Skip to main content
SpringerLink
Log in

New data on Henneguya postexilis Minchew, 1977, a parasite of channel catfish Ictalurus punctatus, with notes on resolution of molecular markers for myxozoan phylogeny

  • Published:
Systematic Parasitology Aims and scope Submit manuscript

Abstract

Previous morphological and histological data are supplemented with molecular and ultrastructural data for a Henneguya sp. isolated from farm-raised channel catfish Ictalurus punctatus in Mississippi, USA. Myxospores were cryptic, encapsulated within a thin layer of epithelium in the gill lamellae with spore measurements consistent with the original description of Henneguya postexilis Minchew, 1977. Myxospores were 42.7–49.1 µm in total length with spore bodies 12.1–17.2 × 3.6–4.8 × 2.9–3 µm. Polar capsules were of unequal length, with the longer capsule being 4.4–6.7 × 1.1–1.6 µm and the shorter capsule being 4.4–6.4 × 1.1–1.6 µm. Polar tubules had 6–8 turns. Caudal processes were 25.7–38.1 µm in length. Spores were encapsulated in a thin layer of epithelium in the gill lamellae. Molecular data from the most commonly used markers for myxozoan identification and phylogeny, partial 18S small subunit ribosomal gene (SSU), partial 28S large subunit ribosomal gene (LSU), and elongation factor 2 (EF2) were generated for H. postexilis. Additionally, novel data for LSU and EF2 were generated for archived myxozoan specimens from farm-raised catfish (H. mississippiensis, H. ictaluri, H. exilis, H. adiposa, H. sutherlandi, H. bulbosus, Unicauda fimbrethilae), as well as archived specimens from wild fish (H. laseeae [from Pylodictis olivaris], Hennegoides flockae [from Aphredoderus sayanus], Myxobolus cloutmani [from Cycleptus elongatus]. These include the first EF2 sequence data for the genera Hennegoides and Unicauda. Phylogenetic analyses using these data placed H. postexilis in well supported clades with other ictalurid-infecting Henneguya species. Phylogenetic signal assessments on these analyses suggest that while SSU provided the greatest phylogenetic signal, LSU yielded comparable signal, supporting previous work implying this region may be underutilised in reconstructing myxobolid phylogenies.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Abrunhosa, J., Sindeaux-Neto, J. L., Hamoy, I., & Matos, E. R. (2018). A new species of Myxosporea, Henneguya quelen, from silver catfish Rhamdia quelen (Siluriforme: Pimelodidae) in the Amazonian region. Parasitology Research, 117, 3809–3820.

    PubMed  Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.

    CAS  PubMed  Google Scholar 

  • Altekar, G. S., Dwarkadas, S., Huelsenbeck, J. P., & Ronquist, F. (2004). Parallel Metropolis-coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics, 20, 407–415.

    CAS  PubMed  Google Scholar 

  • Angosti, D., Jacobs, D., & DeSalle, R. (1996). On combining protein sequences and nucleic acid sequences in phylogenetic analysis: The homeobox protein case. Cladistics, 12, 65–82.

    Google Scholar 

  • Atkinson, S. D., Bartošová-Sojková, P., Whipps, C. M., & Bartholomew, J. L. (2015). Approaches for characterizing myxozoan species. In B. Okamura, A. Gruhl, & J. L. Bartholomew (Eds.), Myxozoan evolution, ecology and development (pp. 111–123). Switzerland: Springer.

    Google Scholar 

  • Barta, J. R., Martin, D. S., Liberator, P. A., Dashkevicz, M., Anderson, J. W., Feigner, S. D., Elbrecht, A., Perkin-Barrow, A., Jenkins, M. C., Danforth, H. D., Ruff, M. F., & Profous-Juchelka, H. (1997). Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. Journal of Parasitology, 83, 262–271.

    CAS  PubMed  Google Scholar 

  • Bartošová, P. (2010). Phylogenetic analyses of myxosporeans based on the molecular data. (PhD Thesis). Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Department of Protistology.

  • Bartošová, P., Fiala, I., & Hypša, V. (2009). Concatenated SSU and LSU rDNA data confirm the main evolutionary trends within myxosporeans (Myxozoa: Myxosporea) and provide an effective tool for their molecular phylogenetics. Molecular Phylogenetics and Evolution, 53, 81–93.

    PubMed  Google Scholar 

  • Bartošová, P., Fiala, I., Jirků, M., Cinková, M., Caffara, M., Fioravanti, M. L., Atkinson, S. D., & Bartholomew, J. L. (2013). Sphaerospora sensu stricto: Taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa). Molecular Phylogenetics and Evolution, 68, 93–105.

    PubMed  Google Scholar 

  • Belem, A. M. G., & Pote, L. M. (2001). Portals of entry and systemic localization of proliferative gill disease organisms in channel catfish Ictalurus punctatus. Diseases of Aquatic Organisms, 48, 37–42.

  • Bellerud, B. L. (1993). Etiological and epidemiological factors effecting outbreaks of proliferative gill disease on Mississippi channel catfish farms. (PhD Dissertation). Mississippi State University, Mississippi State, Mississippi, USA.

  • Blasco-Costa, I., Cutmore, S. C., Miller, T. L., & Nolan, M. J. (2016). Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Systematic Parasitology, 93, 295–306.

    PubMed  Google Scholar 

  • Briosio-Aguilar, R., Varela, M. G., Mena, D. I. H., Rubio-Godoy, M., & de León, G. P.-P. (2018). Morphological and molecular characterization of an enigmatic clinostomid trematode (Digenea: Clinostomidae) parasitic as metacercariae in the body cavity of freshwater fishes (Cichlidae) across Middle America. Journal of Helminthology, 93(4), 1–14.

    Google Scholar 

  • CABI. (2020). Ictalurus punctatus [Original article by Carole Engle]. In Invasive species compendium. Wallingford, UK: CAB International.

  • Carriero, M. M., Adriano, E. A., Silva, M. R. M., Ceccarelli, P. S., & Maia, A. A. M. (2013). Molecular phylogeny of the Myxobolus and Henneguya genera with several new South American species. PLoS ONE, 8(9), e73713. https://doi.org/10.1371/journal.pone.0073713.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciudice, G. M., Bayne, D. R., & Pompa, T. J. (2004) Threadfin shad Dorosoma petenense effects on water quality, phytoplankton, and channel catfish production in ponds. Journal of the World Aquaculture Society, 35(3), 345–356.

    Google Scholar 

  • Deng, W., Xiao, Y. H., Cao, K. D., Ma, L. (2010). 我国蛔鱼产业的发展、挑战及对策. 中国水产 [Development, challenges and strategies of channel catfish industry. China Fisheries], 12, 11–13. (In Chinese).

  • Eiras, J. C. (2002). Synopsis of the species of the genus Henneguya Thélohan, 1892 (Myxozoa: Myxosporea: Myxoblidae). Systematic Parasitology, 52, 43–54.

    CAS  PubMed  Google Scholar 

  • Eiras, J. C., & Adriano, E. A. (2012). A checklist of new species of Henneguya Thélohan, 1892 (Myxozoa: Myxosporea, Myxobolidae) described between 2002 and 2012. Systematic Parasitology, 83, 95–104.

    CAS  PubMed  Google Scholar 

  • Fiala, I. (2006). The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology, 36, 1521–1534.

    CAS  PubMed  Google Scholar 

  • Fiala, I., & Bartošová, P. (2010). History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evolutionary Biology, 10, 228. http://www.biomedcentral.com/1471-2148/10/228.

  • Fiala, I., Hlavničková, M., Kodáková, A., Freeman, M. A., Bartošová-Sojková, P., & Atkinson, S. D. (2015). Evolutionary origin of Ceratonova shasta and phylogeny of the marine myxosporean lineage. Molecular Phylogenetics and Evolution, 86, 75–89.

    PubMed  Google Scholar 

  • Freudenstein, J. V., Pickett, K. M., Simmons, M. P., & Wenzel, J. W. (2003). From basepairs to birdsongs: phylogenetic data in the age of genomics. Cladistics, 19(4), 333–347.

    Google Scholar 

  • Goldman, N., Yang, Z. (1994). A codon-based model of nucleotide substitution for protein-coding DNA sequences. Molecular Biology and Evolution, 11, 725–736.

    CAS  PubMed  Google Scholar 

  • Griffin, M. 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. Journal of Parasitology, 100(1), 110–116.

  • Griffin, M. J., Wise, D. J., & Pote, L. M. (2009). Morphology and small-subunit ribosomal DNA sequence of Henneguya adiposa (Myxosporea) from Ictalurus punctatus (Siluriformes). Journal of Parasitology, 95, 1076–1085.

    CAS  PubMed  Google Scholar 

  • Griffin, M. J., Camus, A. C., Wise, D. J., Greenway, T. E., Mauel, M. J., & Pote, L. M. (2010). Variation in susceptibility to Henneguya ictaluri infection by two species of catfish and their hybrid cross. Journal of Aquatic Animal Health, 22, 21–35.

    PubMed  Google Scholar 

  • Griffin, M. J., Ware, C., Rosser, T. G., Woodyard, E. T., Mischke, C. C., Byars, T. S., & Wise, D. J. (2020). Monoculture of ♀ channel (Ictalurus punctatus) × ♂ blue (I. furcatus) hybrid catfish mitigates proliferative gill disease caused by Henneguya ictaluri (Cnidaria: Myxobolidae) in catfish aquaculture ponds. Journal of the World Aquaculture Society, 51, 729–739.

    CAS  Google Scholar 

  • Hanson, L. A., Lin, D., Pote, L. M. W., & 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. Journal of Aquatic Animal Health, 13, 117–123.

    Google Scholar 

  • Hashimoto, T., Nakamura, Y., Kamaishi, T., Nakamura, F., Adachi, J., Okamoto, K., & Hasegawa, M. (1995). Phylogenetic place of mitochondria-lacking protozoan, Giardia lamblia, inferred from amino acid sequences of Elongation Factor 2. Molecular Biology and Evolution, 12(5), 782–793.

    CAS  PubMed  Google Scholar 

  • Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A., & Jermiin, L. S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kress, W. J., & Erickson, D. L. (2008). DNA barcodes: Genes, genomics, and bioinformatics. PNAS, 105(8), 2761–2762.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ksepka, S., Whelan, N., Whipps, C. M., & Bullard, S. A. (2020). A new species of Thelohanellus Kudo, 1933 (Myxozoa: Bivalvulida) infecting skeletal muscle of blacktail shiner, Cyprinella venusta Girard, 1856 (Cypriniformes: Cyprinidae) in the Chattahoochee River Basin, Georgia. Journal of Parasitology, 106, 350–359.

    PubMed  Google Scholar 

  • Kück, P., Meid, S. A., Groß, C., Wägele, J. W., & Misof, B. (2014). AliGROVE – visualization of heterogeneous sequence divergence within multiple sequence alignments and detection of inflated branch support. BMC Bioinformatics, 15, 294. https://doi.org/10.1186/1471-2105-15-294.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kück, P. (2020). Alicut. Retrieved August 31, 2020, from https://www.zfmk.de/en/research/research-centres-and-groups/utilities.

  • Leis, E. M., Rosser, T. G., Baumgartner, W. A., & Griffin, M. J. (2017). Henneguya laseeae n. sp. from flathead catfish (Pylodictus olivaris) in the upper Mississippi River. Parasitology Research, 116, 81–89.

    PubMed  Google Scholar 

  • Leis, E. M., Rosser, T. G., Baumgartner, W. A., & Griffin, M. J. (2019). Two novel myxozoans from pirate perch Aphredoderus sayanus (Gilliams, 1824) in the upper Mississippi River, including the first North American species of Hennegoides Lom, Tonguthai, & Dyková, 1991. Journal of Parasitology, 105(6), 918–927.

    Google Scholar 

  • Li, D.P., Xie, C. X., He, X. G., Qi, C. L., & Liang, X. (2018). Channel Catfish Aquaculture. In J. F. Gui, Q. S. Tang, Z. J. Li, J. S. Liu, & S. S. de Silva (Eds.), Aquaculture in China: Success stories and modern trends (pp. 393–403).

  • Lin, D., Hanson, L. A., & Pote, L. M. (1999). Small subunit ribosomal RNA sequence of Henneguya exilis (Class Myxosporea) identifies the actinosporean stage from an oligochaete host. Journal of Eukaryotic Microbiology, 46, 66–68.

    CAS  PubMed  Google Scholar 

  • Lisnerová, M., Fiala, I., Cantatore, D., Irigoitia, M., Timi, J., Pecková, H., Bartošová-Sojková, P., Sandoval, C. M., Luer, C., Morris, J., & Holzer, A. S. (2020). Mechanisms and drivers for the establishment of life cycle complexity in myxozoan parasites. Biology, 9(1), 10. https://doi.org/10.3390/biology9010010.

    Article  PubMed Central  Google Scholar 

  • Liu, Y., Lövy, A., Gu, Z. M., & Fiala, I. (2019). Phylogeny of Myxobolidae (Myxozoa) and the evolution of myxospore appendages in the Myxobolus clade. International Journal for Parasitology, 49(7), 523–530.

    PubMed  Google Scholar 

  • Lom, J., & Arthur, J. R. (1989). A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases, 12, 151–156.

    Google Scholar 

  • Löytynoja, A. (2013). Phylogeny-aware alignment with PRANK. In Russell, D. J. (Eds.), Multiple sequence alignment methods (pp. 155–170).

  • Löytynoja, A., & Goldman, N. (2008). A model of evolution and structure for multiple sequence alignment. Philosophical Transactions of the Royal Society B, 363, 3913-3919.

    Google Scholar 

  • López-Giráldez, F., & Townsend, J. P. (2011). PhyDesign: an online application for profiling phylogenetic informativeness. BMC Evolutionary Biology, 11, 152. https://doi.org/https://doi.org/10.1186/1471-2148-11-152.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mayrose, I., Graur, D., Ben-Tal, N., & Pupko, T. (2004). Comparison of site-specific rate-inference methods for protein sequences: empirical Bayesian methods are superior. Molecular Biology and Evolution, 21(9), 1781–1791.

    CAS  PubMed  Google Scholar 

  • Minchew, C. D. (1977). Five new species of Henneguya (Protozoa: Myxosporida) from ictalurid fishes. Journal of Protozoology, 24(2), 213–220.

    CAS  PubMed  Google Scholar 

  • Maddison, W. P., & Maddison, D. R. (2018). Mesquite: a modular system for evolutionary analysis. Version 3.61. Retrieved August 31, 2020, from http://www.mesquiteproject.org.

  • Mathews, P. D., Maia, A. A. M., & Adriano, E. A. (2016). Henneguya melini n. sp. (Myxosporea: Myxobolidae), a parasite of Corydoras melini (Teleostei: Siluriformes) in the Amazon region: morphological and ultrastructural aspects. Parasitology Research, 115, 3599–3604.

    PubMed  Google Scholar 

  • Mathews, P. D., Mertins, O., Espinoza, L., Milanin, T., Alama-Bermejo, G., Audebert, F., & Morandini, A. C. (2020). Taxonomy and 18S rDNA-based phylogeny of Henneguya multiradiatus n. sp. (Cnidaria: Myxobolidae) a parasite of Brochis multiradiatus from Peruvian Amazon. Microbial Pathogenesis, 147, 104372. https://doi.org/10.1016/j.micpath.2020.104372

    Article  CAS  PubMed  Google Scholar 

  • McAllister, C. T., Woodyard, E. T., Rosser, T. G., Fayton, T. J., Griffin, M. J., & Robinson, H. W. (2021). A new species of Myxobolus (Cnidaria: Myxosporea: Myxobolidae) from the blue sucker, Cycleptus elongatus Lesueur (Cypriniformes: Catostomidae: Cycleptinae), from Arkansas. Journal of Parasitology, 107, 582–592.

    PubMed  Google Scholar 

  • Mischke, C. C., Griffin, M. J., Greenway, T. E., & Wise, D. (2013). Effects of mosquitofish Gambusia affinis, on channel catfish, Ictalurus punctatus, production ponds. Journal of the World Aquaculture Society, 44(2), 288–292.

    Google Scholar 

  • Mischke, C. C., Griffin, M. J., Wise, D. J., & Greenway, T. E. (2016). Effects of co-stocking smallmouth buffalo, Ictionbus bubalus, with channel catfish, Ictalurus punctatus. Journal of the World Aquaculture Society, 47(2), 212–219.

    Google Scholar 

  • Misof, B., & Misof, K. (2009). A Monte Carlo approach successfully identifies randomness in multiple sequence alignments: a more objective means of data exclusion. Systematic Biology, 58, 21–34.

    CAS  PubMed  Google Scholar 

  • Naldoni, J., Maia, A. A. M., da Silva, M. R. M., & Adriano, E. A. (2014). Henneguya cuniculator sp. nov., a parasite of spotted sorubim Pseudoplatystoma corruscans in the São Francisco Basin, Brazil. Diseases of Aquatic Organisms, 107, 211–221.

    PubMed  Google Scholar 

  • Negrelli, D. C., Vieira, D. H. M. D., Tagliavini, V. P., Abdallah, V. D., & de Azevedo, R. K. (2019). Molecular and morphological analysis of Henneguya jundiai n. sp. (Cnidaria: Myxosporea), a new parasite of the gills of Rhamdia quelen in Brazil. Acta Tropica, 197, 105053. https://doi.org/10.1016/j.actatropica.2019.105053.

    Article  CAS  PubMed  Google Scholar 

  • Nie, R. E., Breeschoten T., Timmermans, M. J. T. N., Nadein, K., Xue, H. J., Bai, M., Huang, Y., Yang, X. K., & Vogler, A. P. (2018). The phylogeny of Galerucinae (Coleoptera: Chrysomelidae) and the performance of mitochondrial genomes in phylogenetic inference compared to nuclear rRNA genes. Cladistics, 34(2), 113–130.

    PubMed  Google Scholar 

  • Ogedengbe, M. E., El-Sherry, S., Ogedengbe, J. D., Chapman, H. D., & Barta, J. M. (2018). Phylogenies based on combined mitochondrial and nuclear sequences conflict with morphologically defined genera in the eimeriid coccidia (Apicomplexa). International Journal for Parasitology, 48, 56–69.

    Google Scholar 

  • Okabe M., & Ito, K. (2008). Color universal design (CUD)—How to make figures and presentations that are friendly to colorblind people. Retrieved from http://jfly.iam.u-tokyo.ac.jp/color/.

  • Pan, Y. C., Yi, Z., Shi, J. W., & Leng, T. H. (2004). The status and proposal of quality and safety management to aquatic products in China. Journal of Food Safety and Quality, 5(7), 2272–2279. (In Chinese).

    Google Scholar 

  • Peterman, M. A., & Posadas, B. C. (2019). Direct economic impact of fish diseases on the east Mississippi catfish industry. North American Journal of Aquaculture, 81(3), 222–229.

    Google Scholar 

  • Pond, S. L. K., Frost, S. D. W., & Muse, S. V. (2004). HyPhy: Hypothesis testing using phylogenies. Bioinformatics, 21(5), 676–679.

    PubMed  Google Scholar 

  • Pote, L. M., Hanson, L. A., & Shivaji, R. (2000). Small subunit ribosomal RNA sequences link the cause of proliferative gill disease in channel catfish to Henneguya n. sp. (Myxozoa: Myxosporea). Journal of Aquatic Animal Health, 12, 230–240.

    Google Scholar 

  • Pote, L. M., Khoo, L. H., & Griffin, M. J. (2012). Henneguya ictaluri. In P. T. K. Woo & K. Buchmann (Eds.), Fish parasites: Pathobiology and protection (pp. 177–182). Boston, Massachusetts: CAB International. https://doi.org/10.1079/9781845938062.0177

    Chapter  Google Scholar 

  • R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved September 5, 2020, from https://www.R-project.org.

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    CAS  PubMed  Google Scholar 

  • Rosser, T. G., Griffin, M. J., Quiniou, S. M. A, Khoo, L. M., & Pote, L. M. (2014a). 18S rRNA gene sequencing identifies a novel species of Henneguya parasitizing the gills of the channel catfish (Ictaluridae). Parasitology Research, 113, 4651–4658.

    PubMed  Google Scholar 

  • Rosser, T. G., Griffin, M. N., Quiniou, S. M. A., Greenway, T. E., Khoo, L. H., Wise, D. J., & Pote, L. M. (2014b). Molecular and morphological characterization of myxozoan actinospore types from a commercial catfish pond in the Mississippi Delta. Journal of Parasitology, 100(6), 828–839.

    PubMed  Google Scholar 

  • Rosser, T. G., Griffin, M. J., Quiniou, S. M. A., Khoo, L. H., Greenway, T. E., Wise, D. J., & Pote, L. M. (2015). 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. Parasitology Research, 114, 1595–1602.

    PubMed  Google Scholar 

  • Rosser, T. G., Alberson, N. R., Baumgartner, W. A., Mauel, M. J., Pote, L. M., & Griffin, M. J. (2016). Morphological, histological, and molecular description of Unicauda fimbrethilae n. sp. (Cnidaria: Myxosporea: Myxobolidae) from the intestinal tract of channel catfish Ictalurus punctatus. Journal of Parasitology, 102(1), 105–113.

    CAS  PubMed  Google Scholar 

  • Rosser, T. G., Khoo, L. H., Wise, D. J., Mischke, C. C., Greenway, T. E., Alberson, N. R., Reichley, S. R., Woodyard, E. T., Steadman, J., Ware, C., Pote, L. M., & Griffin, M. J. (2019). Arrested development of Henneguya ictaluri (Cnidaria: Myxobolidae) in ♀ Channel Catfish × ♂ Blue Catfish Hybrid. Journal of Aquatic Animal Health, 31(2), 201–213.

    CAS  PubMed  Google Scholar 

  • Rosser, T. G., Woodyard, E. T., Mychajlonka, M. N., King, D. T., Griffin, M. J., Gunn, M. A., & López-Porras, A. (2020). Ithyoclinostomum yamagutii n. sp. (Digenea: Clinostomidae) in the great blue heron Ardea Herodias L. (Aves: Ardeidae) from Mississippi, USA. Systematic Parasitology, 97, 69–82.

    PubMed  Google Scholar 

  • Rosser, T. G., Loch, T. P., Faisal, M., Baumgartner, W. A., & Griffin, M. J. (2021). Henneguya michiganensis n. sp. (Cnidaria: Myxosporea) from the gills of muskellunge Esox masquinongy Mitchill (Esociformes: Esocidae). Systematic Parasitology, 98, 119–130.

    PubMed  Google Scholar 

  • Salinas, N. R., & Little, D. P. (2014). 2matrix: a utility for indel coding and phylogenetic matrix concatenation. Applications in Plant Sciences, 2, 1300083. https://doi.org/10.3732/apps.1300083.

    Article  Google Scholar 

  • Shapiro, S. S., & Wilk, M. B. (1965). An analysis of variance test for normality (complete samples). Biometrika, 52(3/4), 591–611.

    Google Scholar 

  • Simmons, M. P., & Ochoterena, H. (2000). Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology, 49(2), 369–381.

    CAS  PubMed  Google Scholar 

  • Spencer, L. T., & Bancroft, J. D. (2013). Tissue processing. In: Suvarna, S. K., Layton, C. Bancroft, J. D. (Eds) Bancroft’s theory and practice of histological techniques. London: Churchill Livingstone, pp. 105–123.

    Google Scholar 

  • van Steenkiste, N., Locke, S. A., Castelin, M., Marcogliese, D. J., & Abbot, C. (2014). New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Molecular Ecology Resources, 15(4), 945–952.

    PubMed  Google Scholar 

  • Stilwell, J. M., Camus, A. C., Leary, J. H., Mohammed, H. H., & Griffin, M. J. (2019a). Molecular confirmation of Henneguya adiposa (Cnidaria: Myxozoa) and associated histologic changes in adipose fins of channel catfish, Ictalurus punctatus (Teleost). Fish Parasitology, 118, 1639–1645.

    Google Scholar 

  • Stilwell, J. M., Camus, A. C., Leary, J. H., Khoo, L. H., & Griffin, M. J. (2019b). Pathologic changes associated with respiratory compromise and morbidity due to massive interlamellar Henneguya exilis infection in channel × blue hybrid catfish. Journal of Parasitology, 105(5), 686–692.

    CAS  PubMed  Google Scholar 

  • Stilwell, J. M., Rosser, T. G., Woodyard, E. T., Richardson, B. M., López-Porras, A., Leary, J. H., Mischke, C. C., Camus, A. C., & Griffin, M. J. (2021). Characterisation of myxozoan fauna of western mosquitofish, Gambusia affinis (Baird and Gerard 1853) (Cyprinidontiformes: Poeciliidae), inhabiting experimental catfish ponds in Mississippi, USA. Systematic Parasitology, 98, 423–441.

  • Takeuchi, F., Sekizuka, T., Ogasawara, Y., Yokoyama, H., Kamikawa, R., Inagaki, Y., Nozaki, T., Sugita-Konishi, Y., Ohnishi, T., & Kuroda, M. (2015). The mitochondrial genomes of a myxozoan genus Kudoa are extremely divergent in Metazoa. PLoS ONE, 10(7), e0132030. https://doi.org/10.1371/journal.pone.0132030.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Truong, T. N. (2011). Biodiversity of metazoan parasites infecting channel catfish (Ictalurus punctatus), blue catfish (Ictalurus furcatus), and C×B hybrid catfish (Female Ictalurus punctatus × Male Ictalurus furcatus) in earthen pond aquaculture (Master’s thesis). Auburn University, Auburn, Alabama, USA.

    Google Scholar 

  • Whelan, S. Allen, J. E., Blackburne, B. P., & Talavera, D. (2015). ModelOMatic: Fast and austomated model selection between RY, nucleotide, amino acid, and codon substitution models. Systematic Biology, 64, 42–55.

    CAS  PubMed  Google Scholar 

  • Wei, T. Y., & Simko, V. (2017). R package "corrplot": Visualization of a correlation matrix. Retrieved April 8, 2021, from https://github.com/taiyun/corrplot.

  • Whipps, C. M., Grossel, G., Adlard, R. D., Yokoyama, H., Bryant, M. S., Munday, B. L., Kent, M. L. (2004). Phylogeny of the Mutlivalvulidae (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. Journal of Parasitology, 90, 618–622.

    CAS  PubMed  Google Scholar 

  • Whipps, C. M., & Kent, M. L. (2006). Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). Journal of Eukaryotic Microbiology, 53(5), 364–373.

    CAS  PubMed  Google Scholar 

  • Wiese, N., Engle, C., Trimpey, J., Quagrainie, K., & Green, B. (2006). Reducing catfish farm losses due to dockages assessed by processing plants. Journal of the World Aquaculture Society, 37(1), 60–73.

    Google Scholar 

  • Wise, D. J., Camus, A. C., Schwedler, T. E., & Terhune, J. S. (2004). Health management. In C. S. Tucker, & J. A. Hargreaves (Eds.), Biology and culture of channel catfish (pp. 444–502).

  • Wise, D. J., Griffin, M. J., Terhune, J. S., Pote, L. M., & Khoo, L. H. (2008). Induction and evaluation of proliferative gill disease in channel catfish fingerlings. Journal of Aquatic Animal Health, 4, 236–244.

    Google Scholar 

  • USDA (U.S. Department of Agriculture) NASS (National Agricultural Statistics Service). Catfish Production. (2021). Retrieved April 8, 2021, from https://www.nass.usda.gov/Publications/Todays_Reports/reports/cfpd0221.pdf.

  • van der Auwera, G., Chapelle, S., & de Wächter, R. (1994). Structure of the large ribosomal subunit RNA of Phytophthora megasperma, and phylogeny of oomycetes. FEBS Letters, 338(2), 133–136.

    PubMed  Google Scholar 

  • Woodyard, E. T., Stilwell, J. M., Camus, A. C., & Rosser, T. G. (2019). Molecular and histopathological data on Levisunguis subaequalis Curran, Overstreet, Collins & Benz, 2014 (Pentastomida: Eupentastomida: Porocephalida: Porocephaloidea: Sebekidae: Sebekinae) from Gambusia affinis in Alabama, USA. Journal of Parasitology, 105(6), 827–839.

    CAS  PubMed  Google Scholar 

  • Woodyard, E. T., Rosser, T. G., & McAllister, C. T. (2020). Morphological and molecular characterization of Myxidium kudoi Meglitsch, 1937 from the blue catfish Ictalurus furcatus, Valenciennes in Oklahoma, USA. Acta Parasitologica, 65, 388–395.

    CAS  PubMed  Google Scholar 

  • Yahalomi, D., Atkinson, S. D., Neuhof, M., Chang, E. S., Philippe, H., Cartwright, P., Bartholomew, J. L., & Huchon, D. (2020). A cnidarian parasite of salmon (Myxozoa: Henneguya) lacks a mitochondrial genome. PNAS, 117(10), 5358–5363.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yan, Y. J. (2011). Phylogenic study of five species of Myxosporeans (Myxozoa: Myxosporea) based on HSP70 gene data. (Master’s thesis.) Chongqing Normal University, Chongqing, China. (In Chinese).

  • Zhong, L. Q., Song, C., Chen, X. H., Deng, W., Xiao, Y. H., Wang, M. H., Qin, Q. M., Luan, S., Kong, J., & Bian, W. J. (2016). Channel catfish in China: Historical aspects, current status, and problems. Aquaculture, 465, 367–373.

    Google Scholar 

Download references

Acknowledgements

The authors thank Derek Marshall of Mississippi State University’s College of Veterinary Medicine Library for providing access to primary literature. Molecular data generated in this study are publicly available in GenBank (MZ905344–MZ905348, OK030693–OK030702, OK065607–OK065617). Photovouchers of myxospores are deposited in the Harold W. Manter Laboratory of Parasitology, University of Nebraska State Museum, Lincoln, Nebraska, USA (HWML 216707). A slide of a histological section through plasmodia is similarly deposited (HWML 216706).

Funding

This material is based upon work supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture, Project Number MIS‐371530, the U.S. Department of Agriculture, Agricultural Research Service–Catfish Health Initiative, the Mississippi State University College of Veterinary Medicine, the Mississippi Agriculture and Forestry Experiment Station (MAFES) and the National Center for Veterinary Parasitology.

Author information

Authors and Affiliations

  1. Department of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS, 39759, USA

    Ethan T. Woodyard, Lester H. Khoo & Matt. J. Griffin

  2. Department of Comparative Biomedical Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS, 39759, USA

    Thomas G. Rosser

  3. Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, GA, 30602, USA

    Justin M. Stilwell & Alvin C. Camus

  4. USDA-ARS Warmwater Aquaculture Research Unit, Thad Cochran National Warmwater Aquaculture Center, Stoneville, MS, 38776, USA

    Geoffrey Waldbieser

  5. Georgia Genomics and Bioinformatics Core, University of Georgia, Athens, GA, 30602, USA

    W. Walter Lorenz

Authors
  1. Ethan T. Woodyard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas G. Rosser
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Justin M. Stilwell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alvin C. Camus
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lester H. Khoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Geoffrey Waldbieser
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. W. Walter Lorenz
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Matt. J. Griffin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ethan T. Woodyard.

Ethics declarations

Conflict of interests

The authors declare no conflict of interest.

Ethical approval

The present work complied with all applicable institutional requirements for the care and handling of laboratory animals.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Woodyard, E.T., Rosser, T.G., Stilwell, J.M. et al. New data on Henneguya postexilis Minchew, 1977, a parasite of channel catfish Ictalurus punctatus, with notes on resolution of molecular markers for myxozoan phylogeny. Syst Parasitol 99, 41–62 (2022). https://doi.org/10.1007/s11230-021-10015-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11230-021-10015-3

Search

Navigation