Dynamic epigenomic landscape of carbon-concentrating mechanisms in the model industrial oleaginous microalgaNannochloropsis oceanica

Abstract

AbstractDespite their ecological and physiological significance, how carbon-concentrating mechanisms (CCM) are regulated in microalgae remains elusive. Here in the model industrial microalgaNannochloropsis oceanica, we uncovered an epigenetic regulatory mechanism for CCM via comprehensive, multi-dimensional epigenomic analyses. Our integrated study reveals the complex interplay among histone modifications, dynamic nucleosome positioning, and 3D chromatin structure in regulating gene expression during low CO2adaptation, despite minimal DNA methylation. Histone modifications, including lysine acetylation (H3K9ac and H3K27ac), crotonylation (Kcr), and methylation (H3K4me2), were associated with active chromatin states. Significantly altered ChIP-Seq peaks were linked to 43.1% of the differentially expressed genes (DEGs). Notably, H3K4me2 exhibited a distinct dual-peak profile around the transcription start site (TSS), which is unique among microalgae and plants. Chromatin compartment dynamics were correlated with gene expression and histone modifications, particularly H3K4me2, while differentially positioned nucleosomes were associated with key CCM-related genes and transcription factors. To further elucidate the role of H3K4me2, we knocked out its methyltransferase, resulting in genome-wide H3K4me2 peak shifts, slower growth, and reduced photosynthesis. These changes were accompanied by differential expression of key genes of NoHINT and NoPMA2, whose subsequent deletion and overexpression revealed their subtle yet significant impacts on growth and photosynthetic efficiency under low CO2conditions, with NoHINT regulating growth and NoPMA2 influencing photosynthesis. Finally, we proposed a comprehensive model for epigenetic regulation of CCM inN. oceanica, which established a foundation for enhancing microalgal productivity through targeted epigenetic modifications.HighlightsMulti-layered epigenetic modifications contribute to the regulation of CCM and its adaptation to low CO2inN. oceanica.The histone modification H3K4me2 regulates the growth and photosynthesis ofN. oceanicaunder low CO2conditions.H3K4me2 targets NoHINT and NoPMA2 inN. oceanica, with NoHINT influencing growth dynamics and NoPMA2 modulating photosynthetic efficiency under low CO2conditions.