Myxobolus wondjii sp. nov. (Myxozoa: Myxobolidae), a parasite of Labeo batesii Boulenger, 1911 (Teleostei: Cyprinidae) from the Makombè River, Cameroon: Morphological and molecular characterization
Abstract
A new species of the genus Myxobolus Bütschli, 1882 (Myxosporea: Bivalvulida) is described based on morphology, histopathology, and small subunit ribosomal DNA (SSU rDNA) sequence data. Myxobolus wondjii sp. nov. was found infecting the gills of Labeo batesii Boulenger, 1911 from the Makombè River at Nkondjock, Cameroon. Large, subspherical, whitish plasmodia measuring 100–2000 µm in length and 60–1400 µm in width were observed. Histopathological examination revealed plasmodia located in the interbranchial septum of the gill. Mature myxospores were ovoid, slightly tapering anteriorly, and with a broad, rounded posterior end. The myxospores measured 12.4 ± 0.1 (12.0–13.2) μm in length and 8.8 ± 0.07 (8.3–9.4) μm in width. The two polar capsules were ovoid and distinctly unequal in size, measuring 5.4 ± 0.50 (4.8–6.3) × 3.2 ± 0.06 (2.7–3.7) μm for the larger capsule and 1.6 ± 0.06 (1.4–1.7) × 1.0 ± 0.08 (0.9–1.1) μm for the smaller one. A partial SSU rDNA sequence was obtained from this new species, and phylogenetic analysis placed it as sister to Myxobolus nkondjockei, which also infects L. batesii in Cameroon.
References
Adriano E.A., Carriero M.M., Maia A.A.M., Silva M.R.M.D., Naldoni J., Ceccarelli P.S. & Arana S. 2012. Phylogenetic and host-parasite relationship analysis of Henneguya multiplasmodialis n. sp. infecting Pseudoplatystoma spp. in Brazilian Pantanal wetland. Veterinary Parasitology 185: 110–120. https://doi.org/10.1016/j.vetpar.2011.10.008
Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W. & Lipman D.J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25 (17): 3389–3402. https://doi.org/10.1093/nar/25.17.3389
Andree K.B., Székely C., Molnár K., Gresoviac S.J. & Hedrick R.P. 1999. Relationships among members of the genus Myxobolus (Myxozoa: Bilvalvidae) based on small subunit ribosomal DNA sequences. Journal of Parasitology 85: 68–74. https://doi.org/10.2307/3285702
Ayoade A., Fagade S. & Adebisi A. 2008. Diet and dietary habits of the fish Schilbe mystus (Siluriformes: Schilbeidae) in two artificial lakes in Southwestern Nigeria. Revista de Biología tropical 56: 1847–1855. https://doi.org/10.15517/rbt.v56i4.5764
Boungou M., Kabre G.B., Sakiti N.G., Marquès A. & Sawadogo L. 2006. Description of four new myxosporean species (Myxozoa: Myxosporea) from genus Myxobolus, fish parasites of Burkina-Faso, West Africa. Journal of Biological Sciences 6 (5): 861–867. https://doi.org/10.3923/jbs.2006.861.867
Carriero M.M., Adriano E.A., Silva M.R., Ceccarelli P.S. & Maia A.A. 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
Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2109
Deli A., Lekeufack Folefack G.B. & Fomena A. 2017. Description of Myxidium tetraodoni sp. nov., Myxidium anisocapsularis sp. nov. and Myxobolus magai sp. nov. (Myxosporea: Bivalvulida) infecting some freshwater fishes in Cameroon (Central Africa). Fisheries and Aquaculture Journal 8 (4): 1–10. https://doi.org/10.4172/2150-3508.1000235
Dyková I. & Lom J. 1978. Histopathological changes in fish gills infected with myxosporidian parasites of the genus Henneguya. Journal of Fish Biology 12 (3): 197–202. https://doi.org/10.1111/j.1095-8649.1978.tb04165.x
Eiras J.C. & D’Souza J. 2004. Myxobolus goensis n. sp. gills of (Myxozoa, Myxosporea, Myxobolidae), a parasite of the gills of Mugil cephalus (Osteichthyes, Mugilidae) from Goa, India. Parasite 11 (3): 243–248. https://doi.org/10.1051/parasite/2004113243
Eiras J.C., Molnár K. & Lu Y.S. 2005. Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Systematic Parasitology 61: 1–46. https://doi.org/10.1007/s11230-004-6343-9
Eiras J.C., Zhang J. & Molnár K. 2014. Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea, Myxobolidae) described between 2005 and 2013. Systematic Parasitology 88: 11–36. https://doi.org/10.1007/s11230-014-9484-5
Eiras J.C., Cruz1 F.C., Saraiva A. & Adriano E.A. 2021. Synopsis of the species of Myxobolus (Cnidaria, Myxozoa, Myxosporea) described between 2014 and 2020. Folia Parasitologica 68: 12–19. https://doi.org/10.14411/fp.2021.012
Eszterbauer E. 2004. Genetic relationship among gill-infecting Myxobolus species (Myxosporea) of cyprinids: molecular evidence of importance of tissue-specificity. Diseases of Aquatic Organisms 58: 35–40. https://doi.org/10.3354/dao058035
Feist S.W., Morris D.J., Alama-Bermejo G. & Holzer A.S. 2015. Cellular processes in myxozoans. In: Okamura B., Gruhl A. & Bartholomew J.L. (eds) Myxozoan Evolution, Ecology and Development: 139–154. Springer, Cham. https://doi.org/10.1007/978-3-319-14753-6_8
Ferguson J.A., Atkinson S.D., Whipps C.M. & Kent M.L. 2008. Molecular and morphological analysis of Myxobolus spp. of salmonid fishes with the description of a new Myxobolus species. Journal of Parasitology 94: 1322–1334. https://doi.org/10.1645/GE-1606.1
Feudjio-Dongmo B. 2023. Myxosporidia (Cnidaria: Myxosporea) Parasites of Labeo batesii Boulenger, 1911 and Labeobarbus batesii (Boulenger, 1903) (Teleostei: Cyprinidae) of the Makombè River at Nkondjock in the Littoral Region, Cameroon: Phenotypic, Molecular, Phylogenetic and Bio-ecological characterizations. Ph.D thesis, University of Yaoundé I.
Feudjio-Dongmo B., Lekeufack-Folefack G.B., Tene-Fossog B., Fomena A., Wondji C.S., Yurakhno V.M., Alomar S. & Mansour L. 2022. Myxobolus makombensis n. sp. infection in African carp Labeobarbus batesii from the Makombè River, Cameroon: morphological and molecular characterization. Diseases of Aquatic Organisms 151: 75–84. https://doi.org/10.3354/dao03691
Fiala I. 2006. The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology 36: 1521–1534. https://doi.org/10.1016/j.ijpara.2006.06.016
Fiala I., Bartošová P. & Whipps C.M. 2015. Classification and phylogenetics of Myxozoa. In: Okamura B., Gruhl A. & Bartholomew J.L. (eds) Myxozoan Evolution, Ecology and Development: 85–110. Springer, Cham. https://doi.org/10.1007/978-3-319-14753-6_5
Fomena A. & Bouix G. 1994. New Myxosporidia species (Myxozoa) from freshwater teleosts in Southern Cameroon (central Africa). Journal of African Zoology 108: 481–491.
Fomena A., Marques A., Bouix G. & Njiné T. 1994. Myxobolus bilongi n. sp., Thelohanellus assambai n. sp. et Thelohanellus sanagaensis n. sp., myxosporidies parasites de Labeo sp. (Téléostéen Cyprinidae) du Bassin de la Sanaga au Cameroun (Afrique Centrale). Annales de la Faculté des Sciences Yaoundé 3: 131–142.
Guo Q., Huang M., Liu Y., Zhang X. & Gu Z. 2018. Morphological plasticity in Myxobolus Bütschli, 1882: a taxonomic dilemma case and renaming of a parasite species of the common carp. Parasites & Vectors 11: e399. https://doi.org/10.1186/s13071-018-2943-0
Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
Hartigan A., Fiala I., Dyková I., Rose K., Phalen D.N. & Šlapeta J. 2012. New species of Myxosporea from frogs and resurrection of the genus Cystodiscus Lutz, 1889 for species with myxospores in gallbladders of amphibians. Parasitology 139: 478–496. https://doi.org/10.1017/S0031182011002149
Howes G.J. 1991. Systematics and biogeography: An overview. In: Winfield I.J. & Nelson J.S. (eds) Cyprinid Fishes—Systematics, Biology and Exploitation: 1–33. Chapman & Hall, London. https://doi.org/10.1007/978-94-011-3092-9_1
Kalavati C. & Nandi N.C. 2007. Handbook on Myxosporean Parasites of Indian Fishes. Zoological Survey of India, Kolkata.
Kalavati C., Rao J.V. & Vaidehi J. 1992. Myxosporidian parasites (Protozoa) of fishes of Chilka Lake, east coast of India: three new species of Henneguya Thélohan, Rudicapsula Kalavati and Narasimha-Murti and Unicauda Auerbach. Indian Journal of Parasitology 16: 77–83.
Kato E., Kasai A., Tomochi H., Li Y.-C. & Sato H. 2017. Four Myxobolus spp. (Myxosporea: Bivalvulida) from the gill lamellae of common carp (Cyprinus carpio) and Japanese silver crucian carp (Carassius langsdorfii) in the western part of Japan, with the description of three new species (M. tanakai n. sp., M. paratoyamai n. sp., and M. ginbuna n. sp.). Parasitology Research 116: 2427–2441. https://doi.org/10.1007/s00436-017-5545-4
Kaur H. & Attri R. 2015. Morphological and molecular characterization of Henneguya bicaudi n. sp. (Myxosporea: Myxobolidae) infecting gills of Cirrhinus mrigala (Ham.) in Harike Wetland, Punjab (India). Parasitology Research 114: 4161–4167. https://doi.org/10.1007/s00436-015-4647-0
Kaur H. & Singh R. 2011. Two new species of Myxobolus (Myxozoa: Myxosporea: Bivalvulida) infecting Indian freshwater fishes in Punjab wetlands (India). Parasitology Research 108: 1075–1082. https://doi.org/10.1007/s00436-011-2307-6
Kent M.L., Khattra J., Hedrick R.P. & Devlin R.H. 2000. Tetracapsula renicola n. sp. (Myxozoa: Saccosporidae); the PKX myxozoan-the cause of proliferative kidney disease of salmonid fishes. Journal of Parasitology 86 (1): 103–111. https://doi.org/10.1645/0022-3395(2000)086[0103:TRNSMS]2.0.CO;2
Kent M., Andree K., Bartholomew J.L., El-Matbouli, M., Desser S.S., Delving R.H., Feist S.W., Hedrick R.P., Hoffman R.W., Khattra J., Hallet S.L., Lester R.J.G., Longshaw M., Palenzuela O., Sidal M.E. & Xiao C. 2001. Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology 49: 395–413. https://doi.org/10.1111/j.1550-7408.2001.tb00173.x
Kozlov A.M., Darriba D., Flouri T., Morel B. & Stamatakis A. 2019. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35: 4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Lalitha Kumari P.S. 1969. Studies on parasitic protozoa (Myxosporidia) of fresh water fishes of Andhra Pradesh, India. Rivista di Parassitologia 30 (3): 153–226.
Lekeufack-Folefack G.B. & Fomena A. 2013. Structure et dynamique des infracommunautés de myxosporidies parasites de Ctenopoma petherici Günther, 1864 (Anabantidae), Clarias pachynema Boulenger, 1903 (Clariidae) et Hepsetus odoe (Bloch, 1794) (Hepsetidae) dans la rivière Sangé au Cameroun. International Journal of Biological and Chemical Sciences 7: 2301–2316. https://doi.org/10.4314/ijbcs.v7i6.11
Lekeufack-Folefack G.B., Abdel-Baki A.A.S., Ateba N.O.O., Fomena A. & Mansour L. 2019. Morphological and molecular characterization of Myxobolus dibombensis sp. n. (Myxozoa: Myxobolidae), a parasite of the African Carp Labeobarbus batesii (Teleostei: Cyprinidae) from Dibombe River, Cameroon. Parasitology Research 118: 763–771. https://doi.org/10.1007/s00436-019-06209-w
Lekeufack-Folefack G.B., Feudjio-Dongmo B., Fomena A., Tene-Fossog B. & Wondji M.J. 2020. An optimized protocol for Myxosporidia (Cnidaria: Myxosporea) DNA extraction for molecular studies. Open Journal of Animal Science 10: 378–386. https://doi.org/10.4236/ojas.2020.103023
Lekeufack-Folefack G.B., Tchoutezo-Tiwa A.E., Al-Tamimi J., Fomena A., AL-Omar S.Y. & Mansour L. 2021. Myxobolus opsaridiumi sp. nov. (Cnidaria: Myxosporea) infecting different tissues of an ornamental fish, Opsaridium ubangiensis (Pellegrin, 1901), in Cameroon: morphological and molecular characterization. European Journal of Taxonomy 733: 56–71. https://doi.org/10.5852/ejt.2021.733.1221
Lekeufack-Folefack G.B., Feudjio-Dongmo B., Tene-Fossog B., Fomena A., Wondji C.S., Al-Tamimi J., Yurakhno V.M. & Mansour L. 2022. Morphological and molecular characterization of Myxobolus nkondjockei sp. nov. (Myxozoa: Myxobolidae), a parasite of Labeo batesii Boulenger, 1911 (Teleostei: Cyprinidae) from Makombè River in Cameroon. Acta Parasitologica 67: 1573–1583. https://doi.org/10.1007/s11686-022-00609-2
Liu Y., Whipps C.M., Gu Z.M. & Zeng L.B. 2010. Myxobolus turpisrotundus (Myxosporea: Bivalvulida) spores with caudal appendages: investigating the validity of the genus Henneguya with morphological and molecular evidence. Parasitology Research 107: 699–706. https://doi.org/10.1007/s00436-010-1924-9
Liu Y., Lövy A., Gu Z. & Fiala I. 2019. Phylogeny of Myxobolidae (Myxozoa) and the evolution of myxospore appendages in the Myxobolus clade. International Journal of Parasitology 49 (7): 523–530. https://doi.org/10.1016/j.ijpara.2019.02.009
Lom J. & Arthur J.R. 1989. A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases 12: 151–156. https://doi.org/10.1111/j.1365-2761.1989.tb00287.x
Lom J. & Dyková I. 2006. Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53: 1–36. https://doi.org/10.14411/fp.2006.001
Mansour L., Abdel-Haleem H.M., Atwa M., Darwish A.B., Al-Quraishy S. & Abdel-Baki A.-A.S. 2021. A new myxozoan parasite, Myxobolus allami sp. n. (Myxozoa: Myxobolidae) from the intestinal wall of Sparidentex hasta (Valenciennes) in Arabian Gulf. Folia Parasitologica 68: e017. https://doi.org/10.14411/fp.2021.017
Mirandola Dias Vieira D.H., Bravin Narciso R. & da Silva R.J. 2022. Diversity of myxozoans parasitizing the catfish Rhamdia quelen (Siluriformes: Heptapteridae), in southeastern Brazil, based on morphological and molecular evidence. Scientific Reports 12: e17596. https://doi.org/10.1038/s41598-022-22418-3
Molnár K. 2002. Site preference of fish myxosporeans in the gill. Diseases of Aquatic Organisms 48 (3): 197–207. https://doi.org/10.3354/dao048197
Molnár K., Eszterbauer E., Székely C., Dán Á. & Harrach B. 2002. Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. Journal of Fish Diseases 25 (11): 643–652. https://doi.org/10.1046/j.1365-2761.2002.00409.x
Molnár K., Marton S., Székely C. & Eszterbauer E. 2010. Differentiation of Myxobolus spp. (Myxozoa: Myxobolidae) infecting roach (Rutilus rutilus) in Hungary. Parasitology Research 107: 1137–1150. https://doi.org/10.1007/s00436-010-1982-z
Nchoutpouen E. & Fomena A. 2011. The study of three new species of Myxobolus (Myxosporea: Myxobolidae) parasites of Labeo parvus Boulenger, 1902, cyprinid fish in Cameroon. Journal of Applied Biosciences 38: 2508–2517.
Nwani C.D., Odoh G.E., Ude E.F. & Okogwu O.I. 2011. Food and feeding habits of Gnathonemus petersii (Osteichthyes: Mormyridae) in Anambra River, Nigeria. International Aquatic Research 3: 45–51.
Okamura B., Gruhl A. & Bartholomew J.L. 2015. An introduction to myxozoan evolution, ecology and developmemt. In: Okamura B., Gruhl A. & Bartholomew J.L. (eds) Myxozoan Evolution, Ecology and Development: 1–20. Springer, Cham. https://doi.org/10.1007/978-3-319-14753-6_1
Okkay S., Gürkanlı C.T., Çiftçi Y. & Özer A. 2024. New molecular evidence on the members of the genus Ortholinea (Cnidaria, Myxozoa) and the description of Ortholinea hamsiensis n. sp. infecting the urinary bladder of European anchovy Engraulis engrasicolus [sic] in the Black Sea. Parasitology 151: 485–494. https://doi.org/10.1017/S0031182024000325
Piaton E., Fabre M., Goubin-Versini I., Bretz-Grenier M.F., Courtade-Saïdi M., Vincent S., Belleannée G., Thivolet F., Boutonnat J., Debaque H., Fleury-Feith J., Vielh P., Cochand-Priollet B., Egelé C., Bellocq J.P. & Michiels J.F. 2015. Recommandations techniques et règles de bonne pratique pour la coloration de May-Grünwald-Giemsa: revue de la littérature et apport de l’assurance qualité. Annales de Pathologie 35: 294–305. https://doi.org/10.1016/j.annpat.2015.05.019
Rácz O.Z., Székely C. & Molnár K. 2004. Intraoligochaete development of Myxobolus intimus (Myxosporea: Myxobolidae), a gill myxosporean of the roach (Rutilus rutilus). Folia Parasitologica 51: 199–207.
Rambaut A. 2016. FigTree v1.4.3. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. Available from http://tree.bio.ed.ac.uk/software/Figtree [accessed 28 Aug. 2025].
Rocha S., Azevedo C., Oliveira E., Alves Â., Antunes C., Rodrigues P. & Casal G. 2019. Phylogeny and comprehensive revision of mugiliform-infecting myxobolids (Myxozoa, Myxobolidae), with the morphological and molecular redescription of the cryptic species Myxobolus exiguus. Parasitology 146: 479–496. https://doi.org/10.1017/S0031182018001671
Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
Ruxton C.H.S., Calder P.C., Reed S.C. & Simpson M.J.A. 2005. The impact of long-chain n-3 polyunsaturated fatty acids on human health. Nutrition Research Reviews 18 (1): 113–129. https://doi.org/10.1079/NRR200497
Seenappa D. & Manohar L. 1981. Five new species of Myxobolus (Myxosporea: Protozoa), parasitic in Cirrhina mrigala (Hamilton) and Labeo rohita (Hamilton), with a note on a new host record for M. curmucae Seenappa & Manohar, 1980. Journal of Protozoology 28: 358–360. https://doi.org/10.1111/j.1550-7408.1981.tb02866.x
Skelton P.H., Tweddle D. & Jackson P.B.N. 1991. Cyprinids of Africa. In: Winfield I.J. & Nelson J.S. (eds) Cyprinid Fishes: Systematics, Biology and Exploitation: 211–239. Chapman & Hall, London. https://doi.org/10.1007/978-94-011-3092-9_7
Smothers J.F., von Dohlen C.D., Smith L.H. & Spall R.D. 1994. Molecular evidence that the myxozoan protists are metazoans. Science 265: 1719–1721. https://doi.org/10.1126/science.8085160
Stiassny I.G., Teugels G.G. & Hopkins C.D. 2007. The Fresh and Brackish Water Fishes of Lower Guinea, West-Central Africa, Volumes 1 & 2. Faune et Flore Tropicales, 42. IRD Editions & Muséum national d’Histoire naturelle, Paris.
Tripathi Y.R. 1952. Studies on parasites of Indian fishes, I, Protozoa Myxosporidia together with a check list of parasitic protozoa described from Indian fishes. Records of the Zoological Survey of India 50: 63–88. https://doi.org/10.26515/rzsi/v50/i1/1952/162075
Urawa S., Freeman M.A., Johnson S.C., Jones S.R.M. & Yokoyama H. 2011. Geographical variation in spore morphology, gene sequences, and host specificity of Myxobolus arcticus (Myxozoa) infecting salmonid nerve tissues. Diseases of Aquatic Organisms 96: 229–237. https://doi.org/10.3354/dao02398
Wolfe D. 2019. Tissue processing. In: Bancroft J.D. & Gamble M. (eds) Bancroft’s Theory and Practice of Histological Techniques: 77–83. Elsevier. https://doi.org/10.1016/B978-0-7020-6864-5.00006-2
Xi B.-W., Zhao X., Li P. & Xie J. 2019. Morphological variation in Myxobolus drjagini (Akhmerov, 1954) from silver carp and description of Myxobolus paratypicus n. sp. (Cnidaria: Myxozoa). Parasitology Research 118: 2149–2157. https://doi.org/10.1007/s00436-019-06350-6
Zhang X., Liu Y., Whipps C.M., Guo Q. & Gu Z. 2019. Multiple evolutionary routes of the single polar capsule in Thelohanellus species (Myxozoa; Myxobolidae). International Journal for Parasitology: Parasites and Wildlife 8: 56–62. https://doi.org/10.1016/j.ijppaw.2018.11.006
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