Chlorophylls are essential for light-harvesting and energy transduction in photosynthesis. Four chemically distinct varieties have been known for the past 60 years. Here we report isolation of a fifth, which we designate chlorophyll f. Its in vitro absorption (706 nanometers) and fluorescence (722 nanometers) maxima are red-shifted compared to all other chlorophylls from oxygenic phototrophs. On the basis of the optical, mass, and nuclear magnetic resonance spectra, we propose that chlorophyll f is [2-formyl]-chlorophyll a (C55H70O6N4Mg). This finding suggests that oxygenic photosynthesis can be extended further into the infrared region and may open associated bioenergy applications.

Chlorophyll d is a photosynthetic pigment that, based on chemical analyses, has only recently been recognized to be widespread in oceanic and lacustrine environments. However, the diversity of organisms harbouring this pigment is not known. Until now, the unicellular cyanobacterium Acaryochloris marina is the only characterized organism that uses chlorophyll d as a major photopigment. In this study we describe a new cyanobacterium possessing a high amount of chlorophyll d, which was isolated from waters around Heron Island, Great Barrier Reef (231 26 0 31.2 00 S, 1511 54 0 50.4 00 E). The 16S ribosomal RNA is 2% divergent from the two previously described isolates of A. marina, which were isolated from waters around the Palau islands (Pacific Ocean) and the Salton Sea lake (California), suggesting that it belongs to a different clade within the genus Acaryochloris. An overview sequence analysis of its genome based on Illumina technology yielded 871 contigs with an accumulated length of 8 371 965 nt. Their analysis revealed typical features associated with Acaryochloris, such as an extended gene family for chlorophyll-binding proteins. However, compared with A. marina MBIC11017, distinct genetic, morphological and physiological differences were observed. Light saturation is reached at lower light intensities, Chl d/a ratios are less variable with light intensity and the phycobiliprotein phycocyanin is lacking, suggesting that cyanobacteria of the genus Acaryochloris occur in distinct ecotypes. These data characterize Acaryochloris as a niche-adapted cyanobacterium and show that more rigorous attempts are worthwhile to isolate, cultivate and analyse chlorophyll d-containing cyanobacteria for understanding the ecophysiology of these organisms.

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Chromatic photoacclimation and photosynthesis were examined in two strains of Acaryochloris marina (MBIC11017 and CCMEE5410) and in Synechococcus PCC7942. Acaryochloris contains Chl d, which has an absorption peak at ca 710 nm in vivo. Cultures were grown in one of the three wavelengths (525 nm, 625 nm and 720 nm) of light from narrow-band photodiodes to determine the effects on pigment composition, growth rate and photosynthesis: no growth occurred in 525 nm light. Synechococcus did not grow in 720 nm light because Chl a does not absorb effectively at this long wavelength. Acaryochloris did grow in 720 nm light, although strain MBIC11017 showed a decrease in phycobilins over time. Both Synechococcus and Acaryochloris MBIC11017 showed a dramatic increase in phycobilin content when grown in 625 nm light. Acaryochloris CCMEE5410, which lacks phycobilins, would not grow satisfactorily under 625 nm light. The cells adjusted their pigment composition in response to the light spectral conditions under which they were grown. Photoacclimation and the Q (y) peak of Chl d could be understood in terms of the ecological niche of Acaryochloris, i.e. habitats enriched in near infrared radiation.

Chlorophyll (Chl) f is the most recently discovered chlorophyll and has only been found in cyanobacteria from wet environments. Although its structure and biophysical properties are resolved, the importance of Chl f as an accessory pigment in photosynthesis remains unresolved. We found Chl f in a cyanobacterium enriched from a cavernous environment and report the first example of Chl f-supported oxygenic photosynthesis in cyanobacteria from such habitats. Pigment extraction, hyperspectral microscopy and transmission electron microscopy demonstrated the presence of Chl a and f in unicellular cyanobacteria found in enrichment cultures. Amplicon sequencing indicated that all oxygenic phototrophs were related to KC1, a Chl f-containing cyanobacterium previously isolated from an aquatic environment. Microsensor measurements on aggregates demonstrated oxygenic photosynthesis at 742 nm and less efficient photosynthesis under 768-and 777-nm light probably because of diminished overlap with the absorption spectrum of Chl f and other far-red absorbing pigments. Our findings suggest the importance of Chl f-containing cyanobacteria in terrestrial habitats.