borrelli J., Haas W. Biostatic activity of piscine serum and mucus on myxozoan fish infective stages. Fish Shellfish Immunol. 2012, 33:969-976.
41. Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002, 30:3059-3066.
42. Kent M.L., Andree K.B., Bartholomew J.L., El-Matbouli M., Desser S.S., Devlin R.H., Feist S.W., Hedrick R.P., Hoffmann R.W., Khattra J., Hallett S.L., Lester R.J., Longshaw M., Palenzeula O., Siddall M.E., Xiao C. Recent advances in our knowledge of the Myxozoa. J. Eukaryot. Microbiol. 2001, 48:395-413.
43. Kipp R., Bailey S.A., MacIsaac H.J., Ricciardi A. Transoceanic ships as vectors for nonindigenous freshwater bryozoans. Divers. Distrib. 2010, 16:77-83.
44. Marcus E. SÔbre bryozoa do Brasil. Zoologia Univ. Sao Paulo Brazil 1941, 10:3-207.
45. Massard J.A., Geimer G. Global diversity of bryozoans (Bryozoa or Ectoprocta) in freshwater: an update. Bull. Soc. Nat. Luxemb. 2008, 109:139-148.
46. McGurk C., Morris D.J., Adams A. Sequential development of Buddenbrockia plumatellae (Myxozoa: Malacosporea) within Plumatella repens (Bryozoa: Phylactolaemata). Dis. Aquat. Organ. 2006, 73:159-169.
47. Monteiro A.S., Okamura B., Holland P.W.H. Orphan worm finds a home: Buddenbrockia is a myxozoan. Mol. Biol. Evol. 2002, 19:968-971.
48. Morris D.J., Adams A., Feist S.W., McGeorge J., Richards R.H. Immunohistochemical and PCR studies of wild fish for Tetracapsula bryosalmonae (PKX), the causative organism of proliferative kidney disease. J. Fish Dis. 2000, 23:129-135.
49. Morris D.J., Adams A. Proliferative, presaccular stages of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) within the invertebrate host Fredericella sultana (Bryozoa: Phylactolaemata). J. Parasitol. 2006, 92:984-989.
50. Morris D.J., Morris D.C., Adams A. Development and release of a malacosporean (Myxozoa) from Plumatella repens (Bryozoa: Phylactolaemata). Folia Parasitol. 2002, 49:25-34.
51. Okamura B., Anderson C.L., Longshaw M., Feist S.W., Canning E.U. Patterns of occurrence and 18S rDNA sequence variation of PKX (Tetracapsula bryosalmonae), the causative agent of salmonid proliferative kidney disease. J. Parasitol. 2001, 87:379-385.
52. Okamura B., Wood T.S. Bryozoans as hosts for Tetracapsula bryosalmonae, the PKX organism. J. Fish Dis. 2002, 25:469-475.
53. Opravilová V. Freshwater bryozoans (Bryozoa: Phyllactolaemata, Gymnolaemata) of Kokořínsko Protected Landscape Area. Bohemia centralis, Praha 2006, 27:573-576.
54. Putnam N.H., Srivastava M., Hellsten U., Dirks B., Chapman J., Salamov A., Terry A., Shapiro H., Lindquist E., Kapitonov V.V., Jurka J., Genikhovich G., Grigoriev I.V., Lucas S.M., Steele R.E., Finnerty J.R., Technau U., Martindale M.Q., Rokhsar D.S. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 2007, 317:86-94.
55. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
56. Schlegel M., Lom J., Stechmann A., Bernhard D., Leipe D., Dyková I., Sogin M.L. Phylogenetic analysis of complete small subunit ribosomal RNA coding region of Myxidium lieberkuehni: Evidence that Myxozoa are Metazoa and related to the Bilateria. Arch. Protistenkd. 1996, 147:1-9.
57. Schröder O. Buddenbrockia plumatellae, a new Mesozoen species from Plumatella repens L. and Pl. fungosa Pall. Z. Wisseschaft. Zool. 1910, 96:525-537. (In German).
58. Seagrave C.P., Bucke D., Alderman D.J. Ultrastructure of a Haplosporean-like organism: the possible causative agent of proliferative kidney-disease in rainbow trout. J. Fish Biol. 1980, 16:453-459.
59. Seagrave C.P., Bucke D., Hudson E.B., McGregor D. A survey of the prevalence and distribution of proliferative kidney disease (PKD) in England and Wales. J. Fish Dis. 1981, 4:437-439.
60. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
61. Tibayrenc M. The species concept in parasites and other pathogens: a pragmatic approach?. Trends Parasitol. 2006, 22:66-70.
62. Tops S., Curry A., Okamura B. Diversity and systematics of the Malacosporea (Myxozoa). Invertebr. Biol. 2005, 124:285-295.
63. Tops S., Okamura B. Malacosporean parasites (Myxozoa, Malacosporea) of freshwater bryozoans (Bryozoa, Phylactolaemata): a review. Denisia 2005, 16:287-298.
64. Van der Auwera G., Chapelle S., Dewachter R. Structure of the large ribosomal subunit RNA of Phytophthora megasperma, and phylogeny of the oomycetes. FEBS Lett. 1994, 338:133-136.
65. Voronin V.N. PKX like organism in common carp during swimbladder inflammation: further evidence of an association with the myxosporean Sphaerospora renicola. B. Eur. Assoc. Fish Pat. 1993, 13:127-129.
66. Voronin V.N., Chernysheva N.B. An intracellular gill parasite as the possible causative agent of mortality during swim-bladder inflammation in common carp, Cyprinus carpio L. J. Fish Dis. 1993, 16:609-611.
67. Waugh J. DNA barcoding in animal species: progress, potential and pitfalls. BioEssays 2007, 29:188-197.
68. Whipps C.M., Kent M.L. Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J. Eukaryot. Microbiol. 2006, 53:364-373.
69. Wolf K., Markiw M.E. Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 1984, 225:1449-1452.
70. Zhang Z.Q. Animal biodiversity: an introduction to higher-level classification and taxonomic richness. Zootaxa 2011, 3148:7-12.