Macroalgal deep genomics illuminate multiple paths to aquatic, photosynthetic multicellularity - ASSEMBLIES [INTERNATIONAL] - Data S1

Macroalgae are a polyphyletic group of multicellular aquatic organisms vital to global climate maintenance and have a wide variety of commercial applications. The lack of genomic datasets and poor physiological records preclude understanding their ecological roles and industrial potential. We de novo sequenced 121 macroalgal genomes from various climates spanning five major latitude parallels. The resultant genomic datasets reveal genetic bases for niche habitation facilitated by morphological complexity in diverse and extreme regions and illuminate the evolutionary mechanisms behind macroalgal diversification and specialization. Adhesome genes (e.g., cadherins, integrins, and lectins), extracellular matrix enzymes, and cytoskeletal organization regulating genes (e.g., spondins, Rho-type GTPases) predominantly distinguished macroalgal genomes from their microalgae correlates. Deep neural networks could accurately classify an alga as micro- or macro- from set of significance-ranked genomic features (n = 251, entropy R² > 0.99, RASE = 0.001) as well as adhesome gene sets (n = 110, entropy R² > 0.86). By deciphering the macroalgal adhesome, a clear picture of the genetic basis for the development and maintenance of complex algal tissues could be resolved. Sequences from giant viruses were rampant in the macroalgal genomes and coded for zinc-finger transcription factors, ankyrins, Rieske proteins, and other exotic codomains. Lineage-specific retentions of transcription factors, cadherins, integrins, polysaccharide-acting enzymes, and receptor kinases, many with predicted viral origins, outline the divergent mechanisms facilitating multicellularity in these three macroalgal lineages. This work sheds new light on the evolution of multicellularity in three phyla (Rhodophyceae, Chlorophyceae, and Ochrophyceae v. Phaeophyceae) through the lens of large-scale genomics and paves the way for the genomic exploration of macroalgal biology.