Sleeping with the enemy: unravelling the symbiotic relationships between the scale worm Neopolynoe chondrocladiae (Annelida: Polynoidae) and its carnivorous sponge hosts
24 pages, 8 figures, 5 tables, supporting Information and supplementary data https://doi.org/10.1093/zoolinnean/zlaa146 The North Atlantic deep-water polynoid worm Neopolynoe chondrocladiae is involved in an exceptional symbiotic relationship with two hosts: the carnivorous sponges Chondrocladia rob...
Published in: | Zoological Journal of the Linnean Society |
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Online Access: | http://hdl.handle.net/10261/253142 https://doi.org/10.1093/zoolinnean/zlaa146 https://doi.org/10.13039/501100011033 https://doi.org/10.13039/501100000780 |
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ftcsic:oai:digital.csic.es:10261/253142 2024-02-11T10:06:01+01:00 Sleeping with the enemy: unravelling the symbiotic relationships between the scale worm Neopolynoe chondrocladiae (Annelida: Polynoidae) and its carnivorous sponge hosts Taboada, S. Serra Silva, Ana Díez-Vives, Cristina Neal, Lenka Cristobo, Francisco J. Ríos, Pilar Hestetun, Jon Thomassen Clark, Brett Rossi, Maria Eleonora Junoy, Juan Navarro, Joan Riesgo Gil, Ana European Commission Agencia Estatal de Investigación (España) 2021-09 http://hdl.handle.net/10261/253142 https://doi.org/10.1093/zoolinnean/zlaa146 https://doi.org/10.13039/501100011033 https://doi.org/10.13039/501100000780 en eng Linnean Society of London https://doi.org/10.1093/zoolinnean/zlaa146 Sí Zoological Journal of the Linnean Society 193(1): 295-318 (2021) 0024-4082 CEX2019-000928-S http://hdl.handle.net/10261/253142 doi:10.1093/zoolinnean/zlaa146 1096-3642 http://dx.doi.org/10.13039/501100011033 http://dx.doi.org/10.13039/501100000780 open Bioluminescence Confocal Microbiome MicroCT Molecular connectivity Mutualism Stable isotopes Trophic relationships artículo http://purl.org/coar/resource_type/c_6501 2021 ftcsic https://doi.org/10.1093/zoolinnean/zlaa14610.13039/50110001103310.13039/501100000780 2024-01-16T11:14:55Z 24 pages, 8 figures, 5 tables, supporting Information and supplementary data https://doi.org/10.1093/zoolinnean/zlaa146 The North Atlantic deep-water polynoid worm Neopolynoe chondrocladiae is involved in an exceptional symbiotic relationship with two hosts: the carnivorous sponges Chondrocladia robertballardi and Chondrocladia virgata. While this is an obligate symbiotic relationship, its real nature is unclear. We used a multidisciplinary approach to narrow down the type of symbiotic relationship between symbiont and hosts. Molecular connectivity analyses using COI and 16S suggest that N. chondrocladiae has high potential for dispersal, connecting sites hundreds of kilometres apart, likely aided by oceanographic currents. Microbial analyses on different anatomical parts of five Chondrocladia species suggest that the presence of the worm in C. robertballardi does not affect the microbiome of the sponge. MicroCT analysis on N. chondrocladiae show that it has dorsally oriented parapodia, which might prevent the worm from getting trapped in the sponge. A faecal pellet recovered from the worm suggests that the polynoid feeds on the crustacean prey captured by the sponge, something corroborated by our stable isotope analysis. Light and confocal microscopy images suggest that N. chondrocladiae elytra produce bioluminescence. We propose that the worm might use bioluminescence as a lure for prey (increasing the food available for both the sponge and the polynoid) and thus fuelling a mutualistic relationship ST received funding from the Juan de la Cierva-Incorporación program (IJCI-2017–33116), the Spanish Government and received a fellowship from the Systematics Research Fund (SRF) in 2018. JN was funded by the Spanish National Program Ramón y Cajal (RYC-2015–17809). CDV received funding from the EU Horizon 2020 Marie Sklodowska-Curie ‘DeepSym’ (grant agreement: 796011) With the institutional support of the ‘Severo OchoaCentre of Excellence’ accreditation (CEX2019-000928-S) Peer reviewed Article in Journal/Newspaper North Atlantic Deep Water North Atlantic Digital.CSIC (Spanish National Research Council) Cierva ENVELOPE(-60.873,-60.873,-64.156,-64.156) Zoological Journal of the Linnean Society 193 1 295 318 |
institution |
Open Polar |
collection |
Digital.CSIC (Spanish National Research Council) |
op_collection_id |
ftcsic |
language |
English |
topic |
Bioluminescence Confocal Microbiome MicroCT Molecular connectivity Mutualism Stable isotopes Trophic relationships |
spellingShingle |
Bioluminescence Confocal Microbiome MicroCT Molecular connectivity Mutualism Stable isotopes Trophic relationships Taboada, S. Serra Silva, Ana Díez-Vives, Cristina Neal, Lenka Cristobo, Francisco J. Ríos, Pilar Hestetun, Jon Thomassen Clark, Brett Rossi, Maria Eleonora Junoy, Juan Navarro, Joan Riesgo Gil, Ana Sleeping with the enemy: unravelling the symbiotic relationships between the scale worm Neopolynoe chondrocladiae (Annelida: Polynoidae) and its carnivorous sponge hosts |
topic_facet |
Bioluminescence Confocal Microbiome MicroCT Molecular connectivity Mutualism Stable isotopes Trophic relationships |
description |
24 pages, 8 figures, 5 tables, supporting Information and supplementary data https://doi.org/10.1093/zoolinnean/zlaa146 The North Atlantic deep-water polynoid worm Neopolynoe chondrocladiae is involved in an exceptional symbiotic relationship with two hosts: the carnivorous sponges Chondrocladia robertballardi and Chondrocladia virgata. While this is an obligate symbiotic relationship, its real nature is unclear. We used a multidisciplinary approach to narrow down the type of symbiotic relationship between symbiont and hosts. Molecular connectivity analyses using COI and 16S suggest that N. chondrocladiae has high potential for dispersal, connecting sites hundreds of kilometres apart, likely aided by oceanographic currents. Microbial analyses on different anatomical parts of five Chondrocladia species suggest that the presence of the worm in C. robertballardi does not affect the microbiome of the sponge. MicroCT analysis on N. chondrocladiae show that it has dorsally oriented parapodia, which might prevent the worm from getting trapped in the sponge. A faecal pellet recovered from the worm suggests that the polynoid feeds on the crustacean prey captured by the sponge, something corroborated by our stable isotope analysis. Light and confocal microscopy images suggest that N. chondrocladiae elytra produce bioluminescence. We propose that the worm might use bioluminescence as a lure for prey (increasing the food available for both the sponge and the polynoid) and thus fuelling a mutualistic relationship ST received funding from the Juan de la Cierva-Incorporación program (IJCI-2017–33116), the Spanish Government and received a fellowship from the Systematics Research Fund (SRF) in 2018. JN was funded by the Spanish National Program Ramón y Cajal (RYC-2015–17809). CDV received funding from the EU Horizon 2020 Marie Sklodowska-Curie ‘DeepSym’ (grant agreement: 796011) With the institutional support of the ‘Severo OchoaCentre of Excellence’ accreditation (CEX2019-000928-S) Peer reviewed |
author2 |
European Commission Agencia Estatal de Investigación (España) |
format |
Article in Journal/Newspaper |
author |
Taboada, S. Serra Silva, Ana Díez-Vives, Cristina Neal, Lenka Cristobo, Francisco J. Ríos, Pilar Hestetun, Jon Thomassen Clark, Brett Rossi, Maria Eleonora Junoy, Juan Navarro, Joan Riesgo Gil, Ana |
author_facet |
Taboada, S. Serra Silva, Ana Díez-Vives, Cristina Neal, Lenka Cristobo, Francisco J. Ríos, Pilar Hestetun, Jon Thomassen Clark, Brett Rossi, Maria Eleonora Junoy, Juan Navarro, Joan Riesgo Gil, Ana |
author_sort |
Taboada, S. |
title |
Sleeping with the enemy: unravelling the symbiotic relationships between the scale worm Neopolynoe chondrocladiae (Annelida: Polynoidae) and its carnivorous sponge hosts |
title_short |
Sleeping with the enemy: unravelling the symbiotic relationships between the scale worm Neopolynoe chondrocladiae (Annelida: Polynoidae) and its carnivorous sponge hosts |
title_full |
Sleeping with the enemy: unravelling the symbiotic relationships between the scale worm Neopolynoe chondrocladiae (Annelida: Polynoidae) and its carnivorous sponge hosts |
title_fullStr |
Sleeping with the enemy: unravelling the symbiotic relationships between the scale worm Neopolynoe chondrocladiae (Annelida: Polynoidae) and its carnivorous sponge hosts |
title_full_unstemmed |
Sleeping with the enemy: unravelling the symbiotic relationships between the scale worm Neopolynoe chondrocladiae (Annelida: Polynoidae) and its carnivorous sponge hosts |
title_sort |
sleeping with the enemy: unravelling the symbiotic relationships between the scale worm neopolynoe chondrocladiae (annelida: polynoidae) and its carnivorous sponge hosts |
publisher |
Linnean Society of London |
publishDate |
2021 |
url |
http://hdl.handle.net/10261/253142 https://doi.org/10.1093/zoolinnean/zlaa146 https://doi.org/10.13039/501100011033 https://doi.org/10.13039/501100000780 |
long_lat |
ENVELOPE(-60.873,-60.873,-64.156,-64.156) |
geographic |
Cierva |
geographic_facet |
Cierva |
genre |
North Atlantic Deep Water North Atlantic |
genre_facet |
North Atlantic Deep Water North Atlantic |
op_relation |
https://doi.org/10.1093/zoolinnean/zlaa146 Sí Zoological Journal of the Linnean Society 193(1): 295-318 (2021) 0024-4082 CEX2019-000928-S http://hdl.handle.net/10261/253142 doi:10.1093/zoolinnean/zlaa146 1096-3642 http://dx.doi.org/10.13039/501100011033 http://dx.doi.org/10.13039/501100000780 |
op_rights |
open |
op_doi |
https://doi.org/10.1093/zoolinnean/zlaa14610.13039/50110001103310.13039/501100000780 |
container_title |
Zoological Journal of the Linnean Society |
container_volume |
193 |
container_issue |
1 |
container_start_page |
295 |
op_container_end_page |
318 |
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1790603394132475904 |