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The evolutionary advantage of toxin production among cyanobacteria, the oldest known organisms on Earth

Cyanobacteria produce toxic secondary metabolites for reasons hitherto unclear. Using a phylogenetic approach that accounts for the high complexity of biosynthetic gene clusters (full or partial inversions, variable length, different number of genes, non-orthologues), we analyzed the sequences of 76 biosynthetic gene clusters covering 19 cyanotoxins. The phylogenetic tree of biosynthetic gene clusters branches first according to the bioactivity of the toxic metabolite (molecular target in another organism), then according to the chemical class and chemical structure of the secondary metabolite, and finally according to the organism and area of origin. The bioactivity of a toxic metabolite can be deduced directly from the nucleotide sequence of the biosynthetic gene cluster, without needing to examine the enzymes themselves or to measure expression levels. Bioactivity may have been the primary driving force behind the diversity of secondary metabolism in cyanobacteria. This genetic machinery evolved to facilitate three specific survival strategies acting separately or in tandem, with dominant cyanobacteria possessing the genetic machinery to support all three strategies. Transmembrane (direct) toxicity targeting ion channels, intracellular (indirect) toxicity targeting cell-cycle regulation, and digestion inhibition targeting proteases may have provided the survival advantage underpinning the evolutionary success of both cyanobacteria and their early symbiotic hosts.