Life cycle and morphogenetic differentiation in heteromorphic cell types of a cosmopolitan marine microalga

Gephyrocapsa huxleyi is a prevalent, bloom-forming phytoplankton species in the oceans. It exhibits a complex haplodiplontic life cycle, featuring a diploid-calcified phase, a haploid phase and a third ‘decoupled’ phase produced during viral infection. Decoupled cells display a haploid-like phenotype, but are diploid. Here, we investigated the fate of decoupled cells during culture observations and we compared the transcriptome profiles and the cellular ultrastructure of the three life cycle cell types. We found that decoupled cells can revert to the calcified form in the absence of viral pressure, revealing the ability of G. huxleyi to modulate cell differentiation as a function of external conditions. Ultrastructural analyses showed distinct nuclear organization with variations in chromatin volume. Transcriptomic analyses revealed gene expression patterns specific to each life phase. These included multiple regulatory functions in chromatin remodeling, broader epigenetic mechanisms and life cycling, likely contributing to cell differentiation. Finally, analyses of available host–virus transcriptomes support life cycle transition during viral infection. This study provides cellular and molecular foundations for nuclear remodeling and cell differentiation in coccolithophores and the identification of gene markers for studying coccolithophore life cycles in natural populations.