Mapping the transcriptional landscape of algal resistance to viral infection reveals a core expression program

Algal blooms and their demise by viruses drive global-scale ecological processes in the ocean. These blooms form the foundation of marine food webs, regulate microbial communities, and shape biogeochemical cycles. Although algal populations are constantly infected by viruses, resistant subpopulations frequently emerge after the infection. Yet, antiviral molecular mechanisms of marine microalgae are underexplored. We used a model system of the ubiquitous microalga Emiliania huxleyi and its giant virus, E. huxleyi virus (EhV), to study how resistant populations evolve and to identify their transcriptional programs. We generated a detailed temporal transcriptomic dataset during a viral infection, covering the stages of lysis and the recovery of a resistant subpopulation. Viral infection triggered prominent transcriptome changes to support viral propagation, followed by a unique transcriptional response in resistant cells. Both infected and resistant cells highly expressed innate immune response genes, notably those with Toll/interleukin-1 receptor (TIR) domains. Additionally, resistant cells expressed genes involved in membrane-bound glycan remodeling, sphingolipid metabolism, and nutrient uptake. Using comparative transcriptomics across diverse resistant E. huxleyi strains, we identified a core group of resistance-related genes, providing a set of gene markers to detect this rare phenotype during the host-virus arms race in algal blooms.