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Molecular cytogenetic analysis of a triploid population of the human broad tapeworm, Dibothriocephalus latus (Diphyllobothriidea)

Published online by Cambridge University Press:  08 March 2021

Martina Orosová Open the ORCID record for Martina Orosová [Opens in a new window] ,
Anna Marková ,
Irena Provazníková Open the ORCID record for Irena Provazníková [Opens in a new window] ,
Mikuláš Oros Open the ORCID record for Mikuláš Oros [Opens in a new window] ,
Alžbeta Radačovská ,
Zuzana Čadková  and
František Marec Open the ORCID record for František Marec [Opens in a new window]
Martina Orosová*
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, Košice04001, Slovakia
Anna Marková
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, Košice04001, Slovakia
Irena Provazníková
Affiliation:
Biology Centre of the Czech Academy of Sciences, Institute of Entomology, Branišovská 31, České Budějovice37005, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 1760, České Budějovice37005
Mikuláš Oros
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, Košice04001, Slovakia
Alžbeta Radačovská
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, Košice04001, Slovakia
Zuzana Čadková
Affiliation:
Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Science Prague (CZU), Kamýcká 129, Prague16500
František Marec
Affiliation:
Biology Centre of the Czech Academy of Sciences, Institute of Entomology, Branišovská 31, České Budějovice37005, Czech Republic
*
Author for correspondence: Martina Orosová, E-mail: [email protected]
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Abstract

The large-sized tapeworm Dibothriocephalus latus is known as the broad or fish-borne cestode of mammals that is capable to infect humans and cause diphyllobothriosis. Recently, molecular data on D. latus has been accumulating in the literature and a complete genome sequence has been published; however, little is known about the karyotype and chromosome architecture. In this study, an in-depth karyological analysis of 2 D. latus specimens was carried out. The plerocercoids originated from a perch caught in subalpine Lake Iseo (Italy) and the tapeworms were reared in hamsters. Both specimens contained cells with a highly variable number of chromosomes ranging from18 to 27. Nevertheless, the largest portion of mitotic figures (47%) showed a number corresponding to the triploid set, 3n = 27. Accordingly, the karyotype of the analyzed specimens consisted of 9 triplets of metacentric chromosomes. Fluorescence in situ hybridization (FISH) with the 18S rDNA probe clearly demonstrated the presence of 3 clusters of hybridization signals on the triplet of chromosome 7, thus confirming the triploid status of the specimens. FISH with a telomeric (TTAGGG)n probe confined hybridization signals exclusively to the terminal chromosomal regions, supporting the earlier findings that this repetitive motif is a conserved feature of tapeworm telomeres.

Keywords

18S rDNAparthenogenesispolyploidizationtelomerestriploid
Type
Research Article
Information
Parasitology , Volume 148 , Issue 7 , June 2021 , pp. 787 - 797
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

*

Present address: Genomics Core Facility, European Molecular Biology Laboratory, Heidelberg, Germany.

References

Agatsuma, T, Terasaki, L, Yang, L and Blair, D (1994) Genetic variation in the triploids of Japanese Fasciola species, and relationships with other species in the genus. Journal of Helminthology 68, 181–186.CrossRefGoogle ScholarPubMed
Andersen, K (1972) Studies of the helminth fauna of Norway. XXIV. The morphology of Diphyllobothrium ditremum (Creplin, 1825) from the golden hamster (Mesocricetus auratus Waterhouse, 1839) and a comparison with D. dendriticum (Nitzsch, 1824) and D. latum (L. 1758) from the same final host. Norwegian Journal of Zoology 20, 255–264.Google Scholar
Andersen, K (1978) The development of the tapeworm Diphyllobothrium latum (L. 1756) (Cestoda; Pseudophyllidea) in its definitive hosts, with special references to the growth patterns of D. dendriticum (Nitzsch, 1824) and D. ditremum (Creplin, 1827). Parasitology 77, 111–120.CrossRefGoogle Scholar
Andersen, K and Halvorsen, O (1978) Egg size and form as taxonomic criteria in Diphyllobothrium (Cestoda: Pseudophyllidea). Parasitology 76, 229–240.CrossRefGoogle Scholar
Bazsalovicsová, E, Koleničová, A, Králová-Hromadová, I, Minárik, G, Šoltys, K, Kuchta, R and Štefka, J (2018) Development of microsatellite loci in zoonotic tapeworm Dibothriocephalus latus (Linnaeus, 1758), Lühe, 1899 (syn. Diphyllobothrium latum) using microsatellite library screening. Molecular and Biochemical Parasitology 225, 1–3.CrossRefGoogle ScholarPubMed
Benazzi, M (1982) Speciation events as evidenced in Turbellaria. In Barigozzi, C (ed.), Mechanisms of Speciation. New York: Alan R. Liss, pp. 307–344.Google Scholar
Blair, D, Nawa, Y, Mitreva, M and Doanh, PN (2016) Genetic diversity and genetic variation in lung flukes (genus Paragonimus). Transactions of the Royal Society of Tropical Medicine and Hygiene 110, 6–12.CrossRefGoogle Scholar
Bombarová, M, Vítková, M, Špakulová, M and Koubková, B (2009) Telomere analysis of platyhelminths and acanthocephalans by FISH and Southern hybridization. Genome 52, 897–903.CrossRefGoogle ScholarPubMed
Bruňanská, M, Drobníková, P and Oros, M (2009) Vitellogenesis in the cestode Atractolytocestus huronensis Anthony, 1958 (Caryophyllidea: Lytocestidae). Parasitology Research 105, 647–654.CrossRefGoogle Scholar
Carabajal Paladino, LZ, Nguyen, P, Šíchová, J and Marec, F (2014) Mapping of single-copy genes by TSA-FISH in the codling moth, Cydia pomonella. BMC Genetics 15, S15.CrossRefGoogle ScholarPubMed
Chai, JY, Darwin Murrell, K and Lymbery, AJ (2005) Fish-borne parasitic zoonoses: status and issues. International Journal of Parasitology 35, 1233–1254.CrossRefGoogle ScholarPubMed
Chinone, A, Nodono, H and Matsumoto, M (2014) Triploid planarian reproduces truly bisexually with euploid gametes produced through a different meiotic system between sex. Chromosoma 123, 265–272.CrossRefGoogle ScholarPubMed
Christen, M and Milinski, M (2003) The consequences of self-fertilization and outcrossing of the cestode Schistocephalus solidus in its second intermediate host. Parasitology 126, 369–378.CrossRefGoogle ScholarPubMed
Comai, L (2005) The advantages and disadvantages of being polyploid. Nature Reviews. Genetics 6, 836–846.CrossRefGoogle ScholarPubMed
Dick, TA and Poole, BC (1985) Identification of Diphyllobothrium dendriticum and Diphyllobothrium latum from some freshwater fishes of central Canada. Canadian Journal of Zoology 63, 196–201.CrossRefGoogle Scholar
Fujino, T and Ishii, Y (1982) Ultrastructural studies on spermatogenesis in a parthenogenetic type of Paragonimus westermani (Kerbert 1878) proposed as P. pulmonalis (Baelz 1880). The Journal of Parasitology 68, 433–441.CrossRefGoogle Scholar
Gassner, M, Dejaco, T, Schönswetter, P, Marec, F, Arthofer, W, Schlick-Steiner, BC and Steiner, FM (2014) Extensive variation in chromosome number and genome size in sexual and parthenogenetic species of the jumping-bristletail genus Machilis (Archaeognatha). Ecology and Evolution 4, 4093–4105.CrossRefGoogle Scholar
Giuliano-Caetano, L, Jorge, LC, Moreira-Filho, O and Bertollo, LAC (2001) Comparative cytogenetics studies in Hoplerythrinus unitaeniatus populations. Cytologia 66, 39–43.CrossRefGoogle Scholar
Grey, AJ (1979) A comparative study of the chromosomes of twenty species of caryophyllidean tapeworms (Dissertation). College of Arts and Sciences, Department of Biology, State University of New York at Albany, USA. p. 214.Google Scholar
Grey, AJ and Mackiewicz, JS (1980) Chromosomes of the caryophyllidean cestodes: diploidy, triploidy and parthenogenesis in Glaridacris catostomi. International Journal for Parasitology 10, 397–407.CrossRefGoogle Scholar
Gustinelli, A, Menconi, V, Prearo, M, Caffara, M, Righetti, M, Scanzio, T, Raglio, A and Fioravanti, ML (2016) Prevalence of Diphyllobothrium latum (Cestoda: Diphyllobothriidae) plerocercoids in fish species from four Italian lakes and risk for the consumers. International Journal of Food Microbiology 17, 109–112.CrossRefGoogle Scholar
International Helminth Genomes Consortium (2019) Comparative genomics of the major parasitic worms. Nature Genetics 51, 163–174.CrossRefGoogle Scholar
Jones, AW and Mackiewicz, JS (1969) Naturally occurring triploidy and parthenogenesis in Atractolytocestus huronensis Anthony (Cestoidea: Caryophyllidea) from Cyprinus carpio L. in North America. The Journal of Parasitology 55, 1105–1118.CrossRefGoogle Scholar
Kato, A, Albert, PS, Vega, JM and Birchler, JA (2006) Sensitive fluorescence in situ hybridization signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotechnic and Histochemistry 81, 71–78.CrossRefGoogle ScholarPubMed
Kuchta, R and Scholz, T (2017) Diphyllobothriidea. In Caira, JN and Jensen, J (eds), Tapeworms From Vertebrate Bowels of the Earth 2008–2017. Special Publication No. 25, USA, Kansas: Lawrence University of Kansas, Natural History Museum, pp. 167–189.Google Scholar
Kuchta, R, Scholz, T, Brabec, J and Bray, RA (2008) Suppression of the tapeworm order Pseudophyllidea (Platyhelminthes: Eucestoda) and the proposal of two new orders. Bothriocephalidea and Diphyllobothriidea. International Journal of Parasitology 38, 49–55.CrossRefGoogle ScholarPubMed
Kuchta, R, Scholz, T, Brabec, J and Narduzi-Wicht, B (2015) Diphyllobothrium, Diplogonoporus and Spirometra. In Xiao L, Ryan U and Feng Y (eds), Biology of Foodborne Parasites. Boca Raton: CRC Press, pp. 299–326.Google Scholar
Kuchta, R, Radačovská, A, Bazsalovicsová, E, Viozzi, G, Semenas, L, Arbetman, M and Scholz, T (2019) Host switching of zoonotic broad fish tapeworm (Dibothriocephalus latus) to salmonids, Patagonia. Emerging Infectious Diseases 25, 2156–2158.CrossRefGoogle ScholarPubMed
Levan, A, Fredga, K and Sandberg, A (1964) Nomenclature for centromere position on chromosomes. Hereditas 52, 201–220.CrossRefGoogle Scholar
Littlewood, DTJ and Olson, PD (2001) Small subunit rDNA and the platyhelminthes: signal, noise, conflict and compromise. In Littlewood, DTJ and Bray, RA (eds), Interrelationships of the Platyhelminthes. London: Taylor and Francis, pp 262–278.Google Scholar
Liu, G and He, L (1988) G-banding of chromosomes and G-bands quantitative analysis of Spirometra mansoni by microscopic photometer. Annual Bulletin of the Society of Parasitology, Guangdong Province 10, 137–138 (In Chinese).Google Scholar
Lutes, AA, Neaves, WB, Baumann, DP, Wiegraabe, W and Baumann, P (2010) Sister chromosome pairing maintains heterozygosity in parthenogenetic lizards. Nature Letters 464, 283–286.CrossRefGoogle ScholarPubMed
Marec, F (1996) Synaptonemal complexes in insects. International Journal of Insect Morphology and Embryology 25, 205–233.CrossRefGoogle Scholar
Okino, T, Ushirogawa, H, Matoba, K, Nishimatsu, S and Saito, M (2017) Establishment of the complete life cycle of Spirometra (Cestoda: Diphyllobothriidae) in the laboratory using a newly isolated triploid clone. Parasitology International 66, 116–118.CrossRefGoogle ScholarPubMed
Orosová, M and Špakulová, M (2018) Tapeworm chromosomes: their value in systematics with instructions for cytogenetic study. Folia Parasitologica 65, 001.CrossRefGoogle ScholarPubMed
Orosová, M, Provazníková, I, Xi, BW and Oros, M (2019) Chromosomal study of Khawia abbottinae (Cestoda: Caryophyllidea): karyotype and localization of telomeric and ribosomal sequences after fluorescence in situ hybridization (FISH). Parasitology Research 118, 2789–2800.CrossRefGoogle Scholar
Otto, SP (2007) The evolutionary consequences of polyploidy. Cell 31, 452–462.CrossRefGoogle Scholar
Otto, SP and Whitton, J (2000) Polyploid incidence and evolution. Annual Review of Genetics 34, 401–437.CrossRefGoogle ScholarPubMed
Park, GM, Yong, TS, Im, KI and Chung, EY (2000) Karyotypes of three species of Corbicula (bivalvia: Veneroida) in Korea. Journal of Shellfish Research 19, 979–982.Google Scholar
Petkevičiūtė, R (1992) Comparative cytogenetics of Diphyllobothrium ditremum (Creplin, 1925) and Ligula intestinalis (Linnaeus, 1758) (Cestoda: Pseudophyllidea). Systematic Parasitology 23, 167–173.CrossRefGoogle Scholar
Petkevičiūtė, R (1996) A chromosome study of Schistocephalus solidus (Muller, 1776) (Cestoda: Pseudophyllidea). Systematic Parasitology 33, 183–186.CrossRefGoogle Scholar
Petkevičiūtė, R and Kuperman, BI (1992) Karyological investigation of Caryophyllaeus laticeps (Pallas, 1781) (Cestoda: Caryophyllidea). Folia Parasitologica 39, 115–121.Google Scholar
Ráb, P and Roth, P (1988) Cold-blooded vertebrates. In Balíček, P, Forejt, J and Rubeš, J (eds), Methods of Chromosome Analysis. Brno: Czechoslovak Biological Society Publishers, pp. 115–124.Google Scholar
Radačovská, A, Bazsalovicsová, E, Blasco Costa, I, Orosová, M, Gustinelli, A and Králová-Hromadová, I (2019) Occurrence of Dibothriocephalus latus in European perch from Alpine lakes, an important focus of diphyllobothriosis in Europe. Revue suisse de Zoologie 126, 219–225.Google Scholar
Rhee, JK, Eun, GS and Lee, SB (1987) Karyotype of Fasciola sp. Obtained from Korean cattle. The Korean Journal of Parasitology 25, 37–41.CrossRefGoogle ScholarPubMed
Sahara, K, Marec, F and Traut, W (1999) TTAGG Telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Research 76, 449–460.CrossRefGoogle Scholar
Sasada, K (1978) Studies on the chromosomes of parasitic helminths. II. Triploidy and cytological mechanism of parthenogenesis in Diphyllobothrium erinacei (Cestoda: Diphyllobothriidae). Japanese Journal of Parasitology 27, 547–560.Google Scholar
Schiffer, PH, Danchin, EGJ, Burnell, AM, Creevey, CJ, Wong, S, Dix, I, O'Mahony, G, Culleton, BA, Rancurel, C, Stier, G, Martínez-Salazar, EA, Marconi, A, Trivedi, U, Kroiher, M, Thorne, MAS, Schierenberg, E, Wiehe, T and Blaxter, M (2019) Signatures of the evolution of parthenogenesis and cryptobiosis in the genomes of panagrolaimid nematodes. iScience 21, 587–602.CrossRefGoogle ScholarPubMed
Scholz, T and Kuchta, R (2016) Fish-borne, zoonotic cestodes (Diphyllobothrium and relatives) in cold climates: a never-ending story of neglected and (re)-emergent parasites. Food and Waterborne Parasitology 4, 1–62.CrossRefGoogle Scholar
Scholz, T, Garcia, HH, Kuchta, R and Wicht, B (2009) Update on the human broad tapeworm (genus Diphyllobothrium) including clinical relevance. Clinical Microbiology Reviews 22, 146–160.CrossRefGoogle ScholarPubMed
Scholz, T, Kuchta, R and Brabec, J (2019) Broad tapeworms (Diphyllobothriidae), parasites of wildlife and humans: recent progress and future challenges. International Journal of Parasitology: Parasites and Wildlife 5, 359–369.Google Scholar
Shaffer, B, Brearley, I, Littlewood, R and Fink, GR (1971) A stable aneuploid of Saccharomyces cerevisiae. Genetics 67, 483–495.CrossRefGoogle ScholarPubMed
Shen, HP, Tsai, C, Fang, YP, Chen, JH (2011) Parthenogenesis, polyploidy and reproductive seasonality in the Taiwanese mountain earthworm Amynthas catenus Tsai et al., 2001 (Oligochaeta, Megascolecidae). Pedobiologia 54, 133–139.CrossRefGoogle Scholar
Špakulová, M, Orosová, M and Mackiewicz, JS (2011) Cytogenetics and chromosomes of the tapeworms (Platyhelmithes, Cestoda). Advances in Parasitology 74, 177–230.CrossRefGoogle Scholar
Špakulová, M, Bombarová, M, Miklisová, D, Nechybová, S and Langrová, I (2019) How to become a successful invasive tapeworm: a case study of abandoned sexuality and exceptional chromosome diversification in the triploid carp parasite Atractolytocestus huronensis Anthony, 1958 (Caryophyllidea: Lytocestidae). Parasites and Vectors 12, 161.CrossRefGoogle Scholar
Storchova, Z and Pellman, D (2004) From polyploidy to aneuploidy, genome instability and cancer. Nature Reviews, Molecular Cell Biology 5, 45–54.CrossRefGoogle ScholarPubMed
Tilquin, A and Kokko, H (2016) What does the geography of parthenogenesis teach us about sex? Philosophical Transactions Royal Society B 371, 20150538.CrossRefGoogle ScholarPubMed
Traut, W, Sahara, K, Otto, TD and Marec, F (1999) Molecular differentiation of sex chromosomes probed by comparative genomic hybridization. Chromosoma 108, 173–180.CrossRefGoogle ScholarPubMed
Waeschenbach, A, Brabec, J, Scholz, T, Littlewood, DTJ and Kuchta, R (2017) The catholic taste of broad tapeworms – multiple routes to human infection. International Journal of Parasitology 47, 831–843.CrossRefGoogle ScholarPubMed
Wicht, B, Yanagida, T, Scholz, T, Ito, A, Jiménez, JA and Brabec, J (2010) Multiplex PCR for differential identification of broad tapeworms (Cestoda: Diphyllobothrium) infecting humans. Journal of Clinical Microbiology 48, 3111–3116.CrossRefGoogle ScholarPubMed
Wikgren, BJP and Gustafsson, MKS (1965) The chromosomes of somatic cells of three Diphyllobothrium species, with notes on the mode of cell division. Acta Academiae Aboensis Serie B 25, 1–12.Google Scholar
Winterfeld, G, Ley, A, Hoffmann, MH, Paule, J and Röser, M (2019) Dysploidy and polyploidy trigger strong variation of chromosome numbers in the prayer-plant family (Marantaceae). Plant Systematics and Evolution 306, 36.CrossRefGoogle Scholar
Wolcott, GB (1959) The chromosomes of Diphyllobothrium ursi. Journal of Parasitology 45, 378.CrossRefGoogle Scholar
Zadesenets, KS, Vizoso, DB, Schlatter, A, Konopatskaia, ID, Berezikov, E, Schärer, L and Rubtsov, NB (2016) Evidence for karyotype polymorphism in the free-living flatworm, Macrostomum lignano, a model organism for evolutionary and developmental biology. PLoS ONE 11, 10.CrossRefGoogle Scholar
Zrzavá, M, Hladová, I, Dalíková, M, Šíchová, J, Ounap, E, Kubíčková, S and Marec, F (2018) Sex chromosomes of the iconic moth Abraxas grossulariata (Lepidoptera, Geometridae) and its congener A. sylvata. Genes 9, 279.CrossRefGoogle ScholarPubMed