Discovery of domoic acid biosynthesis genes in Chaetoceros costatus expands the phylogenetic range of toxigenic diatoms.

Abstract

Domoic acid (DA) is the neurotoxin responsible for amnesic shellfish poisoning (ASP) long thought to be confined to only two phylogenetically related diatom genera Pseudo-nitzschia and Nitzschia in one class Bacillariophyceae, leaving the occurrence and evolutionary origin of this trait in other diatom classes unresolved. Here we revealed homologs of DA biosynthesis (dab) genes across diverse diatom lineages through large-scale mining of Tara Oceans metatranscriptomes, suggesting that other diatom lineages may harbor sequences with similarity to DA‑biosynthetic dab genes. We identified dab genes in Chaetoceros costatus (class Mediophyceae) through genome-based screening of 281 diatom strains representing 54 diatom species from Chinese waters. The C. costatus genome encodes three of the four canonical dab genes (dabA, dabC, and dabD) but lacks dabB, which is similarly absent in the DA-producing red alga Chondria armata. Analytical validation using LC-MS/MS confirmed DA production in the C. costatus strains. Chromosome-level genome assemblies revealed haplotype-specific expansions of dabA and dabD, suggesting possible key functions in diversifying DA biosynthetic capacity. The observed phylogenetic patterns are consistent with the hypothesis of multiple horizontal gene transfer events, including a putative cross-eukaryote gene acquisition between Pseudo-nitzschia and C. costatus. These findings substantially expand the known taxonomic range of DA-producing diatoms and highlight the hidden toxin potential of ecologically dominant marine diatoms.

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