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

Authors: DICKINSON, GABRIELLA - University Of Florida; STUTTS, LAUREN - University Of Florida; LATIMER, SCOTT - University Of Florida; SMITH, NATHAN - University Of Nebraska; BATYRSHINA, ZHANIYA - University Of Florida; KULA-MAXIMENKO, MONIKA - Polish Academy Of Sciences; SLESAK, IRENEUSZ - Polish Academy Of Sciences; Block, Anna; WILSON, MARK - University Of Nebraska; BASSET, GILLES - University Of Florida

Submitted to: Photosynthesis Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/3/2025
Publication Date: 11/13/2025
Citation: Dickinson, G., Stutts, L.R., Latimer, S., Smith, N., Batyrshina, Z., Kula-Maximenko, M., Slesak, I., Block, A.K., Wilson, M., Basset, G.J. 2025. Quinol C-methyltransferases from extant species of early cyanobacterial lineages shed light on the emergence of plastoquinone in oxygenic phototrophs. Photosynthesis Research. 163(6),59. https://doi.org/10.1007/s11120-025-01180-3.
DOI: https://doi.org/10.1007/s11120-025-01180-3

Interpretive Summary: Cyanobacteria are photosynthetic microorganisms that provide unique insights into how life evolved the ability to capture energy from sunlight. In developing their photosynthetic systems cyanobacteria needed to select compounds to carry electrons that worked in photosynthesis but did not interfere with respiration (the energy utilization process). Researchers at the University of Florida, in collaboration with ARS scientists from Gainesville, FL investigated the way many different species of cyanobacteria make these electron carriers and discovered that two different mechanisms were developed that provide the necessary functional specificity. These findings provide information on the constraints and evolution of photosynthesis and may be leveraged to identify mechanisms to help control cyanobacterial blooms that impact human and aquatic health.

Technical Abstract: Cyanobacteria and plastids harbor two prenylated quinones that serve as vital redox 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. Such an arrangement is thought to have driven, in oxygenic phototrophs, the evolution and retention of unique quinol C-methyltransferases that act exclusively on naphthoqinol substrates. Here, we identified in two extant taxa of early cyanobacterial lineages, Gloeobacter violaceus and Synechococcus sp. JA-2-3B'a, quinol C- methyltransferases 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 detectable amounts of methyl-plastoquinone-9. Furthermore, functional complementation assays in the cyanobacterium Synechocystis sp. PCC6803 revealed that G. violaceus and Synechococcus sp. JA-2-3B'a quinol C-methyltransferases are the remnants of a semi-promiscuous enzyme present during the emergence of plastoquinone as a photosynthetic electron carrier.