New types of ATP ‐grasp ligase are associated with the novel pathway for complicated mycosporine‐like amino acid production in desiccation‐tolerant cyanobacteria

Abstract

Summary Mycosporine‐like amino acids (MAAs) were widespread in diverse organisms to attenuate UV radiation. We recently characterized the large, complicated MAA mycosporine‐2‐(4‐deoxygadusolyl‐ornithine) in desert cyanobacterium Nostoc flagelliforme . Synthesis of this MAA requires the five‐gene cluster mysABDC2C3 . Here, bioinformatic analysis indicated that mysC duplication within five‐gene mys clusters is strictly limited to drought‐tolerant cyanobacteria. Phylogenic analysis distinguished these duplicated MysCs into two clades that separated from canonical MysCs. Heterologous expression of N. flagelliforme mys genes in Escherichia coli showed that MysAB produces 4‐deoxygadusol. The ATP‐grasp ligase of MysC3 catalyses the linkage of the δ‐ or ε‐amino group of ornithine/lysine to 4‐deoxygadusol, yielding mycosporine‐ornithine or mycosporine‐lysine respectively. The ATP‐grasp ligase of MysC2 strictly condenses the α‐amino group of mycosporine‐ornithine to another 4‐deoxygadusol. MysD (D‐Ala–D‐Ala ligase) functions following MysC2 to catalyse the formation of mycosporine‐2‐(4‐deoxygadusolyl‐ornithine). High arginine content likely provides a greater pool of ornithine over other amino acids during rehydration of desiccated N. flagelliforme . Duplication of ATP‐grasp ligases is specific for the use of substrates that have two amino groups (such as ornithine) for the production of complicated MAAs with multiple chromophores. This five‐enzyme biosynthesis pathway for complicated MAAs is a novel adaptation of cyanobacteria for UV tolerance in drought environments.

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