Haplotype-aware multiomics unveils the regulatory basis of haplodiplontic life-cycle differentiation in a cosmopolitan marine alga

Gephyrocapsa huxleyi (formerly Emiliania huxleyi), a key coccolithophore alga influencing the global carbon cycle through photosynthesis and calcification, undergoes a haplodiplontic sexual life cycle with a calcifying non-flagellate diploid and a non-calcifying biflagellate haploid stage. To reveal the molecular basis of their morpho-physiological distinctions, we generated chromosome-level genome assemblies and compared the transcriptomes, proteomes, and methylomes for a pair of isogenic haploid and diploid model strains and conducted haplotype-aware analyses of their multiomic features. In addition to calcification and flagella, transcriptomes and proteomes of haploid and diploid cells modulate their differentiation in photosynthesis, sulfatases, DMSP degradation, DNA replication, and endomembrane system and transport. Haploid-diploid differential gene expression can be partially attributable to allelic imbalance (allele-specific expression) in diploid cells. Gene transcript abundance is positively associated with both CG and CHG gene-body DNA methylation, which can be inheritable, allele-specific, and differentiated between life-cycle phases. This multiomic study unravels the regulatory basis of unicellular algal life-cycle differentiation and provides valuable resources for investigating the ecologically important coccolithophore algae.