First Immunodetection of Sensory and Nervous Systems of Parasitic Larvae (Glochidia) of Freshwater Bivalve Nodularia douglasiae
Most freshwater mussels have an unusual life cycle that requires host fish species for larval (glochidia) development and dispersal. Glochidia have a unique morphological structure that adapts to parasitic lifestyles and survival. The morphology of the glochidial shells of most Unionoidea, a group o...
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Frontiers Media S.A.
2022-04-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2022.879540/full |
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| author | Viktoria E. Nikishchenko Elena M. Sayenko Vyacheslav A. Dyachuk |
| author_facet | Viktoria E. Nikishchenko Elena M. Sayenko Vyacheslav A. Dyachuk |
| author_sort | Viktoria E. Nikishchenko |
| collection | DOAJ |
| description | Most freshwater mussels have an unusual life cycle that requires host fish species for larval (glochidia) development and dispersal. Glochidia have a unique morphological structure that adapts to parasitic lifestyles and survival. The morphology of the glochidial shells of most Unionoidea, a group of freshwater bivalve mollusks, has been studied in detail using light and scanning electron microscopy. This study summarizes our data on the glochidia shell morphology of the Asian mussel Nodularia douglasiae from two localities in the Primorsky Territory, the Russian Far East. In contrast to the shell morphology of glochidia, little is known about the neurodevelopment of the Unionoidea. Herein, we first demonstrate that the structures of the sensory, muscle, and nervous systems of the glochidia larvae of N. douglasiae differ dramatically from those of the comparable larval systems of marine bivalve species, as revealed through alpha-acetylated tubulin, serotonin (5-HT), and FMRFamide antibodies as well as phalloidin for detection of F-actin and whole-mount confocal microscopy. We found that the glochidia sensory system included four pairs of tubulin-lir multicilia hair cells. Non-ciliar tubulin-lir cells synthesize the neuropeptide FMRFamide and are identified as afferent neurons collecting information from peripheral tubulin-lir hair sensory cells to nervous regulators. The glochidia’s muscular system was represented by a smooth adductor, retractors, and minor muscle bundles associated with the shell and visceral organs. The 5-HT-lir larval system is arranged most simply and consists of two immunopositive neurons innervating the adductor. The FMRFamide-lir system is more complicated and consists of several neuronal centers comprising neuronal bodies and their neurites in different areas of the larva. The FMRFamide-lir neurons are closely associated with sensory hair cells, and others, together with 5-HT-lir neurons, may be involved in the anlagen of adult ganglia. Thus, the nervous system of N. douglasiae glochidia is drastically different from other mollusks and lophotrochozoans because of the absence of an apical organ and the location and composition of FMRFamide and 5-HT cells. Morphological, molecular, and behavioral investigations of Unionoidea taxa need to be further conducted to investigate the parasite-host relationship, nerve-dependent regulation of parasite behavior, and evolution of mollusks. |
| first_indexed | 2024-12-17T06:56:33Z |
| format | Article |
| id | doaj.art-27f5e2eedd2b43ed9b76d7c12d90b815 |
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| language | English |
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| publishDate | 2022-04-01 |
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| spelling | doaj.art-27f5e2eedd2b43ed9b76d7c12d90b8152022-12-21T21:59:25ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2022-04-011310.3389/fphys.2022.879540879540First Immunodetection of Sensory and Nervous Systems of Parasitic Larvae (Glochidia) of Freshwater Bivalve Nodularia douglasiaeViktoria E. Nikishchenko0Elena M. Sayenko1Vyacheslav A. Dyachuk2A. V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, RussiaFederal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, RussiaA. V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, RussiaMost freshwater mussels have an unusual life cycle that requires host fish species for larval (glochidia) development and dispersal. Glochidia have a unique morphological structure that adapts to parasitic lifestyles and survival. The morphology of the glochidial shells of most Unionoidea, a group of freshwater bivalve mollusks, has been studied in detail using light and scanning electron microscopy. This study summarizes our data on the glochidia shell morphology of the Asian mussel Nodularia douglasiae from two localities in the Primorsky Territory, the Russian Far East. In contrast to the shell morphology of glochidia, little is known about the neurodevelopment of the Unionoidea. Herein, we first demonstrate that the structures of the sensory, muscle, and nervous systems of the glochidia larvae of N. douglasiae differ dramatically from those of the comparable larval systems of marine bivalve species, as revealed through alpha-acetylated tubulin, serotonin (5-HT), and FMRFamide antibodies as well as phalloidin for detection of F-actin and whole-mount confocal microscopy. We found that the glochidia sensory system included four pairs of tubulin-lir multicilia hair cells. Non-ciliar tubulin-lir cells synthesize the neuropeptide FMRFamide and are identified as afferent neurons collecting information from peripheral tubulin-lir hair sensory cells to nervous regulators. The glochidia’s muscular system was represented by a smooth adductor, retractors, and minor muscle bundles associated with the shell and visceral organs. The 5-HT-lir larval system is arranged most simply and consists of two immunopositive neurons innervating the adductor. The FMRFamide-lir system is more complicated and consists of several neuronal centers comprising neuronal bodies and their neurites in different areas of the larva. The FMRFamide-lir neurons are closely associated with sensory hair cells, and others, together with 5-HT-lir neurons, may be involved in the anlagen of adult ganglia. Thus, the nervous system of N. douglasiae glochidia is drastically different from other mollusks and lophotrochozoans because of the absence of an apical organ and the location and composition of FMRFamide and 5-HT cells. Morphological, molecular, and behavioral investigations of Unionoidea taxa need to be further conducted to investigate the parasite-host relationship, nerve-dependent regulation of parasite behavior, and evolution of mollusks.https://www.frontiersin.org/articles/10.3389/fphys.2022.879540/fullfreshwater molluskglochidiaparasitic larvaehair cellneurotransimitterserotonin |
| spellingShingle | Viktoria E. Nikishchenko Elena M. Sayenko Vyacheslav A. Dyachuk First Immunodetection of Sensory and Nervous Systems of Parasitic Larvae (Glochidia) of Freshwater Bivalve Nodularia douglasiae Frontiers in Physiology freshwater mollusk glochidia parasitic larvae hair cell neurotransimitter serotonin |
| title | First Immunodetection of Sensory and Nervous Systems of Parasitic Larvae (Glochidia) of Freshwater Bivalve Nodularia douglasiae |
| title_full | First Immunodetection of Sensory and Nervous Systems of Parasitic Larvae (Glochidia) of Freshwater Bivalve Nodularia douglasiae |
| title_fullStr | First Immunodetection of Sensory and Nervous Systems of Parasitic Larvae (Glochidia) of Freshwater Bivalve Nodularia douglasiae |
| title_full_unstemmed | First Immunodetection of Sensory and Nervous Systems of Parasitic Larvae (Glochidia) of Freshwater Bivalve Nodularia douglasiae |
| title_short | First Immunodetection of Sensory and Nervous Systems of Parasitic Larvae (Glochidia) of Freshwater Bivalve Nodularia douglasiae |
| title_sort | first immunodetection of sensory and nervous systems of parasitic larvae glochidia of freshwater bivalve nodularia douglasiae |
| topic | freshwater mollusk glochidia parasitic larvae hair cell neurotransimitter serotonin |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2022.879540/full |
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