Movement and storage of nematocysts across development in the nudibranch Berghia stephanieae (Valdés, 2005)
Abstract Background Intracellular sequestration requires specialized cellular and molecular mechanisms allowing a predator to retain and use specific organelles that once belonged to its prey. Little is known about how common cellular mechanisms, like phagocytosis, can be modified to selectively int...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-04-01
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| Series: | Frontiers in Zoology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12983-022-00460-1 |
| _version_ | 1828414930961825792 |
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| author | Jessica A. Goodheart Vanessa Barone Deirdre C. Lyons |
| author_facet | Jessica A. Goodheart Vanessa Barone Deirdre C. Lyons |
| author_sort | Jessica A. Goodheart |
| collection | DOAJ |
| description | Abstract Background Intracellular sequestration requires specialized cellular and molecular mechanisms allowing a predator to retain and use specific organelles that once belonged to its prey. Little is known about how common cellular mechanisms, like phagocytosis, can be modified to selectively internalize and store foreign structures. One form of defensive sequestration involves animals that sequester stinging organelles (nematocysts) from their cnidarian prey. While it has been hypothesized that nematocysts are identified by specialized phagocytic cells for internalization and storage, little is known about the cellular and developmental mechanisms of this process in any metazoan lineage. This knowledge gap is mainly due to a lack of genetically tractable model systems among predators and their cnidarian prey. Results Here, we introduce the nudibranch Berghia stephanieae as a model system to investigate the cell, developmental, and physiological features of nematocyst sequestration selectivity. We first show that B. stephanieae, which feeds on Exaiptasia diaphana, selectively sequesters nematocysts over other E. diaphana tissues found in their digestive gland. Using confocal microscopy, we document that nematocyst sequestration begins shortly after feeding and prior to the formation of the appendages (cerata) where the organ responsible for sequestration (the cnidosac) resides in adults. This finding is inconsistent with previous studies that place the formation of the cnidosac after cerata emerge. Our results also show, via live imaging assays, that both nematocysts and dinoflagellates can enter the nascent cnidosac structure. This result indicates that selectivity for nematocysts occurs inside the cnidosac in B. stephanieae, likely in the cnidophage cells themselves. Conclusions Our work highlights the utility of B. stephanieae for future research, because: (1) this species can be cultured in the laboratory, which provides access to all developmental stages, and (2) the transparency of early juveniles makes imaging techniques (and therefore cell and molecular assays) feasible. Our results pave the way for future studies using live imaging and targeted gene editing to identify the molecular mechanisms involved in nematocyst sequestration. Further studies of nematocyst sequestration in B. stephanieae will also allow us to investigate how common cellular mechanisms like phagocytosis can be modified to selectively internalize and store foreign structures. |
| first_indexed | 2024-12-10T13:35:32Z |
| format | Article |
| id | doaj.art-118705a629ff47a3a9f20e42162f0fc1 |
| institution | Directory Open Access Journal |
| issn | 1742-9994 |
| language | English |
| last_indexed | 2024-12-10T13:35:32Z |
| publishDate | 2022-04-01 |
| publisher | BMC |
| record_format | Article |
| series | Frontiers in Zoology |
| spelling | doaj.art-118705a629ff47a3a9f20e42162f0fc12022-12-22T01:46:50ZengBMCFrontiers in Zoology1742-99942022-04-0119111510.1186/s12983-022-00460-1Movement and storage of nematocysts across development in the nudibranch Berghia stephanieae (Valdés, 2005)Jessica A. Goodheart0Vanessa Barone1Deirdre C. Lyons2Scripps Institution of Oceanography, University of California, San DiegoScripps Institution of Oceanography, University of California, San DiegoScripps Institution of Oceanography, University of California, San DiegoAbstract Background Intracellular sequestration requires specialized cellular and molecular mechanisms allowing a predator to retain and use specific organelles that once belonged to its prey. Little is known about how common cellular mechanisms, like phagocytosis, can be modified to selectively internalize and store foreign structures. One form of defensive sequestration involves animals that sequester stinging organelles (nematocysts) from their cnidarian prey. While it has been hypothesized that nematocysts are identified by specialized phagocytic cells for internalization and storage, little is known about the cellular and developmental mechanisms of this process in any metazoan lineage. This knowledge gap is mainly due to a lack of genetically tractable model systems among predators and their cnidarian prey. Results Here, we introduce the nudibranch Berghia stephanieae as a model system to investigate the cell, developmental, and physiological features of nematocyst sequestration selectivity. We first show that B. stephanieae, which feeds on Exaiptasia diaphana, selectively sequesters nematocysts over other E. diaphana tissues found in their digestive gland. Using confocal microscopy, we document that nematocyst sequestration begins shortly after feeding and prior to the formation of the appendages (cerata) where the organ responsible for sequestration (the cnidosac) resides in adults. This finding is inconsistent with previous studies that place the formation of the cnidosac after cerata emerge. Our results also show, via live imaging assays, that both nematocysts and dinoflagellates can enter the nascent cnidosac structure. This result indicates that selectivity for nematocysts occurs inside the cnidosac in B. stephanieae, likely in the cnidophage cells themselves. Conclusions Our work highlights the utility of B. stephanieae for future research, because: (1) this species can be cultured in the laboratory, which provides access to all developmental stages, and (2) the transparency of early juveniles makes imaging techniques (and therefore cell and molecular assays) feasible. Our results pave the way for future studies using live imaging and targeted gene editing to identify the molecular mechanisms involved in nematocyst sequestration. Further studies of nematocyst sequestration in B. stephanieae will also allow us to investigate how common cellular mechanisms like phagocytosis can be modified to selectively internalize and store foreign structures.https://doi.org/10.1186/s12983-022-00460-1Nudibranch gastropodsIntracellular sequestrationNematocystsCell and particle recognitionJuvenile development |
| spellingShingle | Jessica A. Goodheart Vanessa Barone Deirdre C. Lyons Movement and storage of nematocysts across development in the nudibranch Berghia stephanieae (Valdés, 2005) Frontiers in Zoology Nudibranch gastropods Intracellular sequestration Nematocysts Cell and particle recognition Juvenile development |
| title | Movement and storage of nematocysts across development in the nudibranch Berghia stephanieae (Valdés, 2005) |
| title_full | Movement and storage of nematocysts across development in the nudibranch Berghia stephanieae (Valdés, 2005) |
| title_fullStr | Movement and storage of nematocysts across development in the nudibranch Berghia stephanieae (Valdés, 2005) |
| title_full_unstemmed | Movement and storage of nematocysts across development in the nudibranch Berghia stephanieae (Valdés, 2005) |
| title_short | Movement and storage of nematocysts across development in the nudibranch Berghia stephanieae (Valdés, 2005) |
| title_sort | movement and storage of nematocysts across development in the nudibranch berghia stephanieae valdes 2005 |
| topic | Nudibranch gastropods Intracellular sequestration Nematocysts Cell and particle recognition Juvenile development |
| url | https://doi.org/10.1186/s12983-022-00460-1 |
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