Evolution of far-red light photoacclimation in cyanobacteria

Summary Cyanobacteria oxygenated the atmosphere of early Earth and continue to be key players in global carbon and nitrogen cycles. A phylogenetically diverse subset of extant cyanobacteria can perform photosynthesis with far-red light through a process called far-red light photoacclimation, or FaRLiP. This phenotype is enabled by a cluster of ∼20 genes and involves the synthesis of red-shifted chlorophylls d and f, together with paralogs of the ubiquitous photosynthetic machinery used in visible light. The FaRLiP gene cluster is present in diverse, environmentally important cyanobacterial groups, but its origin, evolutionary history, and connection to early biotic environments have remained unclear. This study takes advantage of the recent increase in (meta)genomic data to help clarify this issue: sequence data mining, metagenomic assembly, and phylogenetic tree networks were used to recover more than 600 new FaRLiP gene sequences, corresponding to 51 new gene clusters. These data enable high-resolution phylogenetics and—by relying on multiple gene trees, together with gene arrangement conservation—support FaRLiP appearing early in cyanobacterial evolution. Sampling information shows that considerable FaRLiP diversity can be observed in microbialites to the present day, and we hypothesize that the process was associated with the formation of microbial mats and stromatolites in the early Paleoproterozoic. The ancestral FaRLiP cluster was reconstructed, revealing features that have been maintained for billions of years. Overall, far-red-light-driven oxygenic photosynthesis may have played a significant role in Earth’s early history.