Single-cell measurement of ammonium and bicarbonate uptake within a photosymbiotic bioeroding sponge

Achlatis, M; Pernice, M; Green, K; Guagliardo, P; Kilburn, MR; Hoegh-Guldberg, O; Dove, S

Single-cell measurement of ammonium and bicarbonate uptake within a photosymbiotic bioeroding sponge

Achlatis, M Pernice, M

Green, K Guagliardo, P Kilburn, MR Hoegh-Guldberg, O Dove, S

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Publication Type:: Journal Article
Citation:: ISME Journal, 2018, 12 (5), pp. 1308 - 1318
Issue Date:: 2018-05-01

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Field	Value	Language
dc.contributor.author	Achlatis, M	en_US
dc.contributor.author	Pernice, M https://orcid.org/0000-0002-3431-2104	en_US
dc.contributor.author	Green, K	en_US
dc.contributor.author	Guagliardo, P	en_US
dc.contributor.author	Kilburn, MR	en_US
dc.contributor.author	Hoegh-Guldberg, O	en_US
dc.contributor.author	Dove, S	en_US
dc.date.available	2020-05-25T19:10:48Z
dc.date.issued	2018-05-01	en_US
dc.identifier.citation	ISME Journal, 2018, 12 (5), pp. 1308 - 1318	en_US
dc.identifier.issn	1751-7362	en_US
dc.identifier.uri	http://hdl.handle.net/10453/123760
dc.description.abstract	© 2018 International Society for Microbial Ecology. Some of the most aggressive coral-excavating sponges host intracellular dinoflagellates from the genus Symbiodinium, which are hypothesized to provide the sponges with autotrophic energy that powers bioerosion. Investigations of the contribution of Symbiodinium to host metabolism and particularly inorganic nutrient recycling are complicated, however, by the presence of alternative prokaryotic candidates for this role. Here, novel methods are used to study nutrient assimilation and transfer within and between the outer-layer cells of the Indopacific bioeroding sponge Cliona orientalis. Combining stable isotope labelling, transmission electron microscopy (TEM) and nanoscale secondary ion mass spectrometry (NanoSIMS), we visualize and measure metabolic activity at the individual cell level, tracking the fate of 15N-ammonium and 13C-bicarbonate within the intact holobiont. We found strong uptake of both inorganic sources (especially 13C-bicarbonate) by Symbiodinium cells. Labelled organic nutrients were translocated from Symbiodinium to the Symbiodinium-hosting sponge cells within 6 h, and occasionally to other sponge cells within 3 days. By contrast, prokaryotic symbionts were not observed to participate in inorganic nutrient assimilation in the outer layers of the sponge. Our findings strongly support the metabolic interaction between the sponge and dinoflagellates, shedding light on the ecological advantages and adaptive capacity of photosymbiotic bioeroding sponges in oligotrophic marine habitats.	en_US
dc.relation.ispartof	ISME Journal	en_US
dc.relation.isbasedon	10.1038/s41396-017-0044-2	en_US
dc.subject.classification	Microbiology	en_US
dc.subject.mesh	Animals	en_US
dc.subject.mesh	Porifera	en_US
dc.subject.mesh	Dinoflagellida	en_US
dc.subject.mesh	Bicarbonates	en_US
dc.subject.mesh	Ammonium Compounds	en_US
dc.subject.mesh	Ecosystem	en_US
dc.subject.mesh	Symbiosis	en_US
dc.subject.mesh	Coral Reefs	en_US
dc.subject.mesh	Single-Cell Analysis	en_US
dc.title	Single-cell measurement of ammonium and bicarbonate uptake within a photosymbiotic bioeroding sponge	en_US
dc.type	Journal Article
utslib.citation.volume	5	en_US
utslib.citation.volume	12	en_US
utslib.for	0602 Ecology	en_US
utslib.for	0601 Biochemistry and Cell Biology	en_US
utslib.for	05 Environmental Sciences	en_US
utslib.for	06 Biological Sciences	en_US
utslib.for	10 Technology	en_US
pubs.embargo.period	Not known	en_US
pubs.organisational-group	/University of Technology Sydney
pubs.organisational-group	/University of Technology Sydney/Faculty of Science
pubs.organisational-group	/University of Technology Sydney/Strength - C3 - Climate Change Cluster
utslib.copyright.status	open_access
pubs.issue	5	en_US
pubs.publication-status	Published	en_US
pubs.volume	12	en_US

Abstract:

© 2018 International Society for Microbial Ecology. Some of the most aggressive coral-excavating sponges host intracellular dinoflagellates from the genus Symbiodinium, which are hypothesized to provide the sponges with autotrophic energy that powers bioerosion. Investigations of the contribution of Symbiodinium to host metabolism and particularly inorganic nutrient recycling are complicated, however, by the presence of alternative prokaryotic candidates for this role. Here, novel methods are used to study nutrient assimilation and transfer within and between the outer-layer cells of the Indopacific bioeroding sponge Cliona orientalis. Combining stable isotope labelling, transmission electron microscopy (TEM) and nanoscale secondary ion mass spectrometry (NanoSIMS), we visualize and measure metabolic activity at the individual cell level, tracking the fate of 15N-ammonium and 13C-bicarbonate within the intact holobiont. We found strong uptake of both inorganic sources (especially 13C-bicarbonate) by Symbiodinium cells. Labelled organic nutrients were translocated from Symbiodinium to the Symbiodinium-hosting sponge cells within 6 h, and occasionally to other sponge cells within 3 days. By contrast, prokaryotic symbionts were not observed to participate in inorganic nutrient assimilation in the outer layers of the sponge. Our findings strongly support the metabolic interaction between the sponge and dinoflagellates, shedding light on the ecological advantages and adaptive capacity of photosymbiotic bioeroding sponges in oligotrophic marine habitats.

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http://hdl.handle.net/10453/123760