The haplotype-resolved Prymnesium parvum (type B) microalga genome reveals the genetic basis of its fish-killing toxins

Abstract

The catastrophic loss of aquatic life in the Central European Oder River in 2022, caused by a toxic bloom of the haptophyte microalga Prymnesium parvum (in a wide sense, s.l.), underscores the need to improve our understanding of the genomic basis of the toxin. Previous morphological, phylogenetic, and genomic studies have revealed cryptic diversity within P. parvum s.l. and uncovered three clade-specific (types A, B, C) prymnesin toxins. Here, we used state-of-the-art long-read sequencing and assembled the first haplotype-resolved diploid genome of a P. parvum type B, the strain responsible for the Oder disaster. Comparative analyses with type A genomes uncovered a genome-size expansion driven by repetitive elements in type B. We also found conserved chromosomal synteny but divergent evolution in several polyketide synthase (PKS) genes, which are known to underlie toxin production in combination with environmental cues. We identified a specific, approximately 20 kilobase pair comprising deletion in the largest PKS gene of type B that we link to differences of the chemical structure of types A and B prymnesins. Electron-microscopy and flow cytometry confirmed diploidy in the Oder River strain and differences to closely related strains in morphology and ploidy. Our results provide unprecedented resolution of strain diversity in P. parvum and a better understanding of the genomic basis of toxin variability in haptophytes. The reference-quality genome will help to understand changes to microbial diversity in the face of increasing environmental pressures, and provides a basis for strain-level monitoring of invasive Prymnesium in the future.