Metagenomics reveal the potential for geosmin and 2-methylisoborneol production across multiple bacterial phyla in recirculating aquaculture systems

Geosmin and 2-methylisoborneol (MIB) are known to cause taste-and-odour problems in recirculating aquaculture systems (RAS). Both geosmin and MIB are microbial metabolites belonging to terpenoids. Precursors for terpenoids are biosynthesized via the methylerythritol phosphate (MEP) and the mevalonate (MVA) pathways. We carried out a metagenomic analysis of 50 samples from five RAS to investigate terpenoid biosynthesis and metabolic potential for geosmin and MIB production in RAS microbiomes. A total of 1008 metagenome-assembled genomes (MAGs) representing 26 bacterial and three archaeal phyla were recovered. Although most archaea are thought to use the MVA pathway for terpenoid precursor biosynthesis, an Iainarchaeota archaeal MAG is shown to harbour a complete set of genes encoding the MEP pathway but lacking genes associated with the MVA pathway. In this study, a total of 16 MAGs affiliated with five bacterial phyla (Acidobacteriota, Actinobacteriota, Bacteroidota, Chloroflexota, and Myxococcota) were identified as possessing potential geosmin or MIB synthases. These putative taste and odour producers were diverse, many were taxonomically unidentified at the genus or species level, and their relative abundance differed between the investigated RAS farms. The metagenomic study of the RAS microbiomes revealed a previously unknown phylogenetic diversity of the potential to produce geosmin and MIB.