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The transcriptomic response of the coral Acropora digitifera to a competent Symbiodinium strain: the symbiosome as an arrested early phagosome

ABSTRACT: Despite the ecological significance of the relationship between reef-building corals and intracellular photosynthetic dinoflagellates of the genus Symbiodinium, very little is known about the molecular mechanisms involved in the establishment of the relationship. Indeed, microarray-based analyses point to the conclusion that host gene expression is largely or completely unresponsive during the establishment of symbiosis with a competent strain of Symbiodinium. In the present study, the use of Illumina RNAseq technology allowed detection of a transient period of differential expression involving a small number of genes (1073 transcripts; <3% of the transcriptome) 4h after the exposure of Acropora digitifera planulae to a competent strain of Symbiodinium (a clade B strain). This phenomenon has not previously been detected as a consequence of both the lower sensitivity of the microarray approaches used and the sampling times used. The results imply that complex changes occur, including transient suppression of mitochondrial metabolism and protein synthesis, but are also consistent with the hypothesis that the symbiosome is a phagosome that has undergone early arrest, raising the possibility of common mechanisms in the symbiotic interactions of corals and symbiotic sea anemones with their endosymbionts.

ORGANISM(S): Acropora digitifera

PROVIDER: GSE76976 | GEO | 2016/04/03

SECONDARY ACCESSION(S): PRJNA309168

REPOSITORIES: GEO

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The transcriptomic response of the coral Acropora digitifera to a competent Symbiodinium strain: the symbiosome as an arrested early phagosome

Project description:Despite the ecological significance of the relationship between reef-building corals and intracellular photosynthetic dinoflagellates of the genus Symbiodinium, very little is known about the molecular mechanisms involved in the establishment of the relationship. Indeed, microarray-based analyses point to the conclusion that host gene expression is largely or completely unresponsive during the establishment of symbiosis with a competent strain of Symbiodinium. In the present study, the use of Illumina RNAseq technology allowed detection of a transient period of differential expression involving a small number of genes (1073 transcripts; <3% of the transcriptome) 4h after the exposure of Acropora digitifera planulae to a competent strain of Symbiodinium (a clade B strain). This phenomenon has not previously been detected as a consequence of both the lower sensitivity of the microarray approaches used and the sampling times used. The results imply that complex changes occur, including transient suppression of mitochondrial metabolism and protein synthesis, but are also consistent with the hypothesis that the symbiosome is a phagosome that has undergone early arrest, raising the possibility of common mechanisms in the symbiotic interactions of corals and symbiotic sea anemones with their endosymbionts. There were 2 conditions (Symbiodinium-infected and control). Samples were taken at 3 time points, there were 3 replicates per condition. 16 samples were analysed comparing the Symbiodinium-infected samples to the control ones

2016-04-03 | E-GEOD-76976 | biostudies-arrayexpress

The host transcriptome remains unaltered during the establishment of coral-algal symbioses

Project description:Coral reefs are based on the symbiotic relationship between corals and photosynthetic dinoflagellates of the genus Symbiodinium. We followed gene expression of coral larvae of Acropora palmata and Montastraea faveolata after exposure to Symbiodinium strains that differed in their ability to establish symbioses. We show that the coral host transcriptome remains almost unchanged during infection by competent symbionts, but is massively altered by symbionts that fail to establish symbioses. Our data suggest that successful coral-algal symbioses depend mainly on the symbionts' ability to enter the host in a stealth manner rather than a more active response from the coral host. Acropora palmata Samples: Three biological replicates of pooled larvae from each species and condition (i.e. untreated control, inoculated with competent Symbiodinium strain, inoculated with incompetent Symbiodinium strain) for both time points were hybridized against a pooled reference. Pooled references were constructed by combining equal amounts of aRNA from all control samples from A. palmata. References were labeled with Cy3, samples with Cy5. Montastraea faveolata Samples: Three biological replicates of pooled larvae from each species and condition (i.e. untreated control, inoculated with competent Symbiodinium strain, inoculated with incompetent Symbiodinium strain) for both time points were hybridized against a pooled reference. Pooled references were constructed by combining equal amounts of aRNA from all control samples from M. faveolata. References were labeled with Cy3, samples with Cy5. Symbiodinium sp. CassKB8: competent strain Symbiodinium sp. EL1: incompetent strain Symbiodinium sp. Mf1.05b: competent strain

2010-06-20 | E-GEOD-14923 | biostudies-arrayexpress

The host transcriptome remains unaltered during the establishment of coral-algal symbioses

2009-04-01 | GSE14923 | GEO

Symbiosis induces widespread changes in the proteome of the model cnidarian Aiptasia

Project description:Coral reef ecosystems are metabolically founded on the mutualism between corals and photosynthetic dinoflagellates of the genus Symbiodinium. The glass anemone Aiptasia sp. has become a tractable model for this symbiosis. We utilized label-free liquid chromatography electrospray-ionization tandem mass spectrometry to analyze the effects of symbiosis on the proteomes of symbiotic and aposymbiotic Aiptasia. We quantified more than 3,300 proteins in 1,578 protein clusters, with 81 protein clusters showing significantly different expression. Symbiotic anemones showed higher expression of proteins involved in lipid storage and transport, nitrogen transport and cycling, intracellular trafficking, endocytosis and inorganic carbon transport. These changes reflect shifts in host metabolism and energy reserves due to increased organic and inorganic nutritional exchange with the symbionts. Aposymbiotic anemones exhibited increased expression of multiple systems responsible for mediating reactive oxygen stress, suggesting that the host derives direct or indirect protection from oxidative stress while in symbiosis. Aposymbiotic anemones also increased their expression of an array of proteases and chitinases, indicating a metabolic shift from autotrophy to heterotrophy. These results provide a comprehensive Aiptasia proteome with more direct relative quantification of protein abundance than transcriptomic methods, allowing more powerful studies of coral physiology and ecosystem function.

2017-02-22 | PXD003202 | Pride

Sex, Scavengers, and Chaperones: Transcriptome Secrets of Divergent Symbiodinium Thermal Tolerances

Project description:Using transcriptomics, we show that Symbiodinium acclimation to elevated temperature involves up-regulated expression of meiosis genes followed by up-regulated expression of numerous reactive oxygen species scavenging genes and molecular chaperone genes. Our study connects Symbiodinium transcriptional regulation with physiological heat stress responses as well as known bleaching responses of corals harboring these same Symbiodinium. By uncovering these critical links, we greatly advance understanding of the bleaching susceptibility of corals, which is a key process responsible for global coral reef health.

2016-06-08 | GSE72763 | GEO

Gene expression of settled and metamorphosed Orbicella faveolata during establishment of symbiosis

Project description:Corals rely on a symbiosis with dinoflagellate algae (Symbiodinium spp.) to thrive in nutrient poor tropical oceans. However, the coral-algal symbiosis can break down during bleaching events, potentially leading to coral death. While genome-wide expression studies have shown the genes associated with the breakdown of this partnership, the full conglomerate of genes responsible for the establishment and maintenance of a healthy symbiosis remains unknown. Results from previous studies suggested little transcriptomic change associated with the establishment of symbiosis. In order to elucidate the transcriptomic response of the coral host in the presence of its associated symbiont, we utilized a comparative framework. Post-metamorphic aposymbiotic coral polyps of Orbicella faveolata were compared to symbiotic coral polyps 9 days after metamorphosis and the subsequent differential gene expression between control and treatment was quantified using cDNA microarray technology. Coral polyps exhibited differential expression of genes associated with nutrient metabolism and development, providing insight into pathways turned as a result of symbiosis driving early polyp growth. Furthermore, genes associated with lysosomal fusion were also upregulated, suggesting host regulation of symbiont densities soon after infection.

2016-12-22 | GSE92695 | GEO

The transcriptomic response to heat stress and bleaching in the Elkhorn coral Acropora palmata

Project description:The emergence of genomic tools for reef-building corals and symbiotic anemones comes at a time when alarming losses in coral cover are being observed worldwide. These tools hold great promise in elucidating novel and unforeseen cellular processes underlying the successful mutualism between corals and their algal endosymbionts (Symbiodinium spp.). Since thermal stress triggers a breakdown in the symbiosis (coral bleaching), measuring the transcriptomic response to thermal stress-induced bleaching offers an extraordinary view of the cellular processes specific to coral-algal symbioses. In the present study, we utilized a cDNA microarray containing 2,059 genes of the Caribbean Elkhorn coral Acropora palmata to identify genes differentially expressed upon thermal stress. Fragments from four separate colonies were exposed to elevated temperature (3˚C increase) for two days, and samples were frozen for microarray analysis after 24 and 48 hours. Fragments experienced a 60% reduction in algal cell density after two days. 204 genes were differentially expressed in samples collected one day after thermal stress; in samples collected after two days, 104 genes. Annotations of the differentially expressed genes indicate a conserved cellular stress response in A. palmata involving: 1) growth arrest; 2) chaperone activity; 3) nucleic acid stabilization and repair; and 4) the removal of damaged macromolecules. Other differentially expressed processes include sensory perception, metabolite transfer between host and symbiont, nitric oxide signaling, and modifications to the actin cytoskeleton and extracellular matrix. The results are also compared to those from a previous coral microarray study of thermal stress in Montastraea faveolata.

2009-10-31 | GSE16151 | GEO

Transcriptomic adaptations to symbiotic life in cnidarians: symbiotic vs bleached Anemonia viridis sea anemones

Project description:Transcriptional comparison between symbiotic and non-symbiotic (bleached) sea anemones Anemonia viridis were analysed in several specimens. We generated an oligonucleotide microarray (2000 selected features), which is to date the only available oligonucleotide array for symbiotic cnidarians. We were able to identify a subset of genes clearly involved in symbiosis.

2011-06-01 | GSE22360 | GEO

Symbiosis in Anemonia viridis sea anemones

Project description:This SuperSeries is composed of the following subset Series: GSE22360: Transcriptomic adaptations to symbiotic life in cnidarians : symbiotic vs bleached Anemonia viridis sea anemones GSE22361: Endoderm- vs ectoderm-specific expression of symbiosis genes in the snakelocks sea anemone Refer to individual Series

2011-06-01 | E-GEOD-22375 | biostudies-arrayexpress

Endoderm- vs ectoderm-specific expression of symbiosis genes in the snakelocks sea anemone

Project description:Transcriptional comparison between endodermal and ectodermal compartment in symbiotic sea anemones Anemonia viridis were analysed in several specimens. We generated an oligonucleotide microarray (2000 selected features), which is to date the only available oligonucleotide array for symbiotic cnidarians. We were able to identify a subset of genes clearly involved in symbiosis.

2011-06-01 | GSE22361 | GEO

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