Skip to main content
SpringerLink
Log in

Small subunit ribosomal RNA sequence links the myxospore stage of Henneguya mississippiensis n. sp. from channel catfish Ictalurus punctatus to an actinospore released by the benthic oligochaete Dero digitata

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

There are more than 200 species of Henneguya described from fish. Of these, only three life cycles have been determined, identifying the actinospore and myxospore stages from their respective hosts. Two of these life cycles involve the channel catfish (Ictalurus punctatus) and the freshwater oligochaete Dero digitata. Herein, we molecularly confirm the life cycle of a previously undescribed Henneguya sp. by matching 18S ribosomal RNA (rRNA) gene sequence of the myxospore stage from channel catfish with the previously described actinospore stage (Aurantiactinomyxon mississippiensis) from D. digitata. Gill tissue from naturally infected channel catfish contained pseudocysts restricted to the apical end of the primary lamellae. Myxospores were morphologically consistent with Henneguya spp. from ictalurid fishes in North America. The spores measured 48.8 ± 4.8 μm (range = 40.7–61.6 μm) in total spore length. The lanceolate spore body was 17.1 ± 1.0 μm (14.4–19.3 μm) in length and 5.0 ± 0.3 μm (4.5–5.5 μm) in width. The two polar capsules were 6.2 ± 0.4 μm (5.8–7.0 μm) long and 5.0 ± 0.3 μm (4.5–5.5 μm) wide. The polar capsule contained eight to nine coils in the polar filament. The two caudal processes were of equal length, measuring 31.0 ± 4.1 μm (22.9–40.6 μm). The 1980-bp 18S rRNA gene sequence obtained from two excised cysts shared 99.4 % similarity (100 % coverage) to the published sequence of A. mississippiensis, an actinospore previously described from D. digitata. The sequence similarity between the myxospore from channel catfish and actinospore from D. digitata suggests that they are conspecific, representing alternate life stages of Henneguya mississippiensis n. sp.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Andree KB, Gresoviac SJ, Hedrick RP (1997) Small subunit ribosomal RNA sequences unite alternate actinosporean and myxosporean stages of Myxobolus cerebralis the causative agent of whirling disease in salmonid fish. J Eukaryot Microbiol 44:208–215

    Article  CAS  PubMed  Google Scholar 

  • Andree KB, El-Matbouli M, Hoffman RW, Hedrick RP (1999) Comparison of 18S and ITS-1 rDNA sequences of selected geographic isolates of Myxobolus cerebralis. Int J Parasitol 29:771–775

    Article  CAS  PubMed  Google Scholar 

  • Atkinson SD, Bartholomew JL (2009) Alternate spore stages of Myxobilatus gasterostei, a myxosporean parasite of three-spined sticklebacks (Gasterosteus aculeatus) and oligochaetes (Nais communis). Parasitol Res 104:1173–1181

    Article  PubMed  Google Scholar 

  • Barassa B, Adriano EA, Cordeiro NS, Arana S, Ceccarelli PS (2012) Morphology and host-parasite interaction of Henneguya azevedoi n. sp., parasite of gills of Leporinus obtusidens from Mogi-Guaçu River, Brazil. Parasitol Res 110:887–894

    Article  PubMed  Google Scholar 

  • Barta JR, Marin DS, Liberator PA, Dshkevicz M, Anderson JW, Feigner SD, Elbrecht A, Perkins-Barrow A, Jenkins MC, Danforth HD, Ruff MD, Profous-Juchelka H (1997) Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol 83:262–271

    Article  CAS  PubMed  Google Scholar 

  • Bartholomew JL, Atkinson SD, Hallett SL (2006) Involvement of Manayunkia speciosa (Annelida: Polychaeta: Sabellidae) in the life cycle of Parvicapsula minibicornis, a myxozoan parasite of Pacific salmon. J Parasitol 92:742–748

    Article  PubMed  Google Scholar 

  • Bartošová P, Fiala I (2011) Molecular evidence for the existence of cryptic species assemblages of several myxosporeans (Myxozoa). Parasitol Res 108:573–583

    Article  PubMed  Google Scholar 

  • Bellerud BL (1993) Etiological and epidemiological factors effecting outbreaks of proliferative gill disease on Mississippi channel catfish farms. Dissertation, College of Veterinary Medicine, Mississippi State University

  • Caffara M, Raimondi E, Florio D, Marcer F, Quaglio F, Fioravanti ML (2009) The life cycle of Myxobolus lentisuturalis (Myxozoa: Myxobolidae), from goldfish (Carassius auratus auratus), involves a Raabeia-type actinospore. Folia Parasitol 56:6–12

    Article  CAS  PubMed  Google Scholar 

  • Easy RH, Johnson SC, Cone DK (2005) Morphological and molecular comparison of Myxobolus procerus (Kudo, 1934) and M. intramusculi n. sp. (Myxozoa) parasitizing muscles of the trout-perch Percopsis omiscomaycus. Syst Parasitol 61:115–122

    Article  CAS  PubMed  Google Scholar 

  • Eiras JC, Adriano EA (2012) A checklist of new species of Henneguya Thélohan, 1892 (Myxozoa: Myxosporea, Myxobolidae) described between 2002 and 2012. Syst Parasitol 83:95–104

    Article  CAS  PubMed  Google Scholar 

  • El-Mansy A, Molnár K (1997a) Development of Myxobolus hungaricus (Myxosporea: Myxobolidae) in oligochaete alternate hosts. Dis Aquat Org 31:227–232

    Article  Google Scholar 

  • El-Mansy A, Molnár K (1997b) Extrapiscine development of Myxobolus drjagini Akhmerov, 1954 (Myxosporea: Myxobolidae) in oligochaete alternative hosts. Acta Vet Hung 45:427–438

    CAS  PubMed  Google Scholar 

  • El-Mansy A, Molnár K, Székely C (1998) Development of Myxobolus portucalensis Saraiva and Molnár, 1990 (Myxosporea: Myxobolidae) in the oligochaete Tubifex tubifex (Müller). Syst Parasitol 41:95–103

    Article  Google Scholar 

  • Eszterbauer E, Székely C, Molnár K, Baska F (2000) Development of Myxobolus bramae (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. J Fish Dis 23:19–25

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Griffin MJ, Pote LM, Wise DJ, Greenway TE, Mauel MJ, Camus AC (2008) A novel Henneguya species from channel catfish described by morphological, histological, and molecular characterization. J Aquat Anim Health 20:127–135

    Article  CAS  PubMed  Google Scholar 

  • Griffin MJ, Wise DJ, Pote LM (2009) Morphology and small-subunit ribosomal DNA sequence of Henneguya adiposa (Myxosporea) from Ictalurus punctatus (Siluriformes). J Parasitol 95:1076–1085

    Article  CAS  PubMed  Google Scholar 

  • Griffin MJ, Quiniou S, Ware C, Bogdanovic L, Soto E (2014) Kudoa thunni from blackfin tuna (Thunnus atlanticus) harvested off the island of St. Kitts, West Indies. J Parasitol 100:110–116

    Article  CAS  PubMed  Google Scholar 

  • Hallett SL, Atkinson SD, Erséus C, El-Matbouli M (2004) Molecular methods clarify morphometric variation in triactinomyxon spores (Myxozoa) released from different oligochaete hosts. Syst Parasitol 57:1–14

    Article  PubMed  Google Scholar 

  • Hanson LA, Lin D, Pote LMW, Shivaji R (2001) Small subunit rRNA gene comparisons of four actinosporean species to establish a polymerase chain reaction test for the causative agent of proliferative gill disease in channel catfish. J Aquat Anim Health 13:117–123

    Article  Google Scholar 

  • Holzer AS, Sommerville C, Wootten R (2004) Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. Int J Parasitol 34:1099–1111

    Article  CAS  PubMed  Google Scholar 

  • Holzer AS, Sommerville C, Wootten R (2006) Molecular identity, phylogeny and life cycle of Chloromyxum schurovi Shul’man & Ieshko 2003. Parasitol Res 99:90–96

    Article  PubMed  Google Scholar 

  • Iwanowicz LR, Iwanowicz DD, Pote LM, Blazer VS, Schill WB (2008) Morphology and 18S rDNA of Henneguya gurlei (Myxosporea) from Ameiurus nebulosus (Siluriformes) in North Carolina. J Parasitol 94:46–57

    Article  CAS  PubMed  Google Scholar 

  • Kallert DM, Eszterbauer E, El-Matbouli M, Erséus C, Haas W (2005) The life cycle of Henneguya nuesslini Schuberg & Schröder, 1905 (Myxozoa) involves a triactinomyxon-type actinospore. J Fish Dis 28:71–79

    Article  CAS  PubMed  Google Scholar 

  • Kent ML, Margolis L, Corliss JO (1994) The demise of a class of protists: taxonomic and nomenclatural revisions proposed for the protist phylum Myxozoa Grassé, 1970. Can J Zool 72:932–937

    Article  Google Scholar 

  • Kent ML, Khattra J, Hervio DML, Devlin RH (1998) Ribosomal DNA sequence analysis of isolates of the PKX myxosporean and their relationship to members of the genus Sphaerospora. J Aquat Anim Health 10:12–21

    Article  Google Scholar 

  • Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJG, Longshaw M, Palenzeula O, Siddall ME, Xiao C (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395–413

    Article  CAS  PubMed  Google Scholar 

  • Køie M, Karlsbakk E, Nylund A (2008) The marine herring myxozoan Ceratomyxa auerbachi (Myxozoa: Ceratomyxidae) uses Chone infundibuliformis (Annelida: Polychaeta: Sabellidae) as invertebrate host. Folia Parasitol 55:100–104

    Article  PubMed  Google Scholar 

  • Kudo RR (1920) Studies on Myxosporidia: a synopsis of genera and species of Myxosporidia. Ill Biol Monogr 5:1–265

    Google Scholar 

  • Kudo R (1929) Histozoic myxosporidia found in freshwater fishes in Illinois, USA. Arch Protistenkd 65:364–378

    Google Scholar 

  • Lin D, Hanson LA, Pote LM (1999) Small subunit ribosomal RNA sequence of Henneguya exilis (Class Myxosporea) identifies the actinosporean stage from an oligochaete host. J Eukaryot Microbiol 46:66–68

    Article  CAS  PubMed  Google Scholar 

  • Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36

    Article  PubMed  Google Scholar 

  • Markiw ME, Wolf K (1983) Myxosoma cerebralis (Myxozoa: Myxosporea) etiologic agent of salmonid whirling disease requires tubificid worm (Annelida: Oligochaeta) in its life cycle. J Protozool 30:561–564

    Article  Google Scholar 

  • Meglitsch PA (1937) On some new and known Myxosporidia of the fishes of Illinois. J Parasitol 23:467–477

    Article  Google Scholar 

  • Minchew CD (1977) Five new species of Henneguya (Protozoa: Myxosporidia) from ictalurid fishes. J Protozool 24:213–220

    Article  CAS  PubMed  Google Scholar 

  • Mischke CC, Griffin MJ (2011) Laboratory mass culture of the freshwater oligochaete Dero digitata. N Am J Aquac 73:13–16

    Google Scholar 

  • Molnár K (2002) Site preference of fish myxosporeans in the gill. Dis Aquat Org 48:197–207

    Article  PubMed  Google Scholar 

  • Molnár K, El-Mansy A, Székely C, Baska F (1999) Development of Myxobolus dispar (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. Folia Parasitol 46:15–21

    Google Scholar 

  • Molnar K, Székely C, Mohamed K, Shaharom-Harrison F (2006) Myxozoan pathogens in cultured Malaysian fishes. II. Myxozoan infections of redtail catfish Hemibagrus nemurus in freshwater cage cultures. Dis Aquat Org 68:219–226

    Article  CAS  PubMed  Google Scholar 

  • Molnár K, Cech G, Székely C (2011) Histological and molecular studies of species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea) in the gills of Abramis, Blicca and Vimba spp. (Cyprinidae), with the redescription of M. macrocapsularis Reuss, 1906 and M. bliccae Donec & Tozyyakova, 1984. Syst Parasitol 79:109–121

    Article  PubMed  Google Scholar 

  • Nigrelli RF, Smith GM (1940) A papillary cystic disease affecting the barbels of Ameiurus nebulosus (la Sueur), caused by the myxosporidian Henneguya ameiurus sp. nov. Zoology 25:89–94

    Google Scholar 

  • Pote LM, Hanson LA, Shivaji R (2000) Small subunit ribosomal RNA sequences link the cause of proliferative gill disease in channel catfish to Henneguya n. sp. (Myxozoa: Myxosporea). J Aquat Anim Health 12:230–240

    Article  Google Scholar 

  • Rosser TG, Griffin MJ, Quiniou SM, Greenway TE, Khoo LH, Wise DJ, Pote LM (2014a) Molecular and morphological characterization of myxozoan actinospore types from a commercial catfish pond in the Mississippi Delta. J Parasitol 100(6):828–839

    Article  PubMed  Google Scholar 

  • Rosser TG, Griffin MJ, Quiniou SMA, Khoo LH, Pote LM (2014b) 18S rRNA gene sequencing identifies a novel species of Henneguya parasitizing the gills of the channel catfish (Ictaluridae). Parasitol Res 113:4651–4658

    Article  PubMed  Google Scholar 

  • Scott SJ, Griffin MJ, Quiniou S, Khoo L, Bollinger TK (2014) Myxobolus neurophilus Guilford (Myxosporea: Myxobolidae): a common parasite infecting yellow perch Perca flavacens (Mitchell, 1814) in Saskatchewan, Canada. J Fish Dis. doi:10.1111/jfd.12242

    PubMed  Google Scholar 

  • Székely C, El-Mansy A, Molnár K, Baska F (1998) Development of Thelohanellus hovorkai and Thelohanellus nikolskii (Myxosporea: Myxozoa) in oligochaete alternate hosts. Fish Pathol 33:107–114

    Article  Google Scholar 

  • Székely C, Molnár K, Eszterbauer E, Baska F (1999) Experimental detection of the actinospores of Myxobolus pseudodispar (Myxosporea: Myxobolidae) in oligochaete alternate hosts. Dis Aquat Org 38:219–224

    Article  PubMed  Google Scholar 

  • Székely C, Molnár K, Rácz O (2001) Complete developmental cycle of Myxobolus pseudodispar (Gorbunova) (Myxosporea: Myxobolidae). J Fish Dis 24:461–468

    Article  Google Scholar 

  • Székely C, Rácz O, Molnár K, Eszterbauer E (2002) Development of Myxobolus macrocapsularis (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. Dis Aquat Org 48:117–123

    Article  PubMed  Google Scholar 

  • Székely C, Hallett SL, Atkinson SD, Molnár K (2009) Complete life cycle of Myxobolus rotundus (Myxosporea: Myxobolidae), a gill myxozoan of common bream Abramis brama. Dis Aquat Org 85:147–155

    Article  PubMed  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whipps CM, Kent ML (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J Eukaryot Microbiol 53:364–373

  • Yokoyama H (1997) Transmission of Thelohanellus hovorkai Achmerov, 1960 (Myxosporea: Myxozoa) to common carp Cyprinus carpio through the alternate oligochaete host. Syst Parasitol 36:79–84

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the Mississippi State University College of Veterinary Medicine, the Mississippi Agricultural and Forestry Experiment Station, and the USDAARS Catfish Health Initiative (CRIS 6402-31320-002-02). This is MAFES publication number: J-12614.

Author information

Authors and Affiliations

  1. Department of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS, 39762, USA

    Thomas G. Rosser & Linda M. Pote

  2. Department of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS, 39762, USA

    Matt J. Griffin & Lester H. Khoo

  3. Thad Cochran National Warmwater Aquaculture Center, Aquatic Research and Diagnostic Laboratory, Delta Research and Extension Center, Mississippi State University, Stoneville, Washington County, MS, 38776, USA

    Matt J. Griffin, Lester H. Khoo, Terrence E. Greenway & David J. Wise

  4. Warmwater Aquaculture Research Unit, Agricultural Research Service, United States Department of Agriculture, Stoneville, MS, 38776, USA

    Sylvie M. A. Quiniou

  5. Mississippi Agricultural and Forestry Experiment Station, Mississippi State University, Mississippi State, MS, 39762, USA

    Terrence E. Greenway & David J. Wise

Authors
  1. Thomas G. Rosser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matt J. Griffin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sylvie M. A. Quiniou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lester H. Khoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Terrence E. Greenway
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. David J. Wise
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Linda M. Pote
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Linda M. Pote.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rosser, T.G., Griffin, M.J., Quiniou, S.M.A. et al. Small subunit ribosomal RNA sequence links the myxospore stage of Henneguya mississippiensis n. sp. from channel catfish Ictalurus punctatus to an actinospore released by the benthic oligochaete Dero digitata . Parasitol Res 114, 1595–1602 (2015). https://doi.org/10.1007/s00436-015-4345-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4345-y

Keywords

Search

Navigation