Cyanobacteria were the first organisms to perform oxygenic photosynthesis. This led to a dramatic increase in oxygen concentration in Earth’s atmosphere at around 2.5 billion years ago and allowed the development of all life we know today. Cyanobacteria are considered to be the ancestors of chloroplasts found in plants and algae. Until recently it has been believed that oxygenic photosynthesis is limited to the visible region of the solar spectrum with chlorophyll a and b as the main photopigments. The discovery of long wavelength chlorophyll forms has challenged this belief.
Here, we investigate the formation of long-wavelength pigments in the unicellular cyanobacterium Croococcidiopsis thermalis. The organism shows remarkable metabolic flexibility to adapt to various ecological niches, such as hot springs and extremely dry and cold deserts. Due to its high tolerance to desiccation and UV radiation it has been studied extensively by astrobiologists in respect to the colonisation of Mars. Exposure of C. thermalis to far-red light (750 nm) induces dramatic changes. During the initial adaptation phase the organism synthesises chlorophyll d and f in addition to chlorophyll a. This allows survival and growth of the cells under this condition. The effect on the remodelling of photosystem (PS) I, PS II and the phycobilisome complexes was investigated by various spectroscopic and microscopic techniques. Our results show the presence of (i) a highly efficient photosynthetic system with chlorophyll f in both photosystems, PSI and PSII, (ii) densely packed thylakoid membranes with phycobilisome complexes strongly reduced in quantity and size, (iii) highly oligomerised photosynthetic complexes of PSI tetramers, and (iv) an altered localisation of photosynthetic pigments. These changes have an important impact on the bioenergetics is discussed of the oxygenic photosystems.