Subcellular view of host-microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan-microbe symbiosis.

Hudspith, M; Rix, L; Achlatis, M; Bougoure, J; Guagliardo, P; Clode, PL; Webster, NS; Muyzer, G; Pernice, M; de Goeij, JM

Subcellular view of host-microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan-microbe symbiosis.

Hudspith, M Rix, L Achlatis, M Bougoure, J Guagliardo, P Clode, PL Webster, NS Muyzer, G Pernice, M

de Goeij, JM

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Publisher:: Springer Science and Business Media LLC
Publication Type:: Journal Article
Citation:: Microbiome, 2021, 9, (1), pp. 44
Issue Date:: 2021-02-14

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Field	Value	Language
dc.contributor.author	Hudspith, M
dc.contributor.author	Rix, L
dc.contributor.author	Achlatis, M
dc.contributor.author	Bougoure, J
dc.contributor.author	Guagliardo, P
dc.contributor.author	Clode, PL
dc.contributor.author	Webster, NS
dc.contributor.author	Muyzer, G
dc.contributor.author	Pernice, M https://orcid.org/0000-0002-3431-2104
dc.contributor.author	de Goeij, JM
dc.date.accessioned	2021-03-15T02:05:22Z
dc.date.available	2020-12-16
dc.date.available	2021-03-15T02:05:22Z
dc.date.issued	2021-02-14
dc.identifier.citation	Microbiome, 2021, 9, (1), pp. 44
dc.identifier.issn	2049-2618
dc.identifier.issn	2049-2618
dc.identifier.uri	http://hdl.handle.net/10453/147135
dc.description.abstract	<h4>Background</h4>Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats. They play an important role in nutrient cycling due to their unrivalled capacity for processing both dissolved and particulate organic matter (DOM and POM) and the exceptional metabolic repertoire of their diverse and abundant microbial communities. Functional studies determining the role of host and microbiome in organic nutrient uptake and exchange, however, are limited. Therefore, we coupled pulse-chase isotopic tracer techniques with nanoscale secondary ion mass spectrometry (NanoSIMS) to visualise the uptake and translocation of <sup>13</sup>C- and <sup>15</sup>N-labelled dissolved and particulate organic food at subcellular level in the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Halisarca caerulea.<h4>Results</h4>The two sponge species showed significant enrichment of DOM- and POM-derived <sup>13</sup>C and <sup>15</sup>N into their tissue over time. Microbial symbionts were actively involved in the assimilation of DOM, but host filtering cells (choanocytes) appeared to be the primary site of DOM and POM uptake in both sponge species overall, via pinocytosis and phagocytosis, respectively. Translocation of carbon and nitrogen from choanocytes to microbial symbionts occurred over time, irrespective of microbial abundance, reflecting recycling of host waste products by the microbiome.<h4>Conclusions</h4>Here, we provide empirical evidence indicating that the prokaryotic communities of a high and a low microbial abundance sponge obtain nutritional benefits from their host-associated lifestyle. The metabolic interaction between the highly efficient filter-feeding host and its microbial symbionts likely provides a competitive advantage to the sponge holobiont in the oligotrophic environments in which they thrive, by retaining and recycling limiting nutrients. Sponges present a unique model to link nutritional symbiotic interactions to holobiont function, and, via cascading effects, ecosystem functioning, in one of the earliest metazoan-microbe symbioses. Video abstract.
dc.format	Electronic
dc.language	eng
dc.publisher	Springer Science and Business Media LLC
dc.relation.ispartof	Microbiome
dc.relation.isbasedon	10.1186/s40168-020-00984-w
dc.rights	info:eu-repo/semantics/openAccess
dc.rights	This is a post-peer-review, pre-copyedit version of an article published in Microbiome. The final authenticated version is available online at: https://dx.doi.org/10.1186/s40168-020-00984-w.	en_US
dc.subject	0602 Ecology, 0605 Microbiology, 1108 Medical Microbiology
dc.title	Subcellular view of host-microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan-microbe symbiosis.
dc.type	Journal Article
utslib.citation.volume	9
utslib.location.activity	England
utslib.for	0602 Ecology
utslib.for	0605 Microbiology
utslib.for	1108 Medical Microbiology
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	*
dc.date.updated	2021-03-15T02:05:21Z
pubs.issue	1
pubs.publication-status	Published
pubs.volume	9
utslib.citation.issue	1

Abstract:

Background

Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats. They play an important role in nutrient cycling due to their unrivalled capacity for processing both dissolved and particulate organic matter (DOM and POM) and the exceptional metabolic repertoire of their diverse and abundant microbial communities. Functional studies determining the role of host and microbiome in organic nutrient uptake and exchange, however, are limited. Therefore, we coupled pulse-chase isotopic tracer techniques with nanoscale secondary ion mass spectrometry (NanoSIMS) to visualise the uptake and translocation of ¹³C- and ¹⁵N-labelled dissolved and particulate organic food at subcellular level in the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Halisarca caerulea.

Results

The two sponge species showed significant enrichment of DOM- and POM-derived ¹³C and ¹⁵N into their tissue over time. Microbial symbionts were actively involved in the assimilation of DOM, but host filtering cells (choanocytes) appeared to be the primary site of DOM and POM uptake in both sponge species overall, via pinocytosis and phagocytosis, respectively. Translocation of carbon and nitrogen from choanocytes to microbial symbionts occurred over time, irrespective of microbial abundance, reflecting recycling of host waste products by the microbiome.

Conclusions

Here, we provide empirical evidence indicating that the prokaryotic communities of a high and a low microbial abundance sponge obtain nutritional benefits from their host-associated lifestyle. The metabolic interaction between the highly efficient filter-feeding host and its microbial symbionts likely provides a competitive advantage to the sponge holobiont in the oligotrophic environments in which they thrive, by retaining and recycling limiting nutrients. Sponges present a unique model to link nutritional symbiotic interactions to holobiont function, and, via cascading effects, ecosystem functioning, in one of the earliest metazoan-microbe symbioses. Video abstract.

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http://hdl.handle.net/10453/147135