Identification of scavenger receptors and thrombospondin‐type‐1 repeat proteins potentially relevant for plastid recognition in Sacoglossa

Abstract Functional kleptoplasty is a photosymbiotic relationship, in which photosynthetically active chloroplasts serve as an intracellular symbiont for a heterotrophic host. Among Metazoa, functional kleptoplasty is only found in marine sea slugs belonging to the Sacoglossa and recently described...

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Main Authors: Jenny Melo Clavijo, Silja Frankenbach, Cátia Fidalgo, João Serôdio, Alexander Donath, Angelika Preisfeld, Gregor Christa
Format: Article
Language:English
Published: Wiley 2020-11-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.6865
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author Jenny Melo Clavijo
Silja Frankenbach
Cátia Fidalgo
João Serôdio
Alexander Donath
Angelika Preisfeld
Gregor Christa
author_facet Jenny Melo Clavijo
Silja Frankenbach
Cátia Fidalgo
João Serôdio
Alexander Donath
Angelika Preisfeld
Gregor Christa
author_sort Jenny Melo Clavijo
collection DOAJ
description Abstract Functional kleptoplasty is a photosymbiotic relationship, in which photosynthetically active chloroplasts serve as an intracellular symbiont for a heterotrophic host. Among Metazoa, functional kleptoplasty is only found in marine sea slugs belonging to the Sacoglossa and recently described in Rhabdocoela worms. Although functional kleptoplasty has been intensively studied in Sacoglossa, the fundamentals of the specific recognition of the chloroplasts and their subsequent incorporation are unknown. The key to ensure the initiation of any symbiosis is the ability to specifically recognize the symbiont and to differentiate a symbiont from a pathogen. For instance, in photosymbiotic cnidarians, several studies have shown that the host innate immune system, in particular scavenger receptors (SRs) and thrombospondin‐type‐1 repeat (TSR) protein superfamily, is playing a major role in the process of recognizing and differentiating symbionts from pathogens. In the present study, SRs and TSRs of three Sacoglossa sea slugs, Elysia cornigera, Elysia timida, and Elysia chlorotica, were identified by translating available transcriptomes into potential proteins and searching for receptor specific protein and/or transmembrane domains. Both receptors classes are highly diverse in the slugs, and many new domain arrangements for each receptor class were found. The analyses of the gene expression of these three species provided a set of species‐specific candidate genes, that is, SR‐Bs, SR‐Es, C‐type lectins, and TSRs, that are potentially relevant for the recognition of kleptoplasts. The results set the base for future experimental studies to understand if and how these candidate receptors are indeed involved in chloroplast recognition.
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spelling doaj.art-c859ce34e3fc47e4b8986460ab0db2c22022-12-21T22:44:47ZengWileyEcology and Evolution2045-77582020-11-011021123481236310.1002/ece3.6865Identification of scavenger receptors and thrombospondin‐type‐1 repeat proteins potentially relevant for plastid recognition in SacoglossaJenny Melo Clavijo0Silja Frankenbach1Cátia Fidalgo2João Serôdio3Alexander Donath4Angelika Preisfeld5Gregor Christa6Fakultät für Mathematik und Naturwissenschaften, Zoologie und Biologiedidaktik Bergische Universität Wuppertal Wuppertal GermanyDepartment of Biology and CESAM – Center for Environmental and Marine Studies University of Aveiro Aveiro PortugalDepartment of Biology and CESAM – Center for Environmental and Marine Studies University of Aveiro Aveiro PortugalDepartment of Biology and CESAM – Center for Environmental and Marine Studies University of Aveiro Aveiro PortugalCenter for Molecular Biodiversity Research Zoological Research Museum Alexander Koenig Bonn GermanyFakultät für Mathematik und Naturwissenschaften, Zoologie und Biologiedidaktik Bergische Universität Wuppertal Wuppertal GermanyFakultät für Mathematik und Naturwissenschaften, Zoologie und Biologiedidaktik Bergische Universität Wuppertal Wuppertal GermanyAbstract Functional kleptoplasty is a photosymbiotic relationship, in which photosynthetically active chloroplasts serve as an intracellular symbiont for a heterotrophic host. Among Metazoa, functional kleptoplasty is only found in marine sea slugs belonging to the Sacoglossa and recently described in Rhabdocoela worms. Although functional kleptoplasty has been intensively studied in Sacoglossa, the fundamentals of the specific recognition of the chloroplasts and their subsequent incorporation are unknown. The key to ensure the initiation of any symbiosis is the ability to specifically recognize the symbiont and to differentiate a symbiont from a pathogen. For instance, in photosymbiotic cnidarians, several studies have shown that the host innate immune system, in particular scavenger receptors (SRs) and thrombospondin‐type‐1 repeat (TSR) protein superfamily, is playing a major role in the process of recognizing and differentiating symbionts from pathogens. In the present study, SRs and TSRs of three Sacoglossa sea slugs, Elysia cornigera, Elysia timida, and Elysia chlorotica, were identified by translating available transcriptomes into potential proteins and searching for receptor specific protein and/or transmembrane domains. Both receptors classes are highly diverse in the slugs, and many new domain arrangements for each receptor class were found. The analyses of the gene expression of these three species provided a set of species‐specific candidate genes, that is, SR‐Bs, SR‐Es, C‐type lectins, and TSRs, that are potentially relevant for the recognition of kleptoplasts. The results set the base for future experimental studies to understand if and how these candidate receptors are indeed involved in chloroplast recognition.https://doi.org/10.1002/ece3.6865ElysiaKleptoplastyphotosymbiosissacoglossascavenger receptorsthrombospondin
spellingShingle Jenny Melo Clavijo
Silja Frankenbach
Cátia Fidalgo
João Serôdio
Alexander Donath
Angelika Preisfeld
Gregor Christa
Identification of scavenger receptors and thrombospondin‐type‐1 repeat proteins potentially relevant for plastid recognition in Sacoglossa
Ecology and Evolution
Elysia
Kleptoplasty
photosymbiosis
sacoglossa
scavenger receptors
thrombospondin
title Identification of scavenger receptors and thrombospondin‐type‐1 repeat proteins potentially relevant for plastid recognition in Sacoglossa
title_full Identification of scavenger receptors and thrombospondin‐type‐1 repeat proteins potentially relevant for plastid recognition in Sacoglossa
title_fullStr Identification of scavenger receptors and thrombospondin‐type‐1 repeat proteins potentially relevant for plastid recognition in Sacoglossa
title_full_unstemmed Identification of scavenger receptors and thrombospondin‐type‐1 repeat proteins potentially relevant for plastid recognition in Sacoglossa
title_short Identification of scavenger receptors and thrombospondin‐type‐1 repeat proteins potentially relevant for plastid recognition in Sacoglossa
title_sort identification of scavenger receptors and thrombospondin type 1 repeat proteins potentially relevant for plastid recognition in sacoglossa
topic Elysia
Kleptoplasty
photosymbiosis
sacoglossa
scavenger receptors
thrombospondin
url https://doi.org/10.1002/ece3.6865
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