Harmful algal bloom species Microcystis aeruginosa releases thiamin antivitamins to suppress competitors

Abstract In environmental ecosystems, vitamin concentrations are often exceedingly low (1, 2) and auxotrophy, or reliance on exogenous vitamin or vitamin precursors, is widespread (3–5). We show here that the widespread harmful algal bloom (HAB) speciesMicrocystis aeruginosa,threatening freshwater aquatic ecosystems globally, releases a complex mixture of thiamin antivitamins, including bacimethrin and methoxythiamin, which induce thiamin deficiency in the benign model green algaChlamydomonas reinhardtii. Putative biosynthetic genes for bacimethrin were upregulated inM. aeruginosawhen grown in co-culture resulting in greater production of bacimethrin. Bacimethrin, methoxythiamin, oxidized forms of thiamin and methoxythiamin, and a novel structural homolog of bacimethrin were all found at elevated levels in the co-culture exometabolome extracts and were all inhibitory to the growth ofC. reinhardtiiindividually at very low concentrations and as a mixture in culture medium extracts. The thiamin-requiring mutantC. reinhardtii, CC-25, was much more sensitive to bacimethrin and methoxythiamin than the wildtype. Thiamin addition largely rescued the inhibitory effects of exposure to antivitamins in both the wildtype and mutant strain. Finally, we determined that bacimethrin is present in aquatic environments and is elevated duringMicrocystisblooms. Thus, allelopathic suppression of competitors, particularly those that are auxotrophic for thiamin, byM. aeruginosavia the production of antivitamins in environments where thiamin availability is low, could help this species to become dominant and form blooms.