Cargando…

Testing the relationship between microbiome composition and flux of carbon and nutrients in Caribbean coral reef sponges

BACKGROUND: Sponges are important suspension-feeding members of reef communities, with the collective capacity to overturn the entire water column on shallow Caribbean reefs every day. The sponge-loop hypothesis suggests that sponges take up dissolved organic carbon (DOC) and, via assimilation and s...

Descripción completa

Detalles Bibliográficos
Autores principales: Gantt, Shelby E., McMurray, Steven E., Stubler, Amber D., Finelli, Christopher M., Pawlik, Joseph R., Erwin, Patrick M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6716902/
https://www.ncbi.nlm.nih.gov/pubmed/31466521
http://dx.doi.org/10.1186/s40168-019-0739-x
_version_ 1783447465956999168
author Gantt, Shelby E.
McMurray, Steven E.
Stubler, Amber D.
Finelli, Christopher M.
Pawlik, Joseph R.
Erwin, Patrick M.
author_facet Gantt, Shelby E.
McMurray, Steven E.
Stubler, Amber D.
Finelli, Christopher M.
Pawlik, Joseph R.
Erwin, Patrick M.
author_sort Gantt, Shelby E.
collection PubMed
description BACKGROUND: Sponges are important suspension-feeding members of reef communities, with the collective capacity to overturn the entire water column on shallow Caribbean reefs every day. The sponge-loop hypothesis suggests that sponges take up dissolved organic carbon (DOC) and, via assimilation and shedding of cells, return carbon to the reef ecosystem as particulate organic carbon (POC). Sponges host complex microbial communities within their tissues that may play a role in carbon and nutrient cycling within the sponge holobiont. To investigate this relationship, we paired microbial community characterization (16S rRNA analysis, Illumina Mi-Seq platform) with carbon (DOC, POC) and nutrient (PO(4), NO(x), NH(4)) flux data (specific filtration rate) for 10 common Caribbean sponge species at two distant sites (Florida Keys vs. Belize, ~ 1203 km apart). RESULTS: Distance-based linear modeling revealed weak relationships overall between symbiont structure and carbon and nutrient flux, suggesting that the observed differences in POC, DOC, PO(4), and NO(x) flux among sponges are not caused by variations in the composition of symbiont communities. In contrast, significant correlations between symbiont structure and NH(4) flux occurred consistently across the dataset. Further, several individual symbiont taxa (OTUs) exhibited relative abundances that correlated with NH(4) flux, including one OTU affiliated with the ammonia-oxidizing genus Cenarchaeum. CONCLUSIONS: Combined, these results indicate that microbiome structure is uncoupled from sponge carbon cycling and does not explain variation in DOC uptake among Caribbean coral reef sponges. Accordingly, differential DOC assimilation by sponge cells or stable microbiome components may ultimately drive carbon flux in the sponge holobiont. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0739-x) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6716902
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-67169022019-09-04 Testing the relationship between microbiome composition and flux of carbon and nutrients in Caribbean coral reef sponges Gantt, Shelby E. McMurray, Steven E. Stubler, Amber D. Finelli, Christopher M. Pawlik, Joseph R. Erwin, Patrick M. Microbiome Research BACKGROUND: Sponges are important suspension-feeding members of reef communities, with the collective capacity to overturn the entire water column on shallow Caribbean reefs every day. The sponge-loop hypothesis suggests that sponges take up dissolved organic carbon (DOC) and, via assimilation and shedding of cells, return carbon to the reef ecosystem as particulate organic carbon (POC). Sponges host complex microbial communities within their tissues that may play a role in carbon and nutrient cycling within the sponge holobiont. To investigate this relationship, we paired microbial community characterization (16S rRNA analysis, Illumina Mi-Seq platform) with carbon (DOC, POC) and nutrient (PO(4), NO(x), NH(4)) flux data (specific filtration rate) for 10 common Caribbean sponge species at two distant sites (Florida Keys vs. Belize, ~ 1203 km apart). RESULTS: Distance-based linear modeling revealed weak relationships overall between symbiont structure and carbon and nutrient flux, suggesting that the observed differences in POC, DOC, PO(4), and NO(x) flux among sponges are not caused by variations in the composition of symbiont communities. In contrast, significant correlations between symbiont structure and NH(4) flux occurred consistently across the dataset. Further, several individual symbiont taxa (OTUs) exhibited relative abundances that correlated with NH(4) flux, including one OTU affiliated with the ammonia-oxidizing genus Cenarchaeum. CONCLUSIONS: Combined, these results indicate that microbiome structure is uncoupled from sponge carbon cycling and does not explain variation in DOC uptake among Caribbean coral reef sponges. Accordingly, differential DOC assimilation by sponge cells or stable microbiome components may ultimately drive carbon flux in the sponge holobiont. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0739-x) contains supplementary material, which is available to authorized users. BioMed Central 2019-08-29 /pmc/articles/PMC6716902/ /pubmed/31466521 http://dx.doi.org/10.1186/s40168-019-0739-x Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Gantt, Shelby E.
McMurray, Steven E.
Stubler, Amber D.
Finelli, Christopher M.
Pawlik, Joseph R.
Erwin, Patrick M.
Testing the relationship between microbiome composition and flux of carbon and nutrients in Caribbean coral reef sponges
title Testing the relationship between microbiome composition and flux of carbon and nutrients in Caribbean coral reef sponges
title_full Testing the relationship between microbiome composition and flux of carbon and nutrients in Caribbean coral reef sponges
title_fullStr Testing the relationship between microbiome composition and flux of carbon and nutrients in Caribbean coral reef sponges
title_full_unstemmed Testing the relationship between microbiome composition and flux of carbon and nutrients in Caribbean coral reef sponges
title_short Testing the relationship between microbiome composition and flux of carbon and nutrients in Caribbean coral reef sponges
title_sort testing the relationship between microbiome composition and flux of carbon and nutrients in caribbean coral reef sponges
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6716902/
https://www.ncbi.nlm.nih.gov/pubmed/31466521
http://dx.doi.org/10.1186/s40168-019-0739-x
work_keys_str_mv AT ganttshelbye testingtherelationshipbetweenmicrobiomecompositionandfluxofcarbonandnutrientsincaribbeancoralreefsponges
AT mcmurraystevene testingtherelationshipbetweenmicrobiomecompositionandfluxofcarbonandnutrientsincaribbeancoralreefsponges
AT stubleramberd testingtherelationshipbetweenmicrobiomecompositionandfluxofcarbonandnutrientsincaribbeancoralreefsponges
AT finellichristopherm testingtherelationshipbetweenmicrobiomecompositionandfluxofcarbonandnutrientsincaribbeancoralreefsponges
AT pawlikjosephr testingtherelationshipbetweenmicrobiomecompositionandfluxofcarbonandnutrientsincaribbeancoralreefsponges
AT erwinpatrickm testingtherelationshipbetweenmicrobiomecompositionandfluxofcarbonandnutrientsincaribbeancoralreefsponges