Quinol C-methyltransferases from extant species of early cyanobacterial lineages shed light on the emergence of plastoquinone in oxygenic phototrophs.

Cyanobacteria and plastids harbor two prenylated quinones that serve as vital photosynthetic cofactors. One is a naphthoquinone (phylloquinone or menaquinone depending on the species), the naphthalene ring of which is always methylated in ortho of the prenyl chain. The other one is a benzoquinone, called plastoquinone-9, the benzenoid ring of which is, in contrast, never methylated at this position. In oxygenic phototrophs, such an arrangement is thought to have driven the evolution and retention of unique quinol C-methyltransferases that act exclusively on naphthoquinol substrates. Here, we identified quinol C-methyltransferases in two extant taxa of early cyanobacterial lineages, Gloeobacter violaceus and Synechococcus sp. JA-2-3B'a, that did not discriminate between naphthoquinol and benzoquinol substrates when these enzymes were expressed in Escherichia coli. Quinone analysis showed, however, that G. violaceus extracts did not contain any detectable amounts of methyl-plastoquinone-9. Furthermore, functional complementation assays in the cyanobacterium Synechocystis sp. PCC 6803 revealed that G. violaceus and S. sp. JA-2-3B'a quinol C-methyltransferases displayed either strict or marked substrate preference for demethyl-phylloquinol. Taken together, these data suggest that G. violaceus and S. sp. JA-2-3B'a quinol C-methyltransferases are the remnants of a promiscuous enzyme present during the emergence of plastoquinone as a photosynthetic electron carrier.