Glucose-Induced Trophic Shift in an Endosymbiont Dinoflagellate with Physiological and Molecular Consequences

Abstract

Interactions between the dinoflagellate endosymbiont Symbiodinium and its cnidarian hosts (e.g. corals, sea anemones) are the foundation of coral-reef ecosystems. Carbon flow between the partners is a hallmark of this mutualism, but the mechanisms governing this flow and its impact on symbiosis remain poorly understood. We showed previously that although Symbiodinium strain SSB01 can grow photoautotrophically, it can grow mixotrophically or heterotrophically when supplied with Glc, a metabolite normally transferred from the alga to its host. Here we show that Glc supplementation of SSB01 cultures causes a loss of pigmentation and photosynthetic activity, disorganization of thylakoid membranes, accumulation of lipid bodies, and alterations of cell-surface morphology. We used global transcriptome analyses to determine if these physiological changes were correlated with changes in gene expression. Glc-supplemented cells exhibited a marked reduction in levels of plastid transcripts encoding photosynthetic proteins, although most nuclear-encoded transcripts (including those for proteins involved in lipid synthesis and formation of the extracellular matrix) exhibited little change in their abundances. However, the altered carbon metabolism in Glc-supplemented cells was correlated with modest alterations (approximately 2x) in the levels of some nuclearencoded transcripts for sugar transporters. Finally, Glc-bleached SSB01 cells appeared unable to efficiently populate anemone larvae. Together, these results suggest links between energy metabolism and cellular physiology, morphology, and symbiotic interactions. However, the results also show that in contrast to many other organisms, Symbiodinium can undergo dramatic physiological changes that are not reflected by major changes in the abundances of nuclear-encoded transcripts and thus presumably reflect posttranscriptional regulatory processes.

Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

“…Notably, 64% of the putative sugar transporters identified in our transcriptome were not differentially expressed. This corresponds with a study that documented relatively small changes in the expression of glucose transporters after supplementing B. minutum cultures with glucose, which concluded that these sugar transporters are not transcriptionally regulated (Xiang et al, 2018) but likely controlled at the post-transcriptional level, either by RNA editing or by microRNA (Aranda et al, 2013;S. Lin et al, 2015).…”

“…In plants, they are responsible for efflux and intracellular trafficking of sugars (Deng & Yan, ) and are localized to different cellular compartments (Feng & Frommer, ). SWEETs were previously identified in a B. minutum transcriptome (strain SSB01), and three out of seven transcripts were up‐regulated when the medium was supplemented with glucose (Xiang et al, ). Intriguingly, all but one (which did not pass the prediction probability threshold) of the SWEET transcripts in our transcriptome are predicted to reside in the plasma membrane.…”

Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations

“…2c). The upregulated transcripts might be those encoding transporters involved in exporting glucose from the endosymbiont to the host 17,18 . Overall, the transcript-level results support the hypothesis that SSB01 is specifically deficient for N in hospite.…”

Live imaging of Aiptasia larvae, a model system for studying coral bleaching, using a simple microfluidic device

“…Animal Culture and Maintenance. Small sea anemone (Aiptasia) larvae were cultured in the laboratory (21). Larvae were obtained via induced spawning of clonal adult Aiptasia anemone lines CC7 (male) and PLF3 (female) in paired co-culture in artificial sea water (ASW; 34 ppt Coral Pro Salt in deionized (DI) water, pH 8.0, Red Sea Inc.) (9).…”