Acaryochloris marina is a unique cyanobacterium that is able to produce chlorophyll d as its primary photosynthetic pigment and thus efficiently use far-red light for photosynthesis. Acaryochloris species have been isolated from marine environments in association with other oxygenic phototrophs, which may have driven the niche-filling introduction of chlorophyll d . To investigate these unique adaptations, we have sequenced the complete genome of A. marina . The DNA content of A. marina is composed of 8.3 million base pairs, which is among the largest bacterial genomes sequenced thus far. This large array of genomic data is distributed into nine single-copy plasmids that code for >25% of the putative ORFs. Heavy duplication of genes related to DNA repair and recombination (primarily recA ) and transposable elements could account for genetic mobility and genome expansion. We discuss points of interest for the biosynthesis of the unusual pigments chlorophyll d and α-carotene and genes responsible for previously studied phycobilin aggregates. Our analysis also reveals that A. marina carries a unique complement of genes for these phycobiliproteins in relation to those coding for antenna proteins related to those in Prochlorococcus species. The global replacement of major photosynthetic pigments appears to have incurred only minimal specializations in reaction center proteins to accommodate these alternate pigments. These features clearly show that the genus Acaryochloris is a fitting candidate for understanding genome expansion, gene acquisition, ecological adaptation, and photosystem modification in the cyanobacteria.

Chlorophylls (Chl) play pivotal roles in energy capture, transfer and charge separation in photosynthesis. Among Chls functioning in oxygenic photosynthesis, Chl f is the most red-shifted type first found in a cyanobacterium Halomicronema hongdechloris. The location and function of Chl f in photosystems are not clear. Here we analyzed the high-resolution structures of photosystem I (PSI) core from H. hongdechloris grown under white or far-red light by cryo-electron microscopy. The structure showed that, far-red PSI binds 83 Chl a and 7 Chl f, and Chl f are associated at the periphery of PSI but not in the electron transfer chain. The appearance of Chl f is well correlated with the expression of PSI genes induced under far-red light. These results indicate that Chl f functions to harvest the far-red light and enhance uphill energy transfer, and changes in the gene sequences are essential for the binding of Chl f.

The composition of photosystem II (PSII) in the chlorophyll (Chl) d -dominated cyanobacterium Acaryochloris marina MBIC 11017 was investigated to enhance the general understanding of the energetics of the PSII reaction center. We first purified photochemically active complexes consisting of a 47-kDa Chl protein (CP47), CP43′ (PcbC), D1, D2, cytochrome b ₅₅₉ , PsbI, and a small polypeptide. The pigment composition per two pheophytin (Phe) a molecules was 55 ± 7 Chl d , 3.0 ± 0.4 Chl a , 17 ± 3 α-carotene, and 1.4 ± 0.2 plastoquinone-9. The special pair was detected by a reversible absorption change at 713 nm (P713) together with a cation radical band at 842 nm. FTIR difference spectra of the specific bands of a 3-formyl group allowed assignment of the special pair. The combined results indicate that the special pair comprises a Chl d homodimer. The primary electron acceptor was shown by photoaccumulation to be Phe a , and its potential was shifted to a higher value than that in the Chl a /Phe a system. The overall energetics of PSII in the Chl d system are adjusted to changes in the redox potentials, with P713 as the special pair using a lower light energy at 713 nm. Taking into account the reported downward shift in the potential of the special pair of photosystem I (P740) in A. marina , our findings lend support to the idea that changes in photosynthetic pigments combine with a modification of the redox potentials of electron transfer components to give rise to an energetic adjustment of the total reaction system.

In a previous study, we measured the redox potential of the primary electron acceptor pheophytin (Phe) a of photosystem (PS) II in the chlorophyll d –dominated cyanobacterium Acaryochloris marina and a chlorophyll a –containing cyanobacterium, Synechocystis . We obtained the midpoint redox potential ( E _m ) values of −478 mV for A. marina and −536 mV for Synechocystis . In this study, we measured the redox potentials of the primary electron acceptor quinone molecule (Q _A ), i.e., E _m (Q _A /Q _A ⁻ ), of PS II and the energy difference between [P680·Phe a ⁻ ·Q _A ] and [P680·Phe a ·Q _A ⁻ ], i.e., Δ G _PhQ . The E _m (Q _A /Q _A ⁻ ) of A. marina was determined to be +64 mV without the Mn cluster and was estimated to be −66 to −86 mV with a Mn-depletion shift (130–150 mV), as observed with other organisms. The E _m (Phe a /Phe a ⁻ ) in Synechocystis was measured to be −525 mV with the Mn cluster, which is consistent with our previous report. The Mn-depleted downshift of the potential was measured to be approximately −77 mV in Synechocystis , and this value was applied to A. marina (−478 mV); the E _m (Phe a /Phe a ⁻ ) was estimated to be approximately −401 mV. These values gave rise to a Δ G _PhQ of −325 mV for A. marina and −383 mV for Synechocystis . In the two cyanobacteria, the energetics in PS II were conserved, even though the potentials of Q _A ⁻ and Phe a ⁻ were relatively shifted depending on the special pair, indicating a common strategy for electron transfer in oxygenic photosynthetic organisms.