Subcellular Investigation of Photosynthesis-Driven Carbon Assimilation in the Symbiotic Reef Coral <italic toggle="yes">Pocillopora damicornis</italic>

ABSTRACT Reef-building corals form essential, mutualistic endosymbiotic associations with photosynthetic Symbiodinium dinoflagellates, providing their animal host partner with photosynthetically derived nutrients that allow the coral to thrive in oligotrophic waters. However, little is known about...

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Autores principales:	Christophe Kopp, Isabelle Domart-Coulon, Stephane Escrig, Bruno M. Humbel, Michel Hignette, Anders Meibom
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/76f67edcc6be41dca8830322b333b4d9
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spelling	oai:doaj.org-article:76f67edcc6be41dca8830322b333b4d92021-11-15T15:41:19ZSubcellular Investigation of Photosynthesis-Driven Carbon Assimilation in the Symbiotic Reef Coral <italic toggle="yes">Pocillopora damicornis</italic>10.1128/mBio.02299-142150-7511https://doaj.org/article/76f67edcc6be41dca8830322b333b4d92015-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02299-14https://doaj.org/toc/2150-7511ABSTRACT Reef-building corals form essential, mutualistic endosymbiotic associations with photosynthetic Symbiodinium dinoflagellates, providing their animal host partner with photosynthetically derived nutrients that allow the coral to thrive in oligotrophic waters. However, little is known about the dynamics of these nutritional interactions at the (sub)cellular level. Here, we visualize with submicrometer spatial resolution the carbon and nitrogen fluxes in the intact coral-dinoflagellate association from the reef coral Pocillopora damicornis by combining nanoscale secondary ion mass spectrometry (NanoSIMS) and transmission electron microscopy with pulse-chase isotopic labeling using [13C]bicarbonate and [15N]nitrate. This allows us to observe that (i) through light-driven photosynthesis, dinoflagellates rapidly assimilate inorganic bicarbonate and nitrate, temporarily storing carbon within lipid droplets and starch granules for remobilization in nighttime, along with carbon and nitrogen incorporation into other subcellular compartments for dinoflagellate growth and maintenance, (ii) carbon-containing photosynthates are translocated to all four coral tissue layers, where they accumulate after only 15 min in coral lipid droplets from the oral gastroderm and within 6 h in glycogen granules from the oral epiderm, and (iii) the translocation of nitrogen-containing photosynthates is delayed by 3 h. IMPORTANCE Our results provide detailed in situ subcellular visualization of the fate of photosynthesis-derived carbon and nitrogen in the coral-dinoflagellate endosymbiosis. We directly demonstrate that lipid droplets and glycogen granules in the coral tissue are sinks for translocated carbon photosynthates by dinoflagellates and confirm their key role in the trophic interactions within the coral-dinoflagellate association.Christophe KoppIsabelle Domart-CoulonStephane EscrigBruno M. HumbelMichel HignetteAnders MeibomAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 1 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Christophe Kopp Isabelle Domart-Coulon Stephane Escrig Bruno M. Humbel Michel Hignette Anders Meibom Subcellular Investigation of Photosynthesis-Driven Carbon Assimilation in the Symbiotic Reef Coral <italic toggle="yes">Pocillopora damicornis</italic>
description	ABSTRACT Reef-building corals form essential, mutualistic endosymbiotic associations with photosynthetic Symbiodinium dinoflagellates, providing their animal host partner with photosynthetically derived nutrients that allow the coral to thrive in oligotrophic waters. However, little is known about the dynamics of these nutritional interactions at the (sub)cellular level. Here, we visualize with submicrometer spatial resolution the carbon and nitrogen fluxes in the intact coral-dinoflagellate association from the reef coral Pocillopora damicornis by combining nanoscale secondary ion mass spectrometry (NanoSIMS) and transmission electron microscopy with pulse-chase isotopic labeling using [13C]bicarbonate and [15N]nitrate. This allows us to observe that (i) through light-driven photosynthesis, dinoflagellates rapidly assimilate inorganic bicarbonate and nitrate, temporarily storing carbon within lipid droplets and starch granules for remobilization in nighttime, along with carbon and nitrogen incorporation into other subcellular compartments for dinoflagellate growth and maintenance, (ii) carbon-containing photosynthates are translocated to all four coral tissue layers, where they accumulate after only 15 min in coral lipid droplets from the oral gastroderm and within 6 h in glycogen granules from the oral epiderm, and (iii) the translocation of nitrogen-containing photosynthates is delayed by 3 h. IMPORTANCE Our results provide detailed in situ subcellular visualization of the fate of photosynthesis-derived carbon and nitrogen in the coral-dinoflagellate endosymbiosis. We directly demonstrate that lipid droplets and glycogen granules in the coral tissue are sinks for translocated carbon photosynthates by dinoflagellates and confirm their key role in the trophic interactions within the coral-dinoflagellate association.
format	article
author	Christophe Kopp Isabelle Domart-Coulon Stephane Escrig Bruno M. Humbel Michel Hignette Anders Meibom
author_facet	Christophe Kopp Isabelle Domart-Coulon Stephane Escrig Bruno M. Humbel Michel Hignette Anders Meibom
author_sort	Christophe Kopp
title	Subcellular Investigation of Photosynthesis-Driven Carbon Assimilation in the Symbiotic Reef Coral <italic toggle="yes">Pocillopora damicornis</italic>
title_short	Subcellular Investigation of Photosynthesis-Driven Carbon Assimilation in the Symbiotic Reef Coral <italic toggle="yes">Pocillopora damicornis</italic>
title_full	Subcellular Investigation of Photosynthesis-Driven Carbon Assimilation in the Symbiotic Reef Coral <italic toggle="yes">Pocillopora damicornis</italic>
title_fullStr	Subcellular Investigation of Photosynthesis-Driven Carbon Assimilation in the Symbiotic Reef Coral <italic toggle="yes">Pocillopora damicornis</italic>
title_full_unstemmed	Subcellular Investigation of Photosynthesis-Driven Carbon Assimilation in the Symbiotic Reef Coral <italic toggle="yes">Pocillopora damicornis</italic>
title_sort	subcellular investigation of photosynthesis-driven carbon assimilation in the symbiotic reef coral <italic toggle="yes">pocillopora damicornis</italic>
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/76f67edcc6be41dca8830322b333b4d9
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Subcellular Investigation of Photosynthesis-Driven Carbon Assimilation in the Symbiotic Reef Coral <italic toggle="yes">Pocillopora damicornis</italic>

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