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First report of Ovipleistophora ovariae and O. diplostomuri in China provides new insights into the intraspecific genetic variation and extends their distribution

Published online by Cambridge University Press:  28 October 2021

Meiqi Weng Open the ORCID record for Meiqi Weng [Opens in a new window] ,
Derong Xie ,
Qianqian Zhang ,
Aihua Li  and
Jinyong Zhang Open the ORCID record for Jinyong Zhang [Opens in a new window]
Meiqi Weng
Affiliation:
The Laboratory of Aquatic Parasitology, School of Marine Science and Engineering, Qingdao Agricultural University, 266237 Qingdao, China Key Laboratory of Aquaculture Diseases Control, Ministry of Agriculture and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 10049, China
Derong Xie
Affiliation:
The Laboratory of Aquatic Parasitology, School of Marine Science and Engineering, Qingdao Agricultural University, 266237 Qingdao, China Key Laboratory of Aquaculture Diseases Control, Ministry of Agriculture and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 10049, China
Qianqian Zhang*
Affiliation:
Key Laboratory of Aquaculture Diseases Control, Ministry of Agriculture and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China
Aihua Li
Affiliation:
Key Laboratory of Aquaculture Diseases Control, Ministry of Agriculture and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China
Jinyong Zhang*
Affiliation:
The Laboratory of Aquatic Parasitology, School of Marine Science and Engineering, Qingdao Agricultural University, 266237 Qingdao, China
*
Author for correspondence: Jinyong Zhang, E-mail: [email protected]
Author for correspondence: Jinyong Zhang, E-mail: [email protected]
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Abstract

Microsporidia of the genus Ovipleistophora are generally parasites of fishes and aquatic crustaceans. In the current study, Ovipleistophora diplostomuri and O. ovariae were firstly reported from Culter alburnus and Xenocypris argentea and Parabramis pekinensis, respectively. Both of them exclusively infected fish ovary and were morphologically, ultrastructurally and genetically characterized. Sporogony occurred in direct contact with the host cell cytoplasm and sporophorous vesicles were not observed for the new isolates of these two Ovipleistophora species. Spores of O. ovariae were for the first time observed to be dimorphic. Genetic analysis indicated that the genetic variation in the ITS and LSU sequences was distinct among between-host O. diplostomuri isolates. High sequence variation in ITS sequence suggests that it can be a reliable molecular marker to explore the population genetics of O. diplostomuri. This is the first report of these two Ovipleistophora species in China which extends their host and geographical range.

Keywords

FishmicrosporidiaovaryOvipleistophora
Type
Research Article
Information
Parasitology , Volume 149 , Issue 3 , March 2022 , pp. 314 - 324
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Copyright
Copyright © Qingdao Agricultural University, 2021. Published by Cambridge University Press.

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References

Al-Quraishy, S, Abdel-Baki, AS, Al-Qahtani, H, Dkhil, M, Casal, G and Azevedo, C (2012) A new microsporidian parasite, Heterosporis saurida n. sp. (Microsporidia) infecting the lizardfish, Saurida undosquamis from the Arabian Gulf, Saudi Arabia: ultrastructure and phylogeny. Parasitology 139, 454–462.CrossRefGoogle Scholar
Andreadis, TG and Vossbrinck, CF (2002) Life cycle, ultrastructure and molecular phylogeny of Hyalinocysta chapmani (Microsporidia: Thelohaniidae), a parasite of Culiseta melanura (Diptera: Culicidae) and Orthocyclops modestus (Copepoda: Cyclopidae). Journal of Eukaryotic Microbiology 49, 350–364.CrossRefGoogle Scholar
Andreadis, TG, Thomas, MC and Shepard, JJ (2018) Amblyospora khaliulini (Microsporidia: Amblyosporidae): investigations on its life cycle and ecology in Aedes communis (Diptera: Culicidae) and Acanthocyclops vernalis (Copepoda: Cyclopidae) with redescription of the species. Journal of Invertebrate Pathology 151, 113–125.CrossRefGoogle ScholarPubMed
Avery, SW and Undeen, AH (1990) Horizontal transmission of Parathelohania anopheles to the copepod, Microcyclops varicans, and the mosquito, Anopheles quadrimaculatus. Journal of Invertebrate Pathology 56, 98–105.CrossRefGoogle Scholar
Baker, MD, Vossbrinck, CR, Didier, ES, Maddox, JV and Shadduck, JA (1995) Small subunit ribosomal DNA phylogeny of various microsporidia with emphasis on AIDS-related forms. Journal of Eukaryotic Microbiology 42, 564–570.CrossRefGoogle ScholarPubMed
Bojko, J, Behringer, DC, Moler, P and Reisinger, L (2020) Ovipleistophora diplostomuri, a parasite of fish and their trematodes, also infects the crayfish Procambarus bivittatus. Journal of Invertebrate Pathology 169, 107306.CrossRefGoogle ScholarPubMed
Branchiccela, B, Arredondo, D, Higes, M, Invernizzi, C, Martín-Hernández, R, Tomasco, I, Zunino, P and Antúnez, K (2017) Characterization of Nosema ceranae genetic variants from different geographic origins. Microbial Ecology 73, 978–987.CrossRefGoogle ScholarPubMed
Cali, A and Takvorian, PM (2014) Developmental morphology and life cycles of the Microsporidia. In Weiss, LM and Becnel, JJ (eds), Microsporidia: Pathogens of Opportunity. Oxford: Wiley Blackwell, pp. 71–133.Google Scholar
Chaimanee, V, Chen, YP, Pettis, JS, Cornman, RS and Chantawannakul, P (2011) Phylogenetic analysis of Nosema ceranae isolated from European and Asian honeybees in Northern Thailand. Journal of Invertebrate Pathology 107, 229–233.CrossRefGoogle ScholarPubMed
Cordes, N, Huang, WF, Strange, JP, Cameron, SA, Griswold, TL, Lozier, JD and Solter, LF (2012) Interspecific geographic distribution and variation of the pathogens Nosema bombi and Crithidia species in United States bumble bee populations. Journal of Invertebrate Pathology 109, 209–216.CrossRefGoogle ScholarPubMed
El-Garhy, M, Cali, A, Morsy, K, Bashtar, AR and Al-Quraishy, S (2017) Ultrastructural characterization of Pleistophora macrozoarcidis Nigerelli 1946 (Microsporidia) infecting the ocean pout Macrozoarces americanus (Perciformes, Zoarcidae) from the Gulf of Maine, MA, USA. Parasitology Research 116, 61–71.CrossRefGoogle ScholarPubMed
Gatehouse, HS and Malone, LA (1998) The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size. Journal of Invertebrate Pathology 71, 97–105.CrossRefGoogle ScholarPubMed
González-Tortuero, E, Rusek, J, Maayan, I, Petrusek, A, Piálek, L, Laurent, S and Wolinska, J (2016) Genetic diversity of two daphnia-infecting microsporidian parasites, based on sequence variation in the internal transcribed spacer region. Parasites Vectors 9, 293.CrossRefGoogle ScholarPubMed
Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Haro, M, del Águila, C, Fenoy, S and Henriques-Gil, N (2003) Intraspecies genotype variability of the microsporidian parasite Encephalitozoon hellem. Journal of Clinical Microbiology 41, 4166–4171.CrossRefGoogle ScholarPubMed
Ironside, JE (2013) Diversity and recombination of dispersed ribosomal DNA and protein-coding genes in microsporidia. PLoS One 8, e55878.CrossRefGoogle ScholarPubMed
Kent, ML, Shaw, RW and Sanders, JL (2014) Microsporidia in fish. In Weiss, LM and Becnel, JJ (eds), Microsporidia: Pathogens of Opportunity. Oxford: Wiley Blackwell, pp. 493–520.Google Scholar
Krebes, K, Blank, M, Frankowski, J and Bastrop, R (2010) Molecular characterisation of the Microsporidia of the amphipod Gammarus duebeni across its natural range revealed hidden diversity, wide-ranging prevalence and potential for co-evolution. Infection Genetics and Evolution 10, 1027–1038.CrossRefGoogle ScholarPubMed
Li, JL, Chen, WF, Wu, J, Peng, WJ, An, JD, Schmid-Hempel, P and Schmid-Hempel, R (2012 a) Diversity of Nosema associated with bumble-bees (Bombus spp.) from China. International Journal for Parasitology 42, 49–61.CrossRefGoogle Scholar
Li, KB, Chang, OQ, Wang, F, Liu, C, Liang, HL and Wu, SQ (2012 b) Ultrastructure, development, and molecular phylogeny of Pleistophora hyphessobryconis, a broad host microsporidian parasite of Puntius tetrazona. Parasitology Research 111, 1715–1724.CrossRefGoogle ScholarPubMed
Liu, HD, Pan, GQ, Luo, B, Li, T, Yang, Q, Vossbrinck, CR, Debrunner-Vossbrinck, BA and Zhou, ZY (2013) Intraspecific polymorphism of rDNA among five Nosema bombycis isolates from different geographic regions in China. Journal of Invertebrate Pathology 113, 63–69.CrossRefGoogle ScholarPubMed
Liu, XH, Xu, LW, Luo, D, Zhao, YL, Zhang, QQ, Liu, GF and Zhang, JY (2018) Outbreak of mass mortality of yearling groupers of Epinephelus (Perciformes, Serranidae) associated with the infection of a suspected new enteric Sphaerospora (Myxozoa: Myxosporea) species in South China Sea. Journal of Fish Diseases 41, 663–672.CrossRefGoogle ScholarPubMed
Liu, XH, Stentiford, GD, Voronin, VN, Sato, H, Li, AH and Zhang, JY (2019) Pseudokabatana alburnus n. gen. n. sp., (Microsporidia) from the liver of topmouth culter Culter alburnus (Actinopterygii, Cyprinidae) from China. Parasitology Research 118, 1689–1699.CrossRefGoogle Scholar
Lovy, J and Friend, SE (2017) Phylogeny and morphology of Ovipleistophora diplostomuri n. sp. (Microsporidia) with a unique dual-host tropism for bluegill sunfish and the digenean parasite Posthodiplostomum minimum (Strigeatida). Parasitology 144, 1898–1911.CrossRefGoogle Scholar
Malcekova, B, Valencakova, A, Luptakova, L, Molnar, L, Ravaszova, P and Novotny, F (2011) First detection and genotyping of Encephalitozoon cuniculi in a new host species, gyrfalcon (Falco rusticolus). Parasitology Research 108, 1479–1482.CrossRefGoogle Scholar
Maside, X, Gómez-Moracho, T, Jara, J, Martín-Hernández, R, Rúa, PD, Higes, M and Bartolomé, C (2015) Population genetics of Nosema apis and Nosema ceranae: one host (Apis mellifera) and two different histories. PLoS One 10, e0145609.CrossRefGoogle ScholarPubMed
Maurand, J, Loubes, C, Gasc, C, Pelletier, J and Barral, J (1988) Pleistophora mirandellae Vaney & Conte, 1901, a microsporidian parasite in cyprinid fish of rivers in Hérault: taxonomy and histopathology. Journal of Fish Diseases 11, 251–258.CrossRefGoogle Scholar
Nylund, S, Nylund, A, Watanabe, K, Arnesen, CE and Karlsbakk, E (2010) Paranucleospora theridion n. gen., n. sp. (Microsporidia, Enterocytozoonidae) with a life cycle in the salmon louse (Lepeophtheirus salmonis, Copepoda) and Atlantic salmon (Salmo salar). Journal of Eukaryotic Microbiology 57, 95–114.CrossRefGoogle Scholar
Park, E and Poulin, R (2021) Revisiting the phylogeny of microsporidia. International Journal for Parasitology 51, 855–864.CrossRefGoogle ScholarPubMed
Pekkarinen, M, Lom, J and Nilsen, F (2002) Ovipleistophora gen. n., a new genus for Pleistophora mirandellae-like microsporidia. Diseases of Aquatic Organisms 48, 133–142.CrossRefGoogle Scholar
Pombert, JF, Xu, J, Smith, DR, Heiman, D, Young, S, Cuomo, CA, Weiss, LM and Keeling, PJ (2013) Complete genome sequences from three genetically distinct strains reveal high intraspecies genetic diversity in the microsporidian Encephalitozoon cuniculi. Eukaryotic Cell 12, 503–511.CrossRefGoogle ScholarPubMed
Ruehl-Fehlert, C, Bomke, C, Dorgerloh, M, Palazzi, X and Rosenbruch, M (2005) Pleistophora infestation in fathead minnows, Pimephales promelas (Rafinesque). Journal of Fish Diseases 28, 629–637.CrossRefGoogle Scholar
Sagastume, S, del Aguila, C, Martín-Hernández, R, Higes, M and Henriques-Gil, N (2011) Polymorphism and recombination for rDNA in the putatively asexual microsporidian Nosema ceranae, a pathogen of honeybees. Environmental Microbiology 13, 84–95.CrossRefGoogle ScholarPubMed
Santín, M and Fayer, R (2009) Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. Journal of Eukaryotic Microbiology 56, 34–38.CrossRefGoogle ScholarPubMed
Shaw, CL, Bilich, R, O'Brien, B, Cáceres, CE, Hall, SR, James, TM and Duffy, MA (2021) Genotypic variation in an ecologically important parasite is associated with host species, lake and spore size. Parasitology 148, 1303–1312.CrossRefGoogle Scholar
Smith, JE (2009) The ecology and evolution of microsporidian parasites. Parasitology 136, 1901–1914.CrossRefGoogle ScholarPubMed
Stentiford, GD, Bateman, KS, Feist, SW, Stone, DM and Dunn, AM (2013) Microsporidia: diverse, dynamic and emergent pathogens in aquatic systems. Trends in Parasitology 29, 567–578.CrossRefGoogle ScholarPubMed
Stentiford, GD, Ross, S, Minardi, D, Feist, SW, Bateman, KS, Gainey, PA and Bass, D (2018) Evidence for trophic transfer of Inodosporus octospora and Ovipleistophora arlo n. sp. (Microsporidia) between crustacean and fish hosts. Parasitology 145, 1105–1117.CrossRefGoogle Scholar
Summerfelt, RC and Goodwin, AE (2010) Ovipleistophoriasis: a microsporidian disease of the golden shiner ovary. In American Fisheries Society-Fish Health Section Blue Book: Suggested Procedures for the Detection and Identification of Certain Finfish and Shellfish Pathogens, 1.3.2.3, 2016 Edn. Accessible at: http://afs-fhs.org/bluebook/bluebook-index.php.Google Scholar
Taggart-Murphy, L, Alama-Bermejo, G, Dolan, B, Takizawa, F and Bartholomew, J (2021) Differences in inflammatory responses of rainbow trout infected by two genotypes of the myxozoan parasite Ceratonova shasta. Developmental and Comparative Immunology 114, 103829.CrossRefGoogle ScholarPubMed
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Thompson, JD, Gibson, TJ, Plewniak, F, Jeanmougin, F and Higgins, DG (1997) The CLUSTAL X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4883.CrossRefGoogle ScholarPubMed
Tsai, SJ, Kou, GH, Lo, CF and Wang, CH (2002) Complete sequence and structure of ribosomal RNA gene of Heterosporis anguillarum. Diseases of Aquatic Organisms 49, 199–206.CrossRefGoogle ScholarPubMed
Vávra, J and Lukeš, J (2013) Microsporidia and ‘the art of living together’. Advances in Parasitology 82, 253–319.CrossRefGoogle ScholarPubMed
Vávra, J, Hyliš, M, Fiala, I, Sacherová, V and Vossbrinck, CR (2017) Microsporidian genus Berwaldia (Opisthosporidia, Microsporidia), infecting daphnids (Crustacea, Branchiopoda): biology, structure, molecular phylogeny and description of two new species. European Journal of Protistology 61, 1–12.CrossRefGoogle ScholarPubMed
Weiss, LM and Vossbrinck, CR (1999) Molecular biology, molecular phylogeny, and molecular diagnostic approaches to the microsporidia. In Wittner, M and Weiss, LM (eds), The Microsporidia and Microsporidiosis. Washington: ASM Press, pp. 129–171.Google Scholar
Wilkinson, TJ, Rock, J, Whiteley, NM, Ovcharenko, MO and Ironside, JE (2011) Genetic diversity of the feminising microsporidian parasite Dictyocoela: new insights into host-specificity, sex and phylogeography. International Journal for Parasitology 41, 959–966.CrossRefGoogle ScholarPubMed
Xu, J, Wang, X, Jing, HQ, Cao, SK, Zhang, XF, Jiang, YY, Yin, JH, Cao, JP and Shen, YJ (2020) Identification and genotyping of Enterocytozoon bieneusi in wild Himalayan marmots (Marmota himalayana) and Alashan ground squirrels (Spermophilus alashanicus) in the Qinghai-Tibetan Plateau area (QTPA) of Gansu Province, China. Parasites Vectors 13, 367.CrossRefGoogle ScholarPubMed