Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial Hydrozoan
<i>Hydractinia symbiolongicarpus</i> is a colonial hydrozoan that displays a division of labor through morphologically distinct and functionally specialized polyp types. As with all cnidarians, their venoms are housed in nematocysts, which are scattered across an individual. Here, we inv...
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| Format: | Article |
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MDPI AG
2023-02-01
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| Series: | Toxins |
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| Online Access: | https://www.mdpi.com/2072-6651/15/2/149 |
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| author | Anna M. L. Klompen Matthew K. Travert Paulyn Cartwright |
| author_facet | Anna M. L. Klompen Matthew K. Travert Paulyn Cartwright |
| author_sort | Anna M. L. Klompen |
| collection | DOAJ |
| description | <i>Hydractinia symbiolongicarpus</i> is a colonial hydrozoan that displays a division of labor through morphologically distinct and functionally specialized polyp types. As with all cnidarians, their venoms are housed in nematocysts, which are scattered across an individual. Here, we investigate the spatial distribution of a specific protein family, jellyfish toxins, in which multiple paralogs are differentially expressed across the functionally specialized polyps. Jellyfish toxins (JFTs) are known pore-forming toxins in the venoms of medically relevant species such as box jellyfish (class Cubozoa), but their role in other medusozoan venoms is less clear. Utilizing a publicly available single-cell dataset, we confirmed that four distinct <i>H. symbiolongicarpus</i> JFT paralogs are expressed in nematocyst-associated clusters, supporting these as true venom components in <i>H. symbiolongicarpus</i>. In situ hybridization and immunohistochemistry were used to localize the expression of these JFTs across the colony. These expression patterns, in conjunction with known nematocyst type distributions, suggest that two of these JFTs, HsymJFT1c-I and HsymJFT1c-II, are localized to specific types of nematocysts. We further interpret JFT expression patterns in the context of known regions of nematogenesis and differential rates of nematocyst turnover. Overall, we show that JFT expression patterns in <i>H. symbiolongicarpus</i> are consistent with the subfunctionalization of JFT paralogs across a partitioned venom system within the colony, such that each JFT is expressed within a specific set of functionally distinct polyp types and, in some cases, specific nematocyst types. |
| first_indexed | 2024-03-11T08:02:44Z |
| format | Article |
| id | doaj.art-49b230422ab0469a96f0d21aa6c6ec38 |
| institution | Directory Open Access Journal |
| issn | 2072-6651 |
| language | English |
| last_indexed | 2024-03-11T08:02:44Z |
| publishDate | 2023-02-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Toxins |
| spelling | doaj.art-49b230422ab0469a96f0d21aa6c6ec382023-11-16T23:39:13ZengMDPI AGToxins2072-66512023-02-0115214910.3390/toxins15020149Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial HydrozoanAnna M. L. Klompen0Matthew K. Travert1Paulyn Cartwright2Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045, USADepartment of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045, USADepartment of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045, USA<i>Hydractinia symbiolongicarpus</i> is a colonial hydrozoan that displays a division of labor through morphologically distinct and functionally specialized polyp types. As with all cnidarians, their venoms are housed in nematocysts, which are scattered across an individual. Here, we investigate the spatial distribution of a specific protein family, jellyfish toxins, in which multiple paralogs are differentially expressed across the functionally specialized polyps. Jellyfish toxins (JFTs) are known pore-forming toxins in the venoms of medically relevant species such as box jellyfish (class Cubozoa), but their role in other medusozoan venoms is less clear. Utilizing a publicly available single-cell dataset, we confirmed that four distinct <i>H. symbiolongicarpus</i> JFT paralogs are expressed in nematocyst-associated clusters, supporting these as true venom components in <i>H. symbiolongicarpus</i>. In situ hybridization and immunohistochemistry were used to localize the expression of these JFTs across the colony. These expression patterns, in conjunction with known nematocyst type distributions, suggest that two of these JFTs, HsymJFT1c-I and HsymJFT1c-II, are localized to specific types of nematocysts. We further interpret JFT expression patterns in the context of known regions of nematogenesis and differential rates of nematocyst turnover. Overall, we show that JFT expression patterns in <i>H. symbiolongicarpus</i> are consistent with the subfunctionalization of JFT paralogs across a partitioned venom system within the colony, such that each JFT is expressed within a specific set of functionally distinct polyp types and, in some cases, specific nematocyst types.https://www.mdpi.com/2072-6651/15/2/149cnidariahydrozoa<i>Hydractinia</i>colonialityvenomJFTs |
| spellingShingle | Anna M. L. Klompen Matthew K. Travert Paulyn Cartwright Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial Hydrozoan Toxins cnidaria hydrozoa <i>Hydractinia</i> coloniality venom JFTs |
| title | Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial Hydrozoan |
| title_full | Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial Hydrozoan |
| title_fullStr | Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial Hydrozoan |
| title_full_unstemmed | Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial Hydrozoan |
| title_short | Localization of Multiple Jellyfish Toxins Shows Specificity for Functionally Distinct Polyps and Nematocyst Types in a Colonial Hydrozoan |
| title_sort | localization of multiple jellyfish toxins shows specificity for functionally distinct polyps and nematocyst types in a colonial hydrozoan |
| topic | cnidaria hydrozoa <i>Hydractinia</i> coloniality venom JFTs |
| url | https://www.mdpi.com/2072-6651/15/2/149 |
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