DYNAMIC GENOME EVOLUTION BETWEEN AND WITHIN SPECIES OF PELAGOPHYTE ALGAE

Abstract

The Pelagophyceae are an ecologically important, but genomically understudied, group of marine stramenopile algae, including Aureococcus anophagefferens and Aureoumbra lagunensis – two species infamous for causing harmful algal blooms (HABs). Despite their ecological significance, relatively few genomic studies have focused on pelagophytes, with only a single reference genome available until recently. The concept of a pangenome readily applies to prokaryotes, where lateral gene transfer (LGT) is one mechanism that contributes to enormous intra-species protein-coding gene variability. In microbial eukaryotes, however, the extent to which LGT-driven pangenomes exist is uncertain. To explore genome evolution across the Pelagophyceae and within Aureococcus anophagefferens, I generated long-read sequencing-based genome assemblies for five strains of Aureococcus anophagefferens (CCMP1707, CCMP1708, CCMP1850, CCMP1984 and CCMP3368) (52-54 Mbp), a fully resolved six chromosome genome assembly for Pelagomonas calceolata CCMP1756 (32 Mbp), and the first reference genome for Aureoumbra lagunensis CCMP1510 (41 Mbp). Comparative genomic and phylogenetic analyses revealed substantial strain-level variation in Ac. anophagefferens, with a pangenome comprised of 81.1% core and 18.9% accessory orthogroups (23,356 orthogroups). Although variation in protein-coding genes within Aureococcus strains did not appear to be largely driven by recent prokaryotic or viral LGTs (~2.6% of accessory orthogroups), >1,000 recent prokaryotic/viral LGTs were identified within the Pelagophyceae, constituting 3.5-4.0% of each species’ orthogroups. Some of these LGTs are part of the accessory genome in Ac. anophagefferens or are species-specific and likely contribute to the ecological success of these algae globally and in blooms. This study is among the first to investigate pangenomes within algae and provides a robust framework for understanding bloom dynamics in pelagophytes, and, more generally, other HAB-causing algae. Collectively, my data offers insight into the fine-scale variation of Ac. anophagefferens organelle and nuclear genomes relative to those of their closest non-HAB-forming species. On a fundamental level, this investigation into pelagophyte genomes and specific gene fusions within algae illustrates the dynamic nature of algal genome evolution both between and within species, shaping our understanding of the patterns and processes that underly their genome evolution as a whole.