Transcriptomics of lifestyle transition in coral symbionts: Symbiosis-derived transcriptional repression
The majority of corals acquire symbionts from the environment through horizontal transmission, whereby the coral hosts in their early life history stages take up symbionts from the environment. While larvae are not the only coral life history stage at which symbiont acquisition can occur, larval stages provide a unique opportunity to study the initiation of the mutualism. Previous transcriptomic work on this topic has focused almost exclusively on the host side of the relationship, largely due to inadequate genomic and transcriptomic data for Symbiodinaceae. This imbalance is partly addressed in this paper. Symbiodiniaceae are facultative symbionts as they can be found in cnidarian hosts (in a coccoid form) or free-living in water column or sediments (in gymnodinioid form). Coral larvae represent a unique symbiont-free stage to study establishment of coral-Symbiodiniaceae symbioses.
Following spawning of Acropora tenuis colonies at the SeaSim, AIMS in November 2014. Coral larvae (planulae) were exposed to a native symbiont (Cladocopium goreaui; ITS2 type C1) and sampled at 3, 12, 48 and 72h post exposure. Total RNA was isolated and cDNA libraries were prepared and sequenced using illumina platform to obtain ~ 35 million paired end (PE) reads per sample. Mapping these data against the symbiont transcriptome estimated the abundance of each transcripts. These data were compared with RNA-Seq data for a cultured C. goreaui as a proxy for the free-living lifestyle. The application of high-throughput sequencing methods permitted the detection of thousands of genes that were differentially expressed in the algal symbiont during colonising the coral host relative to the cultured algae.
In this paper, thousands of genes were deferentially expressed in symbiotic condition. The algal response to the symbiotic lifestyle was complex, one aspect of this being suppression of transcription of a wide range of genes “symbiosis-derived transcriptional repression”. This molecular response is consistent with the idea that the algal niche in hospite represents a very stable environment compared to the free-living condition. This phenomenon may reflect an adjustment to relatively stable intracellular conditions rather than the variable and unpredictable external environment. The fact that extensive genome reduction is not seen in Symbiodiniaceae presumably reflects the fact that most or all members of this group have a free-living stage, requiring the retention of the ability to respond to changing conditions. The dramatic decrease in transcriptome complexity observed here in adjusting to the symbiotic state may be analogous to the genome reduction observed in many obligate associations. This mechanism might enable algal symbionts turn expressions of a suite of genes (ON and OFF) according to changes in lifestyle. So some genes are repressed only in symbiosis, but they are still functional in the free-living state and that can explain the facultative nature of Symbiodiniaceae .
Against the background of genome-wide transcriptional repression, the predicted functions of the genes upregulated in the symbiotic state reveals transcriptional signals of active symbiont to host metabolite translocation at the host larval stage. Results presented here suggest that, whereas in free-living Symbiodiniaceae fixed carbon in excess of immediate requirements likely accumulates in glycogen and/or starch, in symbiosis the balance shifts to glycogen / starch breakdown; limit dextrinase is upregulated to enable glucose mobilization, glycogen synthase is downregulated and the carbohydrate transporter R144.6 is activated. These results provide the first evidence of active metabolic response from the symbiont to translocate glucose to the coral host at this early stage of symbiosis.
In a sense, the interaction studied here, between algal symbionts and coral larvae can be viewed as the opposite of what happens during coral bleaching - where symbionts depart their host during stress. A corollary of this idea is that genes associated with the initial infection process might be informative in assessment of the fitness of coral colonies. On the host side of this interaction, the small GTPases Rab4/5 and Rab7, together with their nucleotide exchange factors, may be considered indicators of the likely stability of the interaction, because of their likely roles in regulating phagosome maturation (Mohamed et al., 2016). On the Symbiodiniaceae side of the interaction, genes implicated in flagellar motility may be similarly informative. The differential expression analyses described in the paper indicate that the flagellar motility genes ODA4 and CFAP58 were downregulated throughout the infection process.
The results presented here are the first to document large-scale gene expression profiles of Symbiodiniaceae in a coral host, the transcriptional responses providing new insights into the potential metabolic contributions of Symbiodiniaceae to the coral association. The preprint version of the paper is available @bioRxiv entitled "Transcriptomic insights into the establishment of coral-algal symbioses from the symbiont perspective"
The majority of corals acquire symbionts from the environment through horizontal transmission, whereby the coral hosts in their early life history stages take up symbionts from the environment. While larvae are not the only coral life history stage at which symbiont acquisition can occur, larval stages provide a unique opportunity to study the initiation of the mutualism. Previous transcriptomic work on this topic has focused almost exclusively on the host side of the relationship, largely due to inadequate genomic and transcriptomic data for Symbiodinaceae. This imbalance is partly addressed in this paper. Symbiodiniaceae are facultative symbionts as they can be found in cnidarian hosts (in a coccoid form) or free-living in water column or sediments (in gymnodinioid form). Coral larvae represent a unique symbiont-free stage to study establishment of coral-Symbiodiniaceae symbioses.
Following spawning of Acropora tenuis colonies at the SeaSim, AIMS in November 2014. Coral larvae (planulae) were exposed to a native symbiont (Cladocopium goreaui; ITS2 type C1) and sampled at 3, 12, 48 and 72h post exposure. Total RNA was isolated and cDNA libraries were prepared and sequenced using illumina platform to obtain ~ 35 million paired end (PE) reads per sample. Mapping these data against the symbiont transcriptome estimated the abundance of each transcripts. These data were compared with RNA-Seq data for a cultured C. goreaui as a proxy for the free-living lifestyle. The application of high-throughput sequencing methods permitted the detection of thousands of genes that were differentially expressed in the algal symbiont during colonising the coral host relative to the cultured algae.
In this paper, thousands of genes were deferentially expressed in symbiotic condition. The algal response to the symbiotic lifestyle was complex, one aspect of this being suppression of transcription of a wide range of genes “symbiosis-derived transcriptional repression”. This molecular response is consistent with the idea that the algal niche in hospite represents a very stable environment compared to the free-living condition. This phenomenon may reflect an adjustment to relatively stable intracellular conditions rather than the variable and unpredictable external environment. The fact that extensive genome reduction is not seen in Symbiodiniaceae presumably reflects the fact that most or all members of this group have a free-living stage, requiring the retention of the ability to respond to changing conditions. The dramatic decrease in transcriptome complexity observed here in adjusting to the symbiotic state may be analogous to the genome reduction observed in many obligate associations. This mechanism might enable algal symbionts turn expressions of a suite of genes (ON and OFF) according to changes in lifestyle. So some genes are repressed only in symbiosis, but they are still functional in the free-living state and that can explain the facultative nature of Symbiodiniaceae .
Against the background of genome-wide transcriptional repression, the predicted functions of the genes upregulated in the symbiotic state reveals transcriptional signals of active symbiont to host metabolite translocation at the host larval stage. Results presented here suggest that, whereas in free-living Symbiodiniaceae fixed carbon in excess of immediate requirements likely accumulates in glycogen and/or starch, in symbiosis the balance shifts to glycogen / starch breakdown; limit dextrinase is upregulated to enable glucose mobilization, glycogen synthase is downregulated and the carbohydrate transporter R144.6 is activated. These results provide the first evidence of active metabolic response from the symbiont to translocate glucose to the coral host at this early stage of symbiosis.
In a sense, the interaction studied here, between algal symbionts and coral larvae can be viewed as the opposite of what happens during coral bleaching - where symbionts depart their host during stress. A corollary of this idea is that genes associated with the initial infection process might be informative in assessment of the fitness of coral colonies. On the host side of this interaction, the small GTPases Rab4/5 and Rab7, together with their nucleotide exchange factors, may be considered indicators of the likely stability of the interaction, because of their likely roles in regulating phagosome maturation (Mohamed et al., 2016). On the Symbiodiniaceae side of the interaction, genes implicated in flagellar motility may be similarly informative. The differential expression analyses described in the paper indicate that the flagellar motility genes ODA4 and CFAP58 were downregulated throughout the infection process.
The results presented here are the first to document large-scale gene expression profiles of Symbiodiniaceae in a coral host, the transcriptional responses providing new insights into the potential metabolic contributions of Symbiodiniaceae to the coral association. The preprint version of the paper is available @bioRxiv entitled "Transcriptomic insights into the establishment of coral-algal symbioses from the symbiont perspective"
