Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-13T12:43:03.421Z Has data issue: false hasContentIssue false
  • English
  • Français

Reduced infectivity in Himasthla elongata (Trematoda, Himasthlidae) cercariae with deviant photoreaction

Published online by Cambridge University Press:  26 February 2020

Anna Solovyeva Open the ORCID record for Anna Solovyeva [Opens in a new window] ,
Kirill Nikolaev ,
Egor Lebedev ,
Edokiia Potolytsina ,
Nickolay Galaktionov  and
Ivan Levakin
Anna Solovyeva*
Affiliation:
Laboratory of Non-Coding DNA, Institute of Cytology of Russian Academy of Sciences, Laboratory of parasitic worms and protists, Zoological Institute of Russian Academy of Sciences, St Petersburg, Russia
Kirill Nikolaev
Affiliation:
Laboratory of parasitic worms and protists, Zoological Institute of Russian Academy of Sciences, St.Petersburg, Russia
Egor Lebedev
Affiliation:
School of Natural Sciences, Far Eastern State University, Vladivostok, Russia
Edokiia Potolytsina
Affiliation:
Department of Molecular Medicine, University of Oslo, Oslo, Norway
Nickolay Galaktionov
Affiliation:
Department of Cytology and Histology, St. Petersburg State University, St.Petersburg, Russia
Ivan Levakin
Affiliation:
Laboratory of parasitic worms and protists, Zoological Institute of Russian Academy of Sciences, St. Petersburg, Russia
*
Author for correspondence: A. Solovyeva, E-mail: orcinuca@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Digenean larvae of hermaphroditic generation – cercariae – are known to be polymorphic at genetic and behavioural levels. Cercariae arise as a result of parthenogenetic reproduction of intramolluscan stages, and represent a clone if a snail was infected with a single miracidium. Here we investigated cercarial clones of Himasthla elongata – namely, the infectivity of cercariae with normal (negative) and deviant (positive) photoreaction. In our study, most H. elongata clones showed intraclonal variance in their response to light. The proportion of photopositive cercariae ranged between 0.2% and 60% in different H. elongata clones. Photopositive larvae demonstrated significantly reduced rates of encystment in Mytilus edulis haemolymph in vitro and in young mussels. We discuss the possible mechanisms behind intraclonal variations, such as non-specific genomic rearrangements.

Keywords

Himasthla elongataclonal polymorphismphotoreaction
Type
Short Communication
Information
Journal of Helminthology , Volume 94 , 2020 , e129
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bayne, CJ and Grevelding, CG (2003) Cloning of Schistosoma mansoni sporocysts in vitro and detection of genetic heterogeneity among individuals within clones. The Journal of Parasitology 89, 1056–1060.CrossRefGoogle ScholarPubMed
Combes, C, Fournier, A, Monѐ, H and Thѐron, A (1994) Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109, S3–S13.CrossRefGoogle ScholarPubMed
Combes, C, Bartoli, P and Theron, A (2002) Trematode transmission strategies. pp. 1–12in Lewis, EE, Campbell, JF and Sukhdeo, MVK (Eds) The behavioural ecology of parasites. Wallingford, New York, CABI Publ.Google Scholar
Cosseau, C, Azzi, A, Rognon, A, Boissier, J, Gourbière, S, Roger, E, Mitta, G and Grunau, C (2010) Epigenetic and phenotypic variability in populations of Schistosoma mansoni– a possible kick-off for adaptive host/parasite evolution. Oikos 119, 669–678.CrossRefGoogle Scholar
Dobrovolskij, AA and Ataev, GL (2003) The nature of reproduction of trematodes rediae and sporocysts. pp. 249–272in Combes, C and Jourdane, J (Eds) Hommage à Louis Euzet – taxonomy, ecology, and evolution of metazoan parasites. Perpignan, France, Presses Universitaires de Perpignan.Google Scholar
Fedoroff, NV (2012) Transposable elements, epigenetics, and genome evolution. Science 338, 758–767.CrossRefGoogle ScholarPubMed
Galaktionov, KV and Bustnes, JO (1999) Distribution patterns of marine bird digenean larvae in periwinkles along the southern Barents Sea coast. Diseases of Aquatic Organisms 37, 221–230.CrossRefGoogle Scholar
Galaktionov, KV and Dobrovolskij, AA (2003) The biology and evolution of trematodes. An essay on the biology, morphology, life cycles, transmissions, and evolution of digenetic trematodes. 592 pp. Boston, Dordrecht & London, Kluwer Academic.Google Scholar
Galaktionov, NK, Solovyeva, AI, Fedorov, AV and Podgornaya, OI (2014) Trematode Himasthla elongata mariner element (Hemar): structure and applications. The Journal of Experimental Zoology – B: Molecular and Developmental Evolution 322, 142–155.CrossRefGoogle ScholarPubMed
Galaktionov, NK, Podgornaya, OI, Strelkov, PP and Galaktionov, KV (2016) Genomic diversity of cercarial clones of Himasthla elongata (Trematoda; Echinostomatidae) determined with AFLP technique. Parasitology Research 115, 4587–4593.CrossRefGoogle ScholarPubMed
Gorbushin, AM and Levakin, IA (2005) Encystment in vitro of the cercariae Himasthla elongata (Trematoda: Echinostomatidae). Journal of Evolutionary Biochemistry and Physiology 41, 428–436.CrossRefGoogle Scholar
Haas, W (1994) Physiological analysis of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109, S15–S29.CrossRefGoogle Scholar
Haas, W (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106, 349–364.CrossRefGoogle ScholarPubMed
Khalturin, KV, Mikhaylova, NI and Granovich, AI (2000) Genetic heterogeneity of natural populations of parthenites Microphallus piriformes and M. pygmaeus (Trematoda: Microphallidae). Parazitologiya 34, 486–500 (in Russian).Google Scholar
Koehler, AV, Springer, YP, Keeney, DB and Poulin, R (2011) Intra- and interclonal phenotypic and genetic variability of the trematode Maritrema novaezealandensis. Biological Journal of the Linnean Society 103, 106–116.CrossRefGoogle Scholar
Korsunenko, A, Chrisanfova, G, Arifov, A, Ryskov, A and Semyenova, S (2013) Characterization of randomly amplified polymorphic DNA (RAPD) fragments revealing clonal variability in cercariae of avian schistosome Trichobilharzia szidati (Trematoda: Schistosomatidae). Open Journal of Genetics 3, 141–158.CrossRefGoogle Scholar
Kulatchkova, VG (1985) Parasites of blue mussels – the aquaculture object in the White Sea. pp. 88–97in Lukanin, VV (Ed) Investigation of the blue mussel of the White Sea. Leningrad, Zoological Institute (in Russian).Google Scholar
Kuris, AM and Lafferty, KD (1994) Community structure: larval trematodes in snail hosts. Annual Review of Ecology and Systematics 25, 189–217.CrossRefGoogle Scholar
Levakin, IA, Nikolaev, KE and Galaktionov, KV (2013a) Long-term variation in trematode (Trematoda, Digenea) component communities associated with intertidal gastropods is linked to abundance of final hosts. Hydrobiologia 706, 103–118.CrossRefGoogle Scholar
Levakin, IA, Losev, EA, Nikolaev, КE and Galaktionov, KV (2013b) In vitro encystment of Himasthla elongata cercariae (Digenea, Echinostomatidae) in the hemolymph of blue mussels Mytilus edulis as a tool for assessing cercarial infectivity and molluscan susceptibility. Journal of Helminthology 87, 180–188.CrossRefGoogle Scholar
McCarthy, AM (1999) Phototactic responses of the cercaria of Echinoparyphium recurvatum during phases of sub-maximal and maximal infectivity. Journal of Helminthology 73, 63–65.CrossRefGoogle Scholar
Nikolaev, KE, Prokofiev, VV, Levakin, IA and Galaktionov, KV (2017) How the position of mussels at the intertidal lagoon affects their infection with the larvae of parasitic flatworms (Trematoda: Digenea): a combined laboratory and field experimental study. Journal of Sea Research 128, 32–40.CrossRefGoogle Scholar
Platt, TR and Dowd, RM (2012) Age-related change in phototaxis by cercariae of Echinostoma caproni (Digenea: Echinostomatidae). Comparative Parasitology 79, 1–4.CrossRefGoogle Scholar
Prokofiev, VV (1996) The effect of temperature and light on the daily emission dynamics of the cercariae Podocotyle atomon (Trematoda: Opecoelidae). Parazitologiya 30, 32–38 (in Russian).Google Scholar
Prokofiev, VV (1997) Reactions to the light of the littoral trematodes Cryptocotyle sp. (Heterophyidae) and Maritrema subdolum (Microphallidae). Zoologicheskii Zhurnal 76, 275–280 (in Russian).Google Scholar
Prokofiev, VV (2001) Reactions to the light of the littoral trematode Renicola thaidus (Trematoda: Renicolidae). Parazitologiya 35, 429–435 (in Russian).Google Scholar
Prokofiev, VV (2002) Vertical migration of cercariae of the littoral trematode Renicola thaidus (Trematoda: Renicolidae) in the water layer. Parazitologiya 36, 314–321 (in Russian).Google Scholar
Prokofiev, VV (2003) Vertical distribution patterns of trematode cercariae Cryptocotyle concavum (Heterophyidae) and Maritrema subdolum (Microphallidae) in the water column. Parazitologiya 37, 207–215 (in Russian).Google Scholar
Prokofiev, VV (2006) Strategies of the animal host infection with trematode cercariae: an attempt of analysis in marine coastal and lake ecosystems of northwestern Russia. 545 pp. Dissertation, Zoological Institute of the Russian Academy of Sciences, St Petersburg (in Russian).Google Scholar
Prokofiev, VV and Galaktionov, KV (2009) Strategies of search behaviour in trematode cercariae. Proceedings of the Zoological Institute RAS 313, 308–318 (in Russian).Google Scholar
Prokofiev, VV, Levakin, IA, Losev, EA, Zavirsky, YV and Galaktionov, КV (2011) Clonal variability in expression of geo- and photoorientation in cercariae of Himasthla elongata (Trematoda: Echinostomatidae). Parazitologiya 45, 345–357 (in Russian).Google Scholar
Rea, JG and Irwin, SWB (1994) The ecology of host-finding behaviour and parasite transmission: past and future perspectives. Parasitology 109, S31–S39.CrossRefGoogle ScholarPubMed
Semyenova, SK, Chrisanfova, GG, Fillipova, EK, Beer, SA, Voronin, MV and Ryskov, AP (2005) Individual and population variation in cercariae of bird schistosomes of the Trichobilharzia ocellata species group as revealed with the polymerase chain reaction. Russian Journal of Genetics 41, 12–16.CrossRefGoogle Scholar
Slotkin, RK and Martienssen, R (2007) Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics 8, 272–285.CrossRefGoogle ScholarPubMed
Solovyeva, AI, Galaktionov, NK and Podgornaya, OI (2013) LINE class retroposon is the component of the DNA polymorphic fragments pattern of trematode Himasthla elongata parthenitae. Cell and Tissue Biology 7, 563–572.CrossRefGoogle Scholar
Sukhdeo, MVK and Sukhdeo, SC (2004) Trematode behaviours and the perceptual worlds of parasites. Canadian Journal of Zoology 82, 292–315.CrossRefGoogle Scholar
Supplementary material: File

Solovyeva et al. supplementary material

Table S1

Download Solovyeva et al. supplementary material(File)
File 14.5 KB