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 ␣-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.comparative microbial genomics ͉ photosynthesis ͉ oxygenic phototrophs ͉ evolution

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 redshifted 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 farred 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.

No abstract

A Fourier transform infrared (FTIR) difference spectrum of the primary electron donor (P680) of photosystem II upon its photooxidation (P680+/P680) was obtained in the frequency region of 1000-3000 cm-1. The reaction center (RC) complex (D1-D2-Cytb559) was used for the measurements in the presence of ferricyanide as an exogenous electron acceptor. Control measurements of electronic absorption (300-1200 nm) showed that illumination of the RC complex at 150 K induced major oxidation of P680 concomitant with oxidation of a carotenoid and an accessory chlorophyll (Chl). Illumination at 250 K also specifically bleached one of the two beta-carotene molecules bound to the RC complex, and the sample thus treated exhibited little formation of a carotenoid cation on subsequent illumination at 150 K. The P680+/P680 FTIR difference spectrum (with minor contamination of Chl+/Chl) was measured at 150 K using this partially carotenoid-deficient RC complex. The spectrum showed a broad positive band centered at approximately 1940 cm-1, which could be ascribed to an infrared electronic transition of P680+ analogous to that previously observed in various bacterial P+. This finding indicates that a positive charge is delocalized over (or hopping between) the two Chl molecules in P680+. The low intensity of this electronic band compared with that of the bacterial band could have three possible explanations: weak resonance interaction between the constituent Chl molecules, an asymmetric structure of P680+, and the difference in Chl species. Bands in the C=O stretching region (1600-1750 cm-1) were interpreted in comparison with resonance Raman spectra of the RC complex. The negative peaks at 1704 and 1679 cm-1 were proposed as candidates for the keto C9=O bands of P680. The observation that neither of these bands agreed with the main keto C9=O band at 1669 cm-1 in the previous 3P680/P680 FTIR spectrum [Noguchi et al. (1993) Biochemistry 32, 7186-7195] led to the idea that the triplet state migrates to a Chl (designated as ChlT) different from P680 at low temperatures. Based on these results, structural models of Chl molecules including P680 and ChlT and their coupling in the cation, triplet, and Qy singlet states are discussed.

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 ␣-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. Acaryochloris marina ͉ FTIR ͉ reaction center ͉ photosynthesis ͉ electron transfer C hlorophyll (Chl) a has a ubiquitous role as an electron donor in the photochemical reactions of oxygenic photosynthesis, in which two kinds of photosystem, namely photosystem I (PSI) and photosystem II (PSII), cooperatively drive photosynthetic electron flow from water to NADP ϩ . The reduced cofactor, NADPH, is then used for CO 2 fixation. Chl a is a key pigment that serves as an electron donor called the special pair in PSI and PSII. Acaryochloris spp. are unique cyanobacteria that differ from the majority of photosynthetic organisms by having Chl d (3-desvinyl-3-formyl Chl a) (1-4) as the major pigment (Ͼ95%); Chl a is a minor component but is never absent (5, 6). In photosynthetic organisms, changes in pigment composition affect both the function of pigments and their reaction environments, including the modified proteins that accommodate them. Photosynthetic pigments function in two roles: as lightharvesting components and as electron transfer components. Light harvesting is mainly governed by the orientation and energy levels of pigments, and, in this context, a particular excitation energy level is not an absolute precondition for function, but a relative one. On the other hand, electron transfer reactions are governed by an absolute redox potential, because the photosynthetic oxidation of water requires a very high potential, whereas reduction of NADP ϩ requires a very low potential. For this reason, it is of particul...