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Proteomics quantifies protein expression changes in a model cnidarian colonised by a thermally tolerant but suboptimal symbiont

ABSTRACT: The acquisition of thermally tolerant algal symbionts by corals has been proposed as a natural or assisted mechanism of increasing coral reef resilience to anthropogenic climate change, but the cell-level processes determining the performance of new symbiotic associations are poorly understood. We used liquid chromatography-mass spectrometry to investigate the effects of an experimentally-induced symbiosis on the host proteome of the model sea anemone Exaiptasia pallida. Aposymbiotic specimens were colonised by either the homologous dinoflagellate symbiont (Breviolum minutum) or a thermally tolerant, ecologically invasive heterologous symbiont (Durusdinium trenchii). Anemones containing D. trenchii exhibited minimal expression of Niemann-Pick C2 proteins, which have predicted biochemical roles in sterol transport and cell recognition, and glutamine synthetases, which are thought to be involved in nitrogen assimilation and recycling between partners. D. trenchii-colonised anemones had higher expression of methionine-synthesizing betaine–homocysteine S-methyltransferases and proteins with predicted oxidative stress response functions. Multiple lysosome-associated proteins were less abundant in both symbiotic treatments compared with the aposymbiotic treatment. The differentially abundant proteins are predicted to represent pathways that may be involved in nutrient transport or resource allocation between partners. These results provide targets for specific experiments to elucidate the mechanisms underpinning compensatory physiology in the coral–dinoflagellate symbiosis.

INSTRUMENT(S): LTQ Orbitrap

ORGANISM(S): Exaiptasia Pallida

TISSUE(S): Whole Body

SUBMITTER: Clinton Oakley

LAB HEAD: Simon K Davy

PROVIDER: PXD009253 | Pride | 2019-05-27

REPOSITORIES: Pride

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			Action	DRS
	AipInf_150-1_120516.mzid	Mzid
	AipInf_150-1_120516.mzid_AipInf_150-1_120516.MGF	Mzid
	AipInf_150-1_120516.raw	Raw
	AipInf_150-1_120516_160514100740.mzid	Mzid
	AipInf_150-1_120516_160514100740.mzid_AipInf_150-1_120516_160514100740.MGF	Mzid

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Project description:Coral bleaching has devastating effects on coral survival and reef ecosystem function, but many of the fundamental cellular effects of thermal stress on cnidarian physiology are unclear. We used label-free liquid chromatography-tandem mass spectrometry to assess the effects of high temperatures on the proteome of the model symbiotic anemone Aiptasia sp. Anemones were acclimated to elevated temperatures (30 °C and 33.5 °C) for two weeks or exposed to short-term thermal shock (33.5 °C, 24 hours) without acclimation. We identified 2,137 protein clusters in Aiptasia, 136 of which were differentially abundant between treatments. There were minimal differences (nine proteins) in protein abundances between the control (25 °C) and acclimated high-temperature (30 °C and 33.5 °C) treatments, indicating that thermal acclimation in symbiotic cnidarians is not primarily regulated at the level of protein expression. Heat shock resulted in significant changes in the abundance of 104 proteins, including those involved in protein folding and synthesis, redox homeostasis, and central metabolism. Nineteen highly abundant cytoskeletal and structural proteins showed particularly reduced abundance (approximately 50%), demonstrating proteostasis disruption and inhibition of protein synthesis. Heat shock induced proteins involved in multiple mechanisms for stabilizing nascent proteins, preventing protein aggregation and degrading damaged proteins, indicative of endoplasmic reticulum stress. Antioxidant mechanisms and metabolic enzymes necessary for redox homeostasis were also upregulated. Disruption of host proteostasis occurred before either bleaching or symbiont photoinhibition was detected, strongly suggesting endogenous reactive oxygen species production as the proximate cause of thermal damage. The effects of thermal shock were most pronounced at the endoplasmic reticulum, and proteostasis maintenance and protein turnover mechanisms may be essential in the response to severe thermal stress in symbiotic cnidarians.

Project description:Background: Cnidarian – dinoflagellate intracellular symbioses are one of the most important mutualisms in the marine environment. They form the trophic and structural foundation of coral reef ecosystems, and have played a key role in the evolutionary radiation and biodiversity of cnidarian species. Despite the prevalence of these symbioses, we still know very little about the molecular modulators that initiate, regulate, and maintain the interaction between these two different biological entities. In this study, we conducted a comparative host anemone transcriptome analysis using a cDNA microarray platform to identify genes involved in cnidarian – algal symbiosis. Results: We detected statistically significant differences in host gene expression profiles between sea anemones (Anthopleura elegantissima) in a symbiotic and non-symbiotic state. The group of genes, whose expression is altered, is diverse, suggesting that the molecular regulation of the symbiosis is governed by changes in multiple cellular processes. In the context of cnidarian – dinoflagellate symbioses, we discuss pivotal host gene expression changes involved in lipid metabolism, cell adhesion, cell proliferation, apoptosis, and oxidative stress. Conclusion: Our data do not support the existence of symbiosis-specific genes involved in controlling and regulating the symbiosis. Instead, it appears that the symbiosis is maintained by altering expression of existing genes involved in vital cellular processes. Specifically, the finding of key genes involved in cell cycle progression and apoptosis have led us to hypothesize that a suppression of apoptosis, together with a deregulation of the host cell cycle, create a platform that might be necessary for symbiont and/or symbiont-containing host cell survival. This first comprehensive molecular examination of the cnidarian – dinoflagellate associations provides critical insight into the maintenance and regulation of the symbiosis. Keywords: comparative genomic hybridization

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Proteomics quantifies protein expression changes in a model cnidarian colonised by a thermally tolerant but suboptimal symbiont

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