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The influence of symbiosis on the proteome of the symbiotic dinoflagellate Breviolum

ABSTRACT: The physiology and cellular mechanisms of the dinoflagellate symbionts of cnidarians, the Symbiodiniaceae, change as a response to symbiosis, nutrient availability, and their surrounding microhabitat, but the underlying processes are poorly understood. Here, we employed liquid chromatography–mass spectrometry-based proteomics to elucidate the changes associated with the symbiotic and nutritional states of Breviolum minutum, a native symbiont of the sea anemone Exaiptasia diaphana. Both symbiosis and nutritional state had significant impacts on the B. minutum proteome. B. minutum in hospite showed increased abundance of proteins that are involved in phosphoinositol manipulation (e.g., glycerophosphoinositol permease 1 and phosphatidylinositol phosphatase), potentially as a means of interpartner signalling to prevent host phagosomal maturation. Proteins involved in carbon concentration and fixation (e.g. carbonic anhydrase, V-type ATPase) and nitrogen assimilation (e.g. glutamine synthase) were upregulated in ex hospite B. minutum, possibly due to nitrogen limitation by host in hospite and a lack of host carbon concentration mechanisms when ex hospite, respectively. Photosystem proteins increased in abundance at high nutrient levels, as were proteins involved in antioxidant mechanisms (e.g. superoxide dismutase, glutathione s-transferase). Proteins involved in iron metabolism was also affected by nutrient state, indicating increased iron demand and uptake in low nutrient treatments. These results provide better insight on the cellular mechanisms of symbiosis and provides potential target pathways for investigating a functional cnidarian-dinoflagellate symbiosis.

INSTRUMENT(S): Orbitrap Fusion Lumos

ORGANISM(S): Breviolum Minutum

SUBMITTER: Clinton Oakley

LAB HEAD: Simon Davy

PROVIDER: PXD036981 | Pride | 2023-01-31

REPOSITORIES: Pride

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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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The influence of symbiosis on the proteome of the symbiotic dinoflagellate Breviolum

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