Epigenetic reprogramming of Nannochloropsis oceanica in response to CO 2 fluctuated environment

Abstract

Low CO2 could induce carbon concentrating mechanism (CCM) in majority of microalgae and CCM are regulated at RNA level are well known, however, epigenetic modifications and their potential regulation of the transcription of masked genes at the genome level in response to CO2 fluctuation remain unclear. Here we examine histone modifications and gene expression during CCM induction using ChIP-seq and mRNA-seq. Epigenetic regulation in response to CO2 fluctuation and epigenome-association with phenotypic plasticity of CCM are firstly uncovered in marine microalga Nannochloropsis oceanica IMET1. The result showed that lysine butyrylation (Kbu) and histone H3K9m2 modifications were present in N. oceanica IMET1. Moreover, Kbu positively regulated gene expression. In response to CO2 fluctuation, there were 5,438 and 1,106 genes regulated by Kbu and H3K9m2, respectively. Differential modifications were enriched in carbon fixation, photorespiration, photosynthesis, and lipid metabolism etc. For low carbon adaption, we observed that massively genome-wide epigenetic reprogramming would occur after N. oceanica cells shifted from high CO2 to low CO2. Gained or lost histone methylations were closely associated with activating or repressing gene expressions. Particularly, we firstly noted that the transcription of the key low CO2 responsive carbonic anhydrase (CA5), a key component involved in CCM stress signaling, was potentially regulated by bivalent Kbu-H3K9m2 modifications in microalgae. This study provides novel insights into epigenetic regulation in Nannochloropsis, which will lay foundation on genetic improvement of CCM at epigenetic level.