Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress

Fan, Lu, Liu, Michael, Simister, Rachel, Webster, Nicole S. and Thomas, Torsten (2013) Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress. ISME Journal, 7 5: 991-1002. doi:10.1038/ismej.2012.165

Author Fan, Lu
Liu, Michael
Simister, Rachel
Webster, Nicole S.
Thomas, Torsten
Title Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress
Journal name ISME Journal   Check publisher's open access policy
ISSN 1751-7362
Publication date 2013-05-01
Year available 2013
Sub-type Article (original research)
DOI 10.1038/ismej.2012.165
Open Access Status Not Open Access
Volume 7
Issue 5
Start page 991
End page 1002
Total pages 12
Place of publication London, United Kingdom
Publisher Nature Publishing Group
Language eng
Abstract Large-scale mortality of marine invertebrates is a major global concern for ocean ecosystems and many sessile, reef-building animals, such as sponges and corals, are experiencing significant declines through temperature-induced disease and bleaching. The health and survival of marine invertebrates is often dependent on intimate symbiotic associations with complex microbial communities, yet we have a very limited understanding of the detailed biology and ecology of both the host and the symbiont community in response to environmental stressors, such as elevated seawater temperatures. Here, we use the ecologically important sponge Rhopaloeides odorabile as a model to explore the changes in symbiosis during the development of temperature-induced necrosis. Expression profiling of the sponge host was examined in conjunction with the phylogenetic and functional structure and the expression profile of the symbiont community. Elevated temperature causes an immediate stress response in both the host and symbiont community, including reduced expression of functions that mediate their partnership. Disruption to nutritional interdependence and molecular interactions during early heat stress further destabilizes the holobiont, ultimately leading to the loss of archetypal sponge symbionts and the introduction of new microorganisms that have functional and expression profiles consistent with a scavenging lifestyle, a lack virulence functions and a high growth rate. Previous models have postulated various mechanisms of mortality and disease in marine invertebrates. Our study suggests that interruption of symbiotic interactions is a major determinant for mortality in marine sessile invertebrates. High symbiont specialization and low functional redundancy, thus make these holobionts extremely vulnerable to environmental perturbations, including climate change.
Keyword Community stability
Functional redundancy
Marine disease
Microbial symbionts
Ocean warming
Q-Index Code C1
Q-Index Status Provisional Code
Institutional Status Non-UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: Non HERDC
Advanced Water Management Centre Publications
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Citation counts: TR Web of Science Citation Count  Cited 49 times in Thomson Reuters Web of Science Article | Citations
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Created: Tue, 02 Jul 2013, 01:09:16 EST by Chris Fan on behalf of Advanced Water Management Centre