Algal epigenetics: insights from DNA methylation in a symbiotic dinoflagellate

Fugacium kawagutii (formerly known as Symbiodinium kawagutii; Fig. 1) is a marine photosynthetic dinoflagellate that is thought to be an endosymbiont of corals (Baker 2003). In this mutualistic symbiosis, corals provide inorganic nutrients and shelter to the symbiotic algae, while the algae provide the coral hosts with organic carbon to satisfy their energy needs (Burriesci et al. 2012). Dinoflagellate genomes are known for extensive methylation, permanently condensed chromosomes, and large genomes (Lin 2011). The genome of F. kawagutii, along with those of five other Symbiodiniaceae algae, has been sequenced; the quality of these sequences is continually being improved (Lin et al. 2015, Liu et al. 2018). While these genome assemblies are still mostly incomplete, researchers are beginning to exploit them to understand the molecular basis of dinoflagellate evolution and coral symbiosis. Epigenetic machineries involved in histone H3 lysine methylation, DNA methylation, and RNA interference are present in many eukaryotic microalgae (Kim et al. 2015). Epigenetic regulation plays an important role in adaptation processes of microalgae, allowing them to quickly alter gene expression in response to fluctuating environmental conditions such as light intensity, temperature, pH, and salinity (Bacova et al. 2020). DNA methylation is a well-studied epigenetic mechanism that involves the transfer of a methyl group to cytosine at the CG position by DNA methyltransferases (DNMTs; Lyko 2018). Two groups of DNMT are present in eukaryotes: (1) maintenance DNMT (such as Dnmt1) that maintain methylation patterns during cell division, and (2) de novo DNMT (such as Dnmt3) that establish new methylation sites on the genome (Lyko 2018). A recent study shows that a putative Dnmt3 of Fugacium kawagutii (Symbio-DIRS-Dnmt3) can catalyze de novo CG methylation in the budding yeast Saccharomyces cerevisiae (de Mendoza et al. 2018). Interestingly, the Symbio-DIRS-Dnmt3 gene is associated with retrotransposons in F. kawagutii; the encoded protein likely “self-methylate” retrotranscribed DNA with a pattern of methylation similar to that of the cell’s genomic DNA. Domestication of transposon-derived proteins has been found to benefit the host as part of defense systems that combat infectious agents such as viruses and transposon elements themselves (Jangam et al. 2017). Discovery of active DNMTs encoded by retrotransposons of F. kawagutii suggests that transposons are also able to “steal” genes (such as DNMTs) involved in epigenetic regulation from their host; this theft can contribute to retrotransposon “survival” in the host and the development of new and adaptive host and retrotransposon features (de Mendoza et al. 2018). How DNMTs regulate gene methylation and expression dynamics in algae remain poorly understood. The work of Yang et al. (2020) sets out to address these questions through exploring the expression dynamics of Symbio-DIRS-Dnmt3 and several photosynthetic genes in Fugacium kawagutii. Their work revealed that an increased transcript level of Symbio-DIRS-Dnmt3 in F. kawagutii grown under elevated light intensity directly correlated with elevated methylation of the peridinin-chlorophyll (chl) a binding protein (PCP) gene. By contrast, the peridinin-chl a/c binding protein (acpPC) gene body methylation level was inversely correlated with expression of the Symbio-DIRS-Dnmt3 gene. These results suggest that Symbio-DIRS-Dnmt3 methylating activity may play a role in regulating PCP methylation under fluctuating light intensities, while the acpPC gene may be regulated by DNA demethylation (not associated with Symbio-DIRSDnmt3 expression) as the intensity of the light increases. The authors propose that methylation levels and expression of F. kawagutii photosynthetic genes such as PCP are modulated by fluctuating light intensities as a consequence of transcriptional regulation of Symbio-DIRS-Dnmt3. However, these findings are still only correlative, but if substantiated by further studies, they would greatly advance our understanding on how DNMTs regulate DNA methylation and gene expression in algae. In evaluating the relationship between the levels of methylation of PCP, acpPC, and the light-harvesting complex protein (LHC) gene bodies and the expression of these genes, Yang et al. (2020) J. Phycol. 59, 289–291 (2023) © 2022 Phycological Society of America DOI: 10.1111/jpy.13090