Molecular diversity and evolution of far-red light-acclimated photosystem I

Abstract

The need to acclimate to different environmental conditions is central to the evolution of cyanobacteria. Far-red light (FRL) photoacclimation, or FaRLiP, is an acclimation mechanism that enables certain cyanobacteria to use FRL to drive photosynthesis. During this process, a well-defined gene cluster is upregulated, resulting in changes to the photosystems that allow them to absorb FRL to perform photochemistry. Because FaRLiP is widespread, and because it exemplifies cyanobacterial adaptation mechanisms in nature, it is of interest to understand its molecular evolution. Here, we performed a phylogenetic analysis of the photosystem I subunits encoded in the FaRLiP gene cluster and analyzed the available structural data to predict ancestral characteristics of FRL-absorbing photosystem I. The analysis suggests that FRL-specific photosystem I subunits arose relatively late during the evolution of cyanobacteria when compared with some of the FRL-specific subunits of photosystem II, and that the order Nodosilineales, which include strains like Halomicronema hongdechloris and Synechococcus sp. PCC 7335, could have obtained FaRLiP via horizontal gene transfer. We show that the ancestral form of FRL-absorbing photosystem I contained three chlorophyll f-binding sites in the PsaB2 subunit, and a rotated chlorophyll a molecule in the A0B site of the electron transfer chain. Along with our previous study of photosystem II expressed during FaRLiP, these studies describe the molecular evolution of the photosystem complexes encoded by the FaRLiP gene cluster.

The ancient evolution of far-red light photoacclimation in cyanobacteria

“…Occasionally these could be used directly (such as the QD site in ChlF) 36 , but sometimes these residues proved impractical as queries due to lack of conservation in neighboring amino acids (e.g. the FaRLiP-specific PsaA2 loop) 38 . In this study, the analysis was done by studying amino acid alignments for areas that were conserved in FaRLiP paralogues, but distinct from white-light versions (Figure 2).…”

“…HGT) or by technical artefacts (e.g. different evolutionary rates, limited data) 37,38 . The present study lends strong support for the latter.…”

“…It has been previously suggested that these mismatches indicate different phylogenetic histories, with PSI genes evolving later and then being transferred by HGT to early branches of the FaRLiP cyanobacterial tree 38 . This hypothesis discounts the influence of divergent evolutionary rates on phylogenetic reconstruction.…”

“…The basis of this adaptation is a cluster of around 20 genes, encoding not only the enzyme synthesizing chlorophyll f (chlF), but also alternative components of Photosystem I (psa), oxygen-evolving Photosystem II (psb), phycobilisomes (apc), and a phytochrome signaling cascade (rfp) 22,[33][34][35][36][37][38][39] . Across the cyanobacterial species tree, FaRLiP is rare, occurring in a small subset of morphologically and phylogenetically diverse cyanobacteria, including early-branching filamentous lineages.…”

“…Early horizontal gene transfer between distantly related cyanobacteria remained a possibility. Trees of different FaRLiP genes were not fully congruent 37,38 , and considerable variation existed in gene arrangement 24,43 , raising the possibility of extensive single-gene HGT. In particular, the HGT of Photosystem I subunits to early FaRLiP lineages has been proposed 38 .…”