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Potential for host-symbiont communication via neurotransmitters and neuromodulators in an aneural animal, the marine sponge Amphimedon queenslandica

Interkingdom signalling within a holobiont allows host and symbionts to communicate and to regulate each other’s physiological and developmental states. Here we show that a suite of signalling molecules that function as neurotransmitters and neuromodulators in most animals with nervous systems, spec...

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Autores principales: Xiang, Xueyan, Vilar Gomez, Arturo A., Blomberg, Simone P., Yuan, Huifang, Degnan, Bernard M., Degnan, Sandie M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10570526/
https://www.ncbi.nlm.nih.gov/pubmed/37841893
http://dx.doi.org/10.3389/fncir.2023.1250694
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author Xiang, Xueyan
Vilar Gomez, Arturo A.
Blomberg, Simone P.
Yuan, Huifang
Degnan, Bernard M.
Degnan, Sandie M.
author_facet Xiang, Xueyan
Vilar Gomez, Arturo A.
Blomberg, Simone P.
Yuan, Huifang
Degnan, Bernard M.
Degnan, Sandie M.
author_sort Xiang, Xueyan
collection PubMed
description Interkingdom signalling within a holobiont allows host and symbionts to communicate and to regulate each other’s physiological and developmental states. Here we show that a suite of signalling molecules that function as neurotransmitters and neuromodulators in most animals with nervous systems, specifically dopamine and trace amines, are produced exclusively by the bacterial symbionts of the demosponge Amphimedon queenslandica. Although sponges do not possess a nervous system, A. queenslandica expresses rhodopsin class G-protein-coupled receptors that are structurally similar to dopamine and trace amine receptors. When sponge larvae, which express these receptors, are exposed to agonists and antagonists of bilaterian dopamine and trace amine receptors, we observe marked changes in larval phototactic swimming behaviour, consistent with the sponge being competent to recognise and respond to symbiont-derived trace amine signals. These results indicate that monoamines synthesised by bacterial symbionts may be able to influence the physiology of the host sponge.
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spelling pubmed-105705262023-10-14 Potential for host-symbiont communication via neurotransmitters and neuromodulators in an aneural animal, the marine sponge Amphimedon queenslandica Xiang, Xueyan Vilar Gomez, Arturo A. Blomberg, Simone P. Yuan, Huifang Degnan, Bernard M. Degnan, Sandie M. Front Neural Circuits Neuroscience Interkingdom signalling within a holobiont allows host and symbionts to communicate and to regulate each other’s physiological and developmental states. Here we show that a suite of signalling molecules that function as neurotransmitters and neuromodulators in most animals with nervous systems, specifically dopamine and trace amines, are produced exclusively by the bacterial symbionts of the demosponge Amphimedon queenslandica. Although sponges do not possess a nervous system, A. queenslandica expresses rhodopsin class G-protein-coupled receptors that are structurally similar to dopamine and trace amine receptors. When sponge larvae, which express these receptors, are exposed to agonists and antagonists of bilaterian dopamine and trace amine receptors, we observe marked changes in larval phototactic swimming behaviour, consistent with the sponge being competent to recognise and respond to symbiont-derived trace amine signals. These results indicate that monoamines synthesised by bacterial symbionts may be able to influence the physiology of the host sponge. Frontiers Media S.A. 2023-09-29 /pmc/articles/PMC10570526/ /pubmed/37841893 http://dx.doi.org/10.3389/fncir.2023.1250694 Text en Copyright © 2023 Xiang, Vilar Gomez, Blomberg, Yuan, Degnan and Degnan. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Xiang, Xueyan
Vilar Gomez, Arturo A.
Blomberg, Simone P.
Yuan, Huifang
Degnan, Bernard M.
Degnan, Sandie M.
Potential for host-symbiont communication via neurotransmitters and neuromodulators in an aneural animal, the marine sponge Amphimedon queenslandica
title Potential for host-symbiont communication via neurotransmitters and neuromodulators in an aneural animal, the marine sponge Amphimedon queenslandica
title_full Potential for host-symbiont communication via neurotransmitters and neuromodulators in an aneural animal, the marine sponge Amphimedon queenslandica
title_fullStr Potential for host-symbiont communication via neurotransmitters and neuromodulators in an aneural animal, the marine sponge Amphimedon queenslandica
title_full_unstemmed Potential for host-symbiont communication via neurotransmitters and neuromodulators in an aneural animal, the marine sponge Amphimedon queenslandica
title_short Potential for host-symbiont communication via neurotransmitters and neuromodulators in an aneural animal, the marine sponge Amphimedon queenslandica
title_sort potential for host-symbiont communication via neurotransmitters and neuromodulators in an aneural animal, the marine sponge amphimedon queenslandica
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10570526/
https://www.ncbi.nlm.nih.gov/pubmed/37841893
http://dx.doi.org/10.3389/fncir.2023.1250694
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