Life-cycle differentiation in a cosmopolitan calcifying microalga: a multiomic view

Gephyrocapsa huxleyi (formerly Emiliania huxleyi), a key microalga influencing the global carbon cycle through photosynthesis and calcification, undergoes a haplodiplontic sexual life cycle involving the alternation between a calcifying non-flagellate diploid and a non-calcifying biflagellate haploid stage. To unravel the molecular basis of their morphological and physiological distinctions, we applied a multi-omic approach, involving de novo genome reconstructions and comparisons of transcriptomes, proteomes, and methylomes for a pair of isogenic haploid and diploid model strains. Genomic sequences of the two life stages revealed unexpected structural variations, including aneuploidy, chromosome-level recombination, and partial loss of heterozygosity in the diploid during asexual reproduction. This provides a plausible explanation for the observed high genomic structure and size variation but low genetic variation among natural populations. In addition to calcification and flagella, transcriptomic and proteomic differences 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 the diploid. We also found that gene transcript abundance is correlated with patterns of DNA methylation, which occurs in CG and CHG contexts and can be inheritable, allele-specific, and differentiated between life-cycle phases. Our multiomic profiling and analyses offer insights into coccolithophore life-cycle differentiation, laying a robust foundation for investigating various biological processes in this phylogenetically distinct and ecologically crucial group of marine protists.

Primary Presenter: Chuan Ku, Academia Sinica (chuanku@gate.sinica.edu.tw)

Authors:

Tzu-Tong Kao, Academia Sinica, Taiwan  (tzutongkao@gate.sinica.edu.tw)

Ming-Wei Lai, Academia Sinica, Taiwan  (mwlai@gate.sinica.edu.tw)

Tzu-Haw Wang, Academia Sinica, Taiwan  (tzuhawwang@gate.sinica.edu.tw)

Chia-Ling Yang, Academia Sinica, Taiwan  (as0190267@gate.sinica.edu.tw)

Miguel Frada, Hebrew University of Jerusalem, Israel  (miguel.frada@mail.huji.ac.il)

Chuan Ku, Academia Sinica, Taiwan  (chuanku@gate.sinica.edu.tw)