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Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge

The ability of organisms to combine autotrophy and heterotrophy gives rise to one of the most successful nutritional strategies on Earth: mixotrophy. Sponges are integral members of shallow-water ecosystems and many host photosynthetic symbionts, but studies on mixotrophic sponges have focused prima...

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Autores principales: Hudspith, Meggie, de Goeij, Jasper M., Streekstra, Mischa, Kornder, Niklas A., Bougoure, Jeremy, Guagliardo, Paul, Campana, Sara, van der Wel, Nicole N., Muyzer, Gerard, Rix, Laura
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9381825/
https://www.ncbi.nlm.nih.gov/pubmed/35654830
http://dx.doi.org/10.1038/s41396-022-01254-3
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author Hudspith, Meggie
de Goeij, Jasper M.
Streekstra, Mischa
Kornder, Niklas A.
Bougoure, Jeremy
Guagliardo, Paul
Campana, Sara
van der Wel, Nicole N.
Muyzer, Gerard
Rix, Laura
author_facet Hudspith, Meggie
de Goeij, Jasper M.
Streekstra, Mischa
Kornder, Niklas A.
Bougoure, Jeremy
Guagliardo, Paul
Campana, Sara
van der Wel, Nicole N.
Muyzer, Gerard
Rix, Laura
author_sort Hudspith, Meggie
collection PubMed
description The ability of organisms to combine autotrophy and heterotrophy gives rise to one of the most successful nutritional strategies on Earth: mixotrophy. Sponges are integral members of shallow-water ecosystems and many host photosynthetic symbionts, but studies on mixotrophic sponges have focused primarily on species residing in high-light environments. Here, we quantify the contribution of photoautotrophy to the respiratory demand and total carbon diet of the sponge Chondrilla caribensis, which hosts symbiotic cyanobacteria and lives in low-light environments. Although the sponge is net heterotrophic at 20 m water depth, photosynthetically fixed carbon potentially provides up to 52% of the holobiont’s respiratory demand. When considering the total mixotrophic diet, photoautotrophy contributed an estimated 7% to total daily carbon uptake. Visualization of inorganic (13)C- and (15)N-incorporation using nanoscale secondary ion mass spectrometry (NanoSIMS) at the single-cell level confirmed that a portion of nutrients assimilated by the prokaryotic community was translocated to host cells. Photoautotrophy can thus provide an important supplemental source of carbon for sponges, even in low-light habitats. This trophic plasticity may represent a widespread strategy for net heterotrophic sponges hosting photosymbionts, enabling the host to buffer against periods of nutritional stress.
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spelling pubmed-93818252022-08-18 Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge Hudspith, Meggie de Goeij, Jasper M. Streekstra, Mischa Kornder, Niklas A. Bougoure, Jeremy Guagliardo, Paul Campana, Sara van der Wel, Nicole N. Muyzer, Gerard Rix, Laura ISME J Article The ability of organisms to combine autotrophy and heterotrophy gives rise to one of the most successful nutritional strategies on Earth: mixotrophy. Sponges are integral members of shallow-water ecosystems and many host photosynthetic symbionts, but studies on mixotrophic sponges have focused primarily on species residing in high-light environments. Here, we quantify the contribution of photoautotrophy to the respiratory demand and total carbon diet of the sponge Chondrilla caribensis, which hosts symbiotic cyanobacteria and lives in low-light environments. Although the sponge is net heterotrophic at 20 m water depth, photosynthetically fixed carbon potentially provides up to 52% of the holobiont’s respiratory demand. When considering the total mixotrophic diet, photoautotrophy contributed an estimated 7% to total daily carbon uptake. Visualization of inorganic (13)C- and (15)N-incorporation using nanoscale secondary ion mass spectrometry (NanoSIMS) at the single-cell level confirmed that a portion of nutrients assimilated by the prokaryotic community was translocated to host cells. Photoautotrophy can thus provide an important supplemental source of carbon for sponges, even in low-light habitats. This trophic plasticity may represent a widespread strategy for net heterotrophic sponges hosting photosymbionts, enabling the host to buffer against periods of nutritional stress. Nature Publishing Group UK 2022-06-02 2022-09 /pmc/articles/PMC9381825/ /pubmed/35654830 http://dx.doi.org/10.1038/s41396-022-01254-3 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Hudspith, Meggie
de Goeij, Jasper M.
Streekstra, Mischa
Kornder, Niklas A.
Bougoure, Jeremy
Guagliardo, Paul
Campana, Sara
van der Wel, Nicole N.
Muyzer, Gerard
Rix, Laura
Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge
title Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge
title_full Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge
title_fullStr Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge
title_full_unstemmed Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge
title_short Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge
title_sort harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9381825/
https://www.ncbi.nlm.nih.gov/pubmed/35654830
http://dx.doi.org/10.1038/s41396-022-01254-3
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