Far-red photosynthesis in early-branching cyanobacteria from a desert

Oxygenic photosynthesis has been considered to be restricted to visible light. However, some cyanobacteria can extend their photosynthetic range into far-red light (FRL) by undergoing a complex and extensive acclimation process known as far-red light photoacclimation (FaRLiP) which leads to the formation of the red-shifted chlorophylls (chl) d and f, as well as modified photosystems and phycobilisomes. In shaded areas, FRL is usually enriched, and it has been shown that for some habitats such as stromatolites, beach rock, or caves, FaRLiP cyanobacteria are commonly found within them. Nevertheless, our understanding of the impact of FRL photosynthesis on a global scale is largely unknown. Here, we focus on Sabkha Oum Dba (Morocco), an arid habitat characterized by photosynthetic soil crusts. We prove that it contains large quantities of chl f, suggesting that FRL might be a key driver of photosynthesis and the carbon cycle in this environment.

By isolating several new FaRLiP cyanobacteria from this habitat, we were able to characterize their photophysiology and define their position in the phylogenetic tree. Two characteristic spectral features were observed for all FRL-grown isolates: (i) the fluorescence emission spectra were shifted to 730-750 nm and (ii) the reflection spectra showed an additional peak at 708 nm. High-performance liquid chromatography (HPLC) experiments confirmed that all FRL samples contain chl d and f. In certain cells of this order, a distinctive segregated distribution of chl a and chl d/f has been observed. All cyanobacteria consist of thin filaments with diameters of 0.9-1.4 μm. The 16S-23S ribosomal RNA (rRNA) phylogenetic tree revealed that the majority of the isolates with the capability to perform FaRLiP belong to phylogenetically early-branching cyanobacteria Nodosilineales (also known as Phormidesmiales), a largely understudied order. Our isolates are closely related to Halomicronema hongdechloris C2206, which is the first chl f-containing FaRLiP strain.