Chromosome analysis and the occurrence of B chromosomes in fish parasite Acanthocephalus anguillae (Palaeacanthocephala: Echinorhynchida)

. 2023 ; 30 () : 44. [epub] 20231023

Jazyk angličtina Země Francie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37870409

Grantová podpora
APVV 18-0467 Agentúra na Podporu Výskumu a Vývoja
2/0093/23 Agentúra Ministerstva Školstva, Vedy, Výskumu a Športu SR
SAV-AV ČR-21-03 Slovenská Akadémia Vied
APP0352 Slovenská Akadémia Vied

The cytogenetics of Acanthocephala is a neglected area in the study of this group of endoparasites. Chromosome number and/or karyotypes are known for only 12 of the 1,270 described species, and molecular cytogenetic data are limited to rDNA mapping in two species. The standard karyological technique and mapping of 18S rRNA and H3 histone genes on the chromosomes of Acanthocephalus anguillae individuals from three populations, one of which originated from the unfavorable environmental conditions of the Zemplínska Šírava reservoir in eastern Slovakia, were applied for the first time. All specimens had 2n = 7/8 (male/female); n = 1m + 1m-sm + 1a + 1a (X). Fluorescence in situ hybridization (FISH) revealed three loci of 18S rDNA on two autosomes and dispersion of H3 histone genes on all autosomes and the X chromosome. In addition to the standard A chromosome set, 34% of specimens from Zemplínska Šírava possessed a small acrocentric B chromosome, which was always found to be univalent, with no pairing observed between the B chromosome and the A complement. The B chromosome had a small amount of heterochromatin in the centromeric and telomeric regions of the chromosomal arms and showed two clusters of H3 genes. It is well known that an environment permanently polluted with chemicals leads to an increased incidence of chromosomal rearrangements. As a possible scenario for the B chromosome origin, we propose chromosomal breaks due to the mutagenic effect of pollutants in the aquatic environment. The results are discussed in comparison with previous chromosome data from Echinorhynchida species.

TITLE: Analyse chromosomique et présence de chromosomes B chez le parasite de poisson Acanthocephalus anguillae (Palaeacanthocephala, Echinorhynchida). ABSTRACT: La cytogénétique des Acanthocephala est un domaine négligé dans l’étude de ce groupe d’endoparasites. Le nombre de chromosomes et/ou les caryotypes ne sont connus que pour 12 des 1270 espèces décrites, et les données cytogénétiques moléculaires se limitent à la cartographie de l’ADNr chez deux espèces. La technique caryologique standard et la cartographie des gènes de l’ARNr 18S et de l’histone H3 ont été appliquées pour la première fois sur les chromosomes d’individus d’Acanthocephalus anguillae provenant de trois populations, dont l’une dans les conditions environnementales défavorables du réservoir de Zemplínska Šírava dans l’est de la Slovaquie. Tous les spécimens avaient 2n = 7/8 (mâle/femelle); n = 1m + 1m-sm + 1a + 1a (X). La technique FISH a révélé trois locus d’ADNr 18S sur deux autosomes et une dispersion des gènes de l’histone H3 sur tous les autosomes et sur le chromosome X. En plus de l’ensemble standard de chromosomes A, 34 % des spécimens de Zemplínska Šírava possédaient un petit chromosome B acrocentrique, qui s’est toujours révélé univalent, sans aucun appariement observé entre le chromosome B et le complément A. Le chromosome B avait une petite quantité d’hétérochromatine dans les régions centromériques et télomériques des bras chromosomiques et présentait deux groupes de gènes H3. Il est bien connu qu’un environnement pollué en permanence par des produits chimiques entraîne une incidence accrue de réarrangements chromosomiques. Comme scénario possible pour l’origine du chromosome B, nous proposons des cassures chromosomiques dues à l’effet mutagène des polluants du milieu aquatique. Les résultats sont discutés en comparaison avec les données chromosomiques précédentes des espèces d’Echinorhynchida.

Zobrazit více v PubMed

Amin OM. 2013. Classification of the Acanthocephala. Folia Parasitologica, 60, 273–305. PubMed

Baršiené J. 1993. The chromosome sets of trematodes. Parazitologiya, 27, 336–353. PubMed

Bombarová M, Marec F, Nguyen P, Špakulová M. 2007. Divergent location of ribosomal genes in chromosomes of fish thorny-headed worms, Pomphorhynchus laevis and Pomphorhynchus tereticollis (Acanthocephala). Genetica, 131, 141–149. PubMed

Bombarová M, Vítková M, Špakulová M, Koubková B. 2009. Telomere analysis of platyhelminths and acanthocephalans by FISH and Southern hybridization. Genome, 52, 897–903. PubMed

Bone LW. 1974. The chromosomes of Leptorhynchoides thecatus (Acanthocephala). Journal of Parasitology, 60, 818. PubMed

Bone LW. 1974. The chromosomes of Neoechinorhynchus cylindratus (Acanthocephala). Journal of Parasitology, 60, 731–732.

Brázová T, Miklisová D, Barčák D, Uhrovič D, Šalamún P, Orosová M, Oros M. 2021. Hazardous pollutants in the environment: Fish host-parasite interactions and bioaccumulation of polychlorinated biphenyls. Environmental Pollution, 291, 118175. PubMed

Bueno D, Palacios-Gimenez OM, Cabral-de-Mello DC. 2013. Chromosomal mapping of repetitive DNAs in the grasshopper Abracris flavolineata reveal possible ancestry of the B chromosome and H3 histone spreading. PLoS One, 8, e66532. PubMed PMC

Cabral-de-Mello DC, Marec F. 2021. Universal fluorescence in situ hybridization (FISH) protocol for mapping repetitive DNAs in insects and other arthropods. Molecular Genetics and Genomics, 296, 513–526. PubMed

Cabrero J, López-León M, Teruel M, Camacho JPM. 2009. Chromosome mapping of H3 and H4 histone gene clusters in 35 species of acridid grasshoppers. Chromosome Research, 17, 397–404. PubMed

Camacho JP, Sharbel TF, Beukeboom LW. 2000. B-chromosome evolution. Philosophical Transactions of the Royal Society B: Biological Sciences, 355, 163–178. PubMed PMC

Camacho JPM. 2005. B Chromosomes, in The Evolution of the Genome. Gregory TR, Editor. Elsevier Academic Press. p. 223–286.

Cavalcante MG, Souza LF, Vicari MR, Matos de Bastos CE, Viana de Sousa J, Nagamachi CY, Pieczarka JC, Martins C, Rodrigues Noronha RC. 2020. Molecular cytogenetics characterization of Rhinoclemmys punctularia (Testudines, Geoemydidae) and description of a Gypsy-H3 association in its genome. Gene, 738, 144477. PubMed

Chmúrčiaková N, Kašný M, Orosová M. 2020. Cytogenetics of Eudiplozoon nipponicum (Monogenea, Diplozoidae): Karyotype, spermatocyte division and 18S rDNA location. Parasitology International, 76, 102031. PubMed

Dhar MK, Friebe B, Koul AK, Bikram SG. 2002. Origin of an apparent B chromosome by mutation, chromosome fragmentation and specific DNA sequence amplification. Chromosoma, 111, 332–340. PubMed

Dobigny G, Terence JF, Robinson J, Volobouev V. 2004. Cytogenetics and cladistics. Systematic Biology, 53, 470–484. PubMed

Guerra Dos Santos. 1986. Reviewing the chromosomes nomenclature of Levan et al. Revista Brasileira de Genetica, 9, 741–743.

Feldberg E, Porto JIR, Alves-Brinn MN, Mendonça MNC, Benzaquem DC. 2004. B chromosomes in Amazonian cichlid species. Cytogenetic and Genome Research, 106, 195–198. PubMed

Fontana F, Dezfuli BS, Benvenuti M. 1993a. The chromosome complement of Leptorhyncoides plagicephalus (Westrumb, 1821), (Acanthocephala: Rhadinorhynchidae). Cytologia, 58, 393–396.

Fontana F, Dezfuli BS, Benvenuti M. 1993b. Somatic and meiotic chromosomes in male and female of Pomphorhynchus laevis Müller, 1776 (Acanthocephala: Pomphorhynchidae). Caryologia, 46, 329–334.

García-Souto D, Pasantes JJ. 2015. Molecular cytogenetics in digenean parasites: Linked and unlinked major and 5S rDNAs, B Chromosomes and karyotype diversification. Cytogenetic and Genome Research, 147, 195–207. PubMed

García-Varela M, Pérez-Ponce de León G, Torre P, Cummings MP, Sarma SSS, Laclette JP. 2000. Phylogenetic relationships of Acanthocephala based on analysis of 18S ribosomal RNA gene sequences. Journal of Molecular Evolution, 50, 532–540. PubMed

García-Varela M, Andrade-Gómez L. 2021. First steps to understand the systematics of Echinorhynchidae Cobbold, 1876 (Acanthocephala), inferred through nuclear gene sequences. Parasitology International, 81, 102264. PubMed

Hamann O. 1891. Monographie der Acanthocephalen (Echinorhynchen). Ihre Entwicklungsgeschichte, Histogenie und Anatomie, nebst Beitragen zur Systematik und Biologie. Jenaische Zeitschrift für Naturwissenschaft, 25, 113–231.

Hejníčková M, Dalíková M, Potocký P, Tammaru T, Trehubenko M, Kubíčková M, Marec F, Zrzavá M. 2021. Degenerated, undifferentiated, rearranged, lost: High variability of sex chromosomes in Geometridae (Lepidoptera) identified by sex chromatin. Cells, 10, 2230. PubMed PMC

Hirai H. 2014. Chromosomal differentiation of schistosomes: What is the message? Frontiers in Genetics, 5, 00301. PubMed PMC

Hirai H, Taguchi T, Saitoh M, Kawanaka M, Sugiyama H, Habe S. 2000. Chromosomal differentiation of the Schistosoma japonicum complex. International Journal for Parasitology, 30, 441–452. PubMed

Huston DC, Cribb TH, Smales LR. 2020. Molecular characterization of acanthocephalans from Australian marine teleosts: proposal of a new family, synonymy of another and transfer of taxa between orders. Systematic Parasitology, 97, 1–23. PubMed

John B. 1957. The chromosomes of zooparasites I. Acanthocephalus ranae (Acanthocephala: Echinorhynchidae). Chromosoma, 8, 730–738. PubMed

Jones AW, Ward HL. 1950. The chromosomes of Macracanthorhynchus hirudinaceous (Pallas). Journal of Parasitology, 36, 86. PubMed

Jones N, Houben A. 2003. B chromosomes in plants: escapees from the A chromosome genome? Trends in Plant Science, 8, 417–423. PubMed

Jones RN. 2018. Transmission and drive involving parasitic B chromosomes. Genes, 9, 388. PubMed PMC

Kellogg EA. 2016. Has the connection between polyploidy and diversification actually been tested? Current Opinion in Plant Biology, 30, 25–32. PubMed

Kennedy CR. 2006. Ecology of the Acanthocephala, 1st edn. Cambridge University Press.

Košková E, Špakulová M, Koubková B, Reblánová M, Orosová M. 2011. Comparative karyological analysis of four diplozoid species (Monogenea, Diplozoidae), gill parasites of cyprinid fishes. Parasitology Research, 108, 935–941. PubMed

Levan A, Fredga K, Sandberg A. 1964. Nomenclature for centromere position on chromosomes. Hereditas, 52, 201–220.

Liehr T. 2021. Molecular cytogenetics in the era of chromosomics and cytogenomic approaches. Frontiers in Genetics, 12, 720507. PubMed PMC

Lisitsyna OI. 2019. Fauna of Ukraine, vol 31. Acanthocephala. Kiev. p. 223.

Milani D, Ruiz-Ruano FJ, Camacho JPM, Cabral-de-Mello DC. 2021. Out of patterns, the euchromatic B chromosome of the grasshopper Abracris flavolineata is not enriched in high-copy repeats. Heredity, 127, 475–483. PubMed PMC

Molbert N, Alliot F, Leroux-Coyau M, Médoc V, Biard C, Meylan S, Jacquin L, Santos R, Goutte A. 2020. Potential benefits of acanthocephalan parasites for chub hosts in polluted environments. Environmental Science & Technology, 54, 5540–5549. PubMed

Mutafova T, Nedeva I. 1988. Oogenesis and spermatogenesis of Pomphorhynchus laevis (Müller, 1776) (Acanthocephala: Pomphorhynchidae). Khelminthologyia, 25, 23–28.

Mutafova T, Nedeva I, Kanev I. 1997. Chromosomes of Acanthocephalus lucii. Journal of Helminthology, 71, 261–262.

Oliveira NL, Cabral-de-Mello DC, Rocha MF, Loreto V, Martins C. 2011. Chromosomal mapping of rDNAs and H3 histone sequences in the grasshopper Rhammatocerus brasiliensis (Acrididae, Gomphocerinae): extensive chromosomal dispersion and co-localization of 5S rDNA/H3 histone clusters in the A complement and B chromosome. Molecular Cytogenetics, 4, 24. PubMed PMC

Orosová M, Špakulová M. 2018. Tapeworm chromosomes: their value in systematics with instructions for cytogenetic study. Folia Parasitologica, 65, 001. PubMed

Orosová M, Provazníková I, Xi BW, 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. PubMed

Orosová M, Marková A, Marec F, Barčák D, Brázová T, Oros M. 2022. New cytogenetic data on Caryophyllaeus laticeps and Paracaryophyllaeus gotoi, parasites of evolutionary interest. Parasitology, 149, 1094–1105. PubMed PMC

Parenti U, Antoniotti L, Beccio C. 1965. Sex ratio and sex digamety in Echinorhynchus truttae. Experientia, 21, 657–658. PubMed

Park GM, Im K, Huh S, Yong TS. 2000. Chromosomes of the liver fluke, Clonorchis sinensis. Korean Journal of Parasitology, 38, 201–206. PubMed PMC

Petkevičiūtė R. 1996. A chromosome study of Schistocephalus solidus (Müller, 1776) (Cestoda: Pseudophyllidea). Systematic Parasitology, 33, 183–186.

Petkevičiūtė R, Stunženas Stanevičiūtė G. 2011. Clarification of the systematic position of Cercariaeum crassum Wesenberg-Lund, 1934 (Digenea), based on karyological analysis and DNA sequences. Journal of Helminthology, 86, 293–301. PubMed

Perazzo GX, Noleto RB, Vicari MR, Gava A, Cestari MM. 2018. B chromosome polymorphism in South American cichlid. Neotropical Biodiversity, 4, 3–9.

Percie du Sert N, Hurst V, Ahluwalia A, Alam S, Avey MT, Baker M, Browne WJ, Clark A, Cuthill IC, Dirnagl U, Emerson M, Garner P, Holgate ST, Howells DW, Karp NA, Lazic SE, Lidster K, MacCallum CJ, Macleod M, Pearl EJ, Petersen OH, Rawle F, Reynolds P, Rooney K, Sena ES, Silberberg SD, Steckler T, Würbel H. 2020. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biology, 18, e3000410. PubMed PMC

Perrot-Minnot MJ. 2004. Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). International Journal for Parasitology, 34, 45–54. PubMed

Perrot-Minnot M-J, Cozzarolo C-S, Amin O, Barčák D, Bauer A, Filipović Marijić V, García-Varela M, Servando Hernández-Orts J, Le Yen TT, Nachev M, Orosová M, Rigaud T, Šariri S, Wattier R, Reyda F, Sures B. 2023. Hooking the scientific community on thorny-headed worms: interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala. Parasite, 30, 23. PubMed PMC

Pucci MB, Nogaroto V, Moreira-Filho O, Vicari MR. 2018. Dispersion of transposable elements and multigene families: Microstructural variation in Characidium (Characiformes: Crenuchidae) genomes. Genetics and Molecular Biology, 41, 585–592. PubMed PMC

Rábová M, Volker M, Pelikánová Š, Ráb P. 2015. Sequential chromosome bandings in fishes, in FISH cytogenetic techniques, ray-fin fishes and chondrichthyans. Ozouf-Costaz C, Pisano E, Foresti F, Toledo LFA, Editors. CRC Press: USA. p. 66–73.

Raskina O, Barber JC, Nevo E, Belyayev A. 2008. Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes. Cytogenetic and Genome Research, 120, 351–357. PubMed

Reblánová M, Špakulová M, Orosová M, Králová-Hromadová I, Bazsalovicsová E. 2011. A comparative study of karyotypes and chromosomal location of rDNA genes in important liver flukes Fasciola hepatica and Fascioloides magna (Trematoda: Fasciolidae). Parasitology Research, 109, 1021–1028. PubMed

Redmond AK, Casey D, Gundappa MK, Macqueen DJ, McLysaght A. 2023. Independent rediploidization masks shared whole genome duplication in the sturgeon-paddlefish ancestor. Nature Communications, 14, 2879. PubMed PMC

Ribas TFA, Pieczarka JC, Griffin DK, Kiazim LG, Nagamachi CY, O’Brien PCM, Ferguson-Smith MA, Yang F, Aleixo A, O’Connor RE. 2021. Analysis of multiple chromosomal rearrangements in the genome of Willisornis vidua using BAC-FISH and chromosome painting on a supposed conserved karyotype. BMC Ecology and Evolution, 21, 34. PubMed PMC

Robinson ES. 1964. Chromosome morphology and behavior in Macracanthorhynchus hirudinaceus. Journal of Parasitology, 50, 694–697. PubMed

Robinson ES. 1965. The chromosomes of Moniliformis dubius (Acanthocephala). Journal of Parasitology, 51, 430–432. PubMed

Roy V, Monti-Dedieu L, Chaminade N, Siljak-Yakovlev S, Aulard S, Lemeunier F, Montchamp-Moreau C. 2005. Evolution of the chromosomal location of rDNA genes in two Drosophila species subgroups: ananassae and melanogaster. Heredity, 94, 388–395. PubMed

Schubert I. 1984. Mobile nucleolus organizing regions (NORs) in Allium (Liliaceae S-Lat)-inferences from the specifity of silver staining. Plant Systematics and Evolution, 144, 291–305.

Stanevičiũté G, Kiseliené V. 2001. Chromosome studies of Ichthyocotylurus platycephalus (Creplin, 1825) Odening 1969 with description of triploid variant and comparative karyology of the genus Ichthyocotylurus. Parasite, 8, 137–145. PubMed

Sures B, Nachev M, Selbach C, Marcogliese DJ. 2017. Parasite responses to pollution: what we know and where we go in ‘Environmental Parasitology’. Parasites & Vectors, 10, 65. PubMed PMC

Šalgovičová D, Zmetáková Z. 2006. Polychlorinated biphenyls in muscle tissue of freshwater fish in East Slovakia. Journal of Food and Nutrition Research, 45, 171–178.

Špakulová M, Kráľová-Hromadová I, Dudiňák V, Reddy PV. 2002. Karyotype of Acanthocephalus lucii: the first record of supernumerary chromosomes in thorny-headed worms. Parasitology Research, 8, 778–780. PubMed

Špakulová M, Cassanova JC. 2004. Current knowledge on B chromosomes in natural populations of helminth parasites: a review. Cytogenetic and Genome Research, 106, 222–229. PubMed

Špakulová M, Orosová M, Mackiewicz JS. 2011. Cytogenetics and chromosomes of the tapeworms (Platyhelminthes, Cestoda). Advances in Parasitology, 74, 177–230. PubMed

Štundlová J, Šmíd J, Nguyen P, Šťáhlavský P. 2019. Cryptic diversity and dynamic chromosome evolution in Alpine scorpions (Euscorpiidae: Euscorpius). Molecular and Phylogenetic Evolution, 134, 152–163. PubMed

Teruel M, Cabrero J, Perfectti F, Camacho JP. 2010. B chromosome ancestry revealed by histone genes in the migratory locust. Chromosoma, 119, 217–225. PubMed

Traut W, Szczepanowski M, Vítková M, Opitz C, Marec F, Zrzavý J. 2007. The telomere repeat motif of basal Metazoa. Chromosome Research, 15, 371–382. PubMed

Traldi JB, Ziemniczak K, de Fátima Martinez J, Blanco DR, Lui RL, Schemberger MO, Nogaroto V, Moreira-Filho O, Vicari MR. 2019. Chromosome mapping of H1 and H4 histones in Parodontidae (Actinopterygii: Characiformes): Dispersed and/or co-opted transposable elements? Cytogenetic and Genome Research, 158, 106–113. PubMed

Turčeková L, Hanzelová V, Špakulová M. 2002. Concentration of heavy metals in perch and its endoparasites in the polluted water reservoir in Eastern Slovakia. Helminthologia, 39, 76–80.

Von-Voss H. 1910. Beitrag zur Kenntnis der Eireifung bei den Acanthocephalen. Archiv für Zellforschung, 5, 430–448.

Walton AC. 1959. Some parasites and their chromosomes. Journal of Parasitology, 45, 1–20. PubMed

Yoshido A, Sahara K, Marec F, Matsuda Y. 2011. Step-by-step evolution of neo-sex chromosomes in geographical populations of wild silkmoths, Samia cynthia ssp. Heredity, 106, 614–624. PubMed PMC

Yoshido A, Šíchová J, Pospíšilová K, Nguyen P, Šafář J, Provazník J, Voleníková A, Vila R, Marec F. 2020. Evolution of multiple sex-chromosomes associated with dynamic genome reshuffling in Leptidea wood-white butterflies. Heredity, 125, 138–154. PubMed PMC

Yuuta M, Kazuko KT. 2018. Significance of whole-genome duplications on the emergence of evolutionary novelties. Briefings in Functional Genomics, 17, 329–338. PubMed

Zadesentes KS, Katokhin AK, Mordvinov VA, Rubtsov NB. 2012. Comparative cytogenetics of opisthorchid species (Trematoda, Opisthorchiidae). Parasitology International, 61, 87–89. PubMed

Zhao TY, Yang RJ, Lü L, Ru SS, Wayland MT, Chen HX, Li YH, Li L. 2023. Phylomitogenomic analyses provided further evidence for the resurrection of the family Pseudoacanthocephalidae (Acanthocephala: Echinorhynchida). Animals, 13, 1256. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...