Pangenome biology and evolution in harmful algal-bloom-forming pelagophyte algae

Abstract

In prokaryotes lateral gene transfer (LGT) is a key mechanism leading to intra-species variability in gene content and the phenomenon of pangenomes. In microbial eukaryotes, however, the extent to which LGT-driven pangenomes exist is unclear. Pelagophytes are ecologically important marine algae that include Aureococcus anophagefferens - a species notorious for causing harmful algal blooms. To investigate genome evolution across Pelagophyceae and within Aureococcus anophagefferens, we used long-read sequencing to produce high-quality genome assemblies for five strains of Ac. anophagefferens (52-54 megabase-pairs; Mbp), a telomere-to-telomere assembly for Pelagomonas calceolata (32 Mbp), and the first reference genome for Aureoumbra lagunensis (41 Mbp). Using comparative genomics and phylogenetics, we show remarkable strain level genetic variation in Ac. anophagefferens with a pangenome (23,356 orthogroups) that is 81.1% core and 18.9% accessory. Although gene content variation within Ac. anophagefferens does not appear to be largely driven by recent prokaryotic LGTs (2.6% of accessory orthogroups), 368 orthogroups were acquired from bacteria in a common ancestor of all analyzed strains and are not found in P. calceolata or Au. lagunensis. 1,077 recent LGTs from prokaryotes and viruses were identified within Pelagophyceae overall, constituting 3.5-4.0% of the orthogroups in each species. This includes genes likely contributing to the ecological success of pelagophytes globally and in long-lasting harmful blooms.