The Genome of Bangia fuscopurpurea Illustrates Early Establishment of Multicellularity and Intertidal Adaptation in Red Algae

Abstract The billion-year-old fossil red alga Bangiomorpha pubescens represents the oldest taxonomically resolved multicellular eukaryote, morphologically indistinguishable from the extant intertidal alga Bangia fuscopurpurea. Here, we report a chromosome-level 107.55 Mb genome assembly of B. fuscopurpurea. Phylogenomic analysis confirms its placement as the most basal multicellular red algal lineage, diverging ∼973.40 million years ago. The genome reveals lineage-specific expansion of Osvaldo-type LTR retrotransposons that influence generation-specific gene expression. Metabolically, B. fuscopurpurea relies exclusively on the methylerythritol phosphate pathway for terpenoid biosynthesis, lacking the mevalonate pathway. Genomic analysis reveals the presence of core abscisic acid biosynthetic genes alongside partial of other hormone pathway components, suggesting that fundamental phytohormone biosynthetic capacity was established in early red algal lineages. Multi-omics profiling reveals pronounced transcriptional and epigenetic differences between haploid gametophytes and diploid sporophytes, with distinct generation-specific DNA methylation patterns (5mC and 6mA). Time-series transcriptomic analyses identified 2,320 rhythmically expressed genes exhibiting diurnal patterns aligned with intertidal environmental fluctuations, including reactive oxygen species detoxification genes peaking at dusk and photoprotective genes at dawn. These findings illuminate the genomic innovations underlying early multicellular evolution, life cycle regulation, and intertidal adaptation in ancient red algae, establishing B. fuscopurpurea as a critical reference for understanding photosynthetic eukaryote diversification.