Global distribution and ancient evolution of far-red photosynthesis

Abstract

Cyanobacteria are photosynthetic prokaryotes which have forever changed our planet. In the billions of years of their existence, they have evolved many adaptations to various light conditions. In the last decade, an adaptation was discovered which enables a small range of phylogenetically and morphologically diverse cyanobacteria to photosynthesize into the near-infrared / far-red. It is hypothesized that this complex Far-Red Photoacclimation system (FaRLiP) using a red-shifted chlorophyll (chlorophyll f) provides an evolutionary advantage when in the shade of other photosynthetic organisms. Although remarkable discoveries have been made about the structure and function of this system, its evolutionary history has remained elusive. Also unclear is how widespread FaRLiP is in nature. Both these aspects could clarify the phenotype’s limitations and its potential usefulness for biotechnology applications. My project has combined molecular biology techniques with bioinformatics in order to explore these questions. Microscopy and spectroscopic techniques were also employed to analyze pigments. Resources used included dozens of strains maintained in six culture collections, as well as multiple online public repositories of sequence data. Terabases of data were searched, and gigabases of relevant data were handled, in order to build up-to-date phylogenetic histories not only of far-red-associated genes, but also of a relevant genus, Chroococcidiopsis. The results contradict the initial statement that horizontal gene transfer is mainly responsible for the phenotype’s distribution in distantly related cyanobacteria, but rather strongly support a combination of vertical descent and loss. Far-Red Photoacclimation is an ancient adaptation. Their earliest last common ancestor can be placed in the early Paleoproterozoic, at the start of the age of stromatolites, and may be suspected to have co-evolved with other evolutionary innovations such as thick biofilms. Simpler red-shifted systems, such as the closely-related Low-Light Photoacclimation, may have existed even earlier. At present, FaRLiP appears to be common in microbialites, but is also present in a wide variety of previously-unknown locations such as Antarctic lakes and hyperarid deserts.