Abstract
Eukaryotic organisms regulate the organization, structure, and accessibility of their genomes through chromatin remodeling that can be inherited as epigenetic modifications. These DNA and histone protein modifications are ultimately responsible for an organism’s molecular adaptation to the environment, resulting in distinctive phenotypes. Epigenetic manipulation of algae holds yet untapped potential for the optimization of biofuel production and bioproduct formation; however, epigenetic machinery and modes-of-action have not been well characterized in algae. We sought to determine the extent to which the biofuel platform species Picochlorum soloecismus utilizes DNA methylation to regulate its genome. We found candidate genes with domains for DNA methylation in the P. soloecismus genome. Whole-genome bisulfite sequencing revealed DNA methylation in all three cytosine contexts (CpG, CHH, and CHG). While global DNA methylation is low overall (∼1.15%), it occurs in appreciable quantities (12.1%) in CpG dinucleotides in a bimodal distribution in all genomic contexts, though terminators contain the greatest number of CpG sites per kilobase. The P. soloecismus genome becomes hypomethylated during the growth cycle in response to nitrogen starvation. Algae cultures were treated daily across the growth cycle with 20 μM 5-aza-2′-deoxycytidine (5AZA) to inhibit propagation of DNA methylation in daughter cells. 5AZA treatment significantly increased optical density and forward and side scatter of cells across the growth cycle (16 days). This increase in cell size and complexity correlated with a significant increase (∼66%) in lipid accumulation. Site specific CpG DNA methylation was significantly altered with 5AZA treatment over the time course, though nitrogen starvation itself induced significant hypomethylation in CpG contexts. Genes involved in several biological processes, including fatty acid synthesis, had altered methylation ratios in response to 5AZA; we hypothesize that these changes are potentially responsible for the phenotype of early induction of carbon storage as lipids. This is the first report to utilize epigenetic manipulation strategies to alter algal physiology and phenotype. Collectively, these data suggest these strategies can be utilized to fine-tune metabolic responses, alter growth, and enhance environmental adaption of microalgae for desired outcomes.
Highlights
Eukaryotic organisms control the organization and accessibly of their genomes via covalent modification of DNA and chromatin proteins
We found homologs for a number of enzymes involved in DNA methylation in the P. soloecismus genome, suggesting the possibility of DNA methylation in multiple contexts (Table 1A)
The three major findings of this work are as follows: (1) P. soloecismus has a small but quantifiable amount of global DNA methylation; (2) this methylation changes during the growth cycle of P. soloecismus in response to nitrogen starvation and 5-aza-2 -deoxycytidine (5AZA) treatment, leading to the induction of lipids; and (3) CpG sites exhibit dynamic methylation in genes involved in fatty acid biosynthesis and the cell cycle
Summary
Eukaryotic organisms control the organization and accessibly of their genomes via covalent modification of DNA and chromatin proteins. Epigenetic mechanisms regulate a plethora of processes in mammalian and plant species, ranging from the fidelity of DNA replication, repair, and protection to DNA transcription and expression (Jaenisch and Bird, 2003). Methylation of cytosines in DNA can occur in multiple genomic regions and dinucleotide contexts, including CpG, CHH, and CHG (where H corresponds to A, T or C). This DNA methylation is important for plant growth and dynamic responses to environmental perturbations and directly influences the plant’s phenotype (Zhang et al, 2018)
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