Proliferating activity in a bryozoan lophophore
Bryozoans are small benthic colonial animals; their colonies consist of zooids which are composed of a cystid and polypide. According to morphological and molecular data, three classes of bryozoans are recognized: Phylactolaemata, Gymnolaemata and Stenolaemata. Bryozoans are active suspension feeder...
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PeerJ Inc.
2020-05-01
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| Online Access: | https://peerj.com/articles/9179.pdf |
| _version_ | 1827607325262741504 |
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| author | Natalia Shunatova Ilya Borisenko |
| author_facet | Natalia Shunatova Ilya Borisenko |
| author_sort | Natalia Shunatova |
| collection | DOAJ |
| description | Bryozoans are small benthic colonial animals; their colonies consist of zooids which are composed of a cystid and polypide. According to morphological and molecular data, three classes of bryozoans are recognized: Phylactolaemata, Gymnolaemata and Stenolaemata. Bryozoans are active suspension feeders and their feeding apparatus, the lophophore, is fringed with a single row of ciliated tentacles. In gymnolaemates, the lophophore is bell-shaped and its tentacles may be equal in length (equitentacled lophophores) or some tentacles may be longer than others (obliquely truncated lophophores). In encrusting colonies, polypides with obliquely truncated lophophores usually border specific sites of excurrent water outlets (colony periphery and chimneys) where depleted water has to be removed. It is known that during colony astogeny, colony-wide water currents rearrange: new chimneys are formed and/or location of the chimneys within a given colony changes with time. Such rearrangement requires remodeling of the lophophore shape and lengthening of some tentacles in polypides surrounding water outlets. However, proliferating activity has not been described for bryozoans. Here, we compared the distribution of S-phase and mitotic cells in young and adult polypides in three species of Gymnolaemata. We tested the hypothesis that tentacle growth/elongation is intercalary and cell proliferation takes place somewhere at the lophophore base because such pattern does not interfere with the feeding process. We also present a detailed description of ultrastructure of two parts of the lophophore base: the oral region and ciliated pits, and uncover the possible function of the latter. The presence of stem cells within the ciliated pits and the oral region of polypides provide evidence that both sites participate in tentacle elongation. This confirms the suggested hypothesis about intercalary tentacle growth which provides a potential to alter a lophophore shape in adult polypides according to rearrangement of colony wide water currents during colony astogeny. For the first time deuterosome-like structures were revealed during kinetosome biogenesis in the prospective multiciliated epithelial cells in invertebrates. Tentacle regeneration experiments in Electra pilosa demonstrated that among all epidermal cell types, only non-ciliated cells at the abfrontal tentacle surface are responsible for wound healing. Ciliated cells on the frontal and lateral tentacle surfaces are specialized and unable to proliferate, not even under wound healing. Tentacle regeneration in E. pilosa is very slow and similar to the morphallaxis type. We suggest that damaged tentacles recover their length by a mechanism similar to normal growth, powered by proliferation of cells both within ciliated pits and the oral region. |
| first_indexed | 2024-03-09T06:52:51Z |
| format | Article |
| id | doaj.art-1631c4743d61425b90419d88761d91c1 |
| institution | Directory Open Access Journal |
| issn | 2167-8359 |
| language | English |
| last_indexed | 2024-03-09T06:52:51Z |
| publishDate | 2020-05-01 |
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| spelling | doaj.art-1631c4743d61425b90419d88761d91c12023-12-03T10:16:07ZengPeerJ Inc.PeerJ2167-83592020-05-018e917910.7717/peerj.9179Proliferating activity in a bryozoan lophophoreNatalia Shunatova0Ilya Borisenko1Department of Invertebrate Zoology, Biological Faculty, St. Petersburg State University, St. Petersburg, RussiaDepartment of Embryology, Biological Faculty, St. Petersburg State University, St. Petersburg, RussiaBryozoans are small benthic colonial animals; their colonies consist of zooids which are composed of a cystid and polypide. According to morphological and molecular data, three classes of bryozoans are recognized: Phylactolaemata, Gymnolaemata and Stenolaemata. Bryozoans are active suspension feeders and their feeding apparatus, the lophophore, is fringed with a single row of ciliated tentacles. In gymnolaemates, the lophophore is bell-shaped and its tentacles may be equal in length (equitentacled lophophores) or some tentacles may be longer than others (obliquely truncated lophophores). In encrusting colonies, polypides with obliquely truncated lophophores usually border specific sites of excurrent water outlets (colony periphery and chimneys) where depleted water has to be removed. It is known that during colony astogeny, colony-wide water currents rearrange: new chimneys are formed and/or location of the chimneys within a given colony changes with time. Such rearrangement requires remodeling of the lophophore shape and lengthening of some tentacles in polypides surrounding water outlets. However, proliferating activity has not been described for bryozoans. Here, we compared the distribution of S-phase and mitotic cells in young and adult polypides in three species of Gymnolaemata. We tested the hypothesis that tentacle growth/elongation is intercalary and cell proliferation takes place somewhere at the lophophore base because such pattern does not interfere with the feeding process. We also present a detailed description of ultrastructure of two parts of the lophophore base: the oral region and ciliated pits, and uncover the possible function of the latter. The presence of stem cells within the ciliated pits and the oral region of polypides provide evidence that both sites participate in tentacle elongation. This confirms the suggested hypothesis about intercalary tentacle growth which provides a potential to alter a lophophore shape in adult polypides according to rearrangement of colony wide water currents during colony astogeny. For the first time deuterosome-like structures were revealed during kinetosome biogenesis in the prospective multiciliated epithelial cells in invertebrates. Tentacle regeneration experiments in Electra pilosa demonstrated that among all epidermal cell types, only non-ciliated cells at the abfrontal tentacle surface are responsible for wound healing. Ciliated cells on the frontal and lateral tentacle surfaces are specialized and unable to proliferate, not even under wound healing. Tentacle regeneration in E. pilosa is very slow and similar to the morphallaxis type. We suggest that damaged tentacles recover their length by a mechanism similar to normal growth, powered by proliferation of cells both within ciliated pits and the oral region.https://peerj.com/articles/9179.pdfBryozoaGymnolaemataTentaclesLophophore baseCiliated pitEdU-labeling |
| spellingShingle | Natalia Shunatova Ilya Borisenko Proliferating activity in a bryozoan lophophore PeerJ Bryozoa Gymnolaemata Tentacles Lophophore base Ciliated pit EdU-labeling |
| title | Proliferating activity in a bryozoan lophophore |
| title_full | Proliferating activity in a bryozoan lophophore |
| title_fullStr | Proliferating activity in a bryozoan lophophore |
| title_full_unstemmed | Proliferating activity in a bryozoan lophophore |
| title_short | Proliferating activity in a bryozoan lophophore |
| title_sort | proliferating activity in a bryozoan lophophore |
| topic | Bryozoa Gymnolaemata Tentacles Lophophore base Ciliated pit EdU-labeling |
| url | https://peerj.com/articles/9179.pdf |
| work_keys_str_mv | AT nataliashunatova proliferatingactivityinabryozoanlophophore AT ilyaborisenko proliferatingactivityinabryozoanlophophore |