Structure of a photosystem I-ferredoxin complex from a marine cyanobacterium provides insights into far-red light photoacclimation

Gisriel, Christopher J.; Flesher, David A.; Shen, Gaozhong; Wang, Jimin; Ho, Ming-Chih; Brudvig, Gary W.; Bryant, Donald A.

doi:10.1016/j.jbc.2021.101408

Cited by 24 publications

(35 citation statements)

References 74 publications

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“…Additionally, the Chl in site 611 is related by pseudo- C 2 symmetry to the Chl f found in FRL-PsbC. Such symmetry in antenna Chl f sites was also observed in FRL-acclimated photosystem I structures [ 50 ], further supporting Chl site 611 binding Chl f in organisms where FRL-PsbB contains Thr at position 244. Thus, we propose that the Chl 611 site in most FRL-PSII complexes binds Chl f , and that this was a characteristic of the ancestral FRL-PSII complex.…”

Section: Resultsmentioning

confidence: 64%

Molecular Evolution of Far-Red Light-Acclimated Photosystem II

et al. 2022

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Cyanobacteria are major contributors to global carbon fixation and primarily use visible light (400−700 nm) to drive oxygenic photosynthesis. When shifted into environments where visible light is attenuated, a small, but highly diverse and widespread number of cyanobacteria can express modified pigments and paralogous versions of photosystem subunits and phycobiliproteins that confer far-red light (FRL) absorbance (700−800 nm), a process termed far-red light photoacclimation, or FaRLiP. During FaRLiP, alternate photosystem II (PSII) subunits enable the complex to bind chlorophylls d and f, which absorb at lower energy than chlorophyll a but still support water oxidation. How the FaRLiP response arose remains poorly studied. Here, we report ancestral sequence reconstruction and structure-based molecular evolutionary studies of the FRL-specific subunits of FRL-PSII. We show that the duplications leading to the origin of two PsbA (D1) paralogs required to make chlorophyll f and to bind chlorophyll d in water-splitting FRL-PSII are likely the first to have occurred prior to the diversification of extant cyanobacteria. These duplications were followed by those leading to alternative PsbC (CP43) and PsbD (D2) subunits, occurring early during the diversification of cyanobacteria, and culminating with those leading to PsbB (CP47) and PsbH paralogs coincident with the radiation of the major groups. We show that the origin of FRL-PSII required the accumulation of a relatively small number of amino acid changes and that the ancestral FRL-PSII likely contained a chlorophyll d molecule in the electron transfer chain, two chlorophyll f molecules in the antenna subunits at equivalent positions, and three chlorophyll a molecules whose site energies were altered. The results suggest a minimal model for engineering far-red light absorbance into plant PSII for biotechnological applications.

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Section: Resultsmentioning

confidence: 64%

Molecular Evolution of Far-Red Light-Acclimated Photosystem II

et al. 2022

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“…We calculated a ratio of Chl f: Chl a of 1:17.6 for the Chroococcidiopsis G-MTQ-3P2 isolate, which was slightly higher than the value reported for Chlorogloeopsis. fritschii [45] and in line with the reported number of Chl f in FRL-acclimated PSII [40][41][42][43]. While the assembly and function of PSII in FRL require Chl d, the enzyme(s) performing the synthesis of Chl d remains unknown.…”

Section: Pigments From Frl-grown Chroococcidiopsis Contained Chl F An...mentioning

confidence: 59%

“…The BChl a found in FRL-pigments is indicative of the presence of another bacterium in the culture of the Chroococcidiopsis G-MTQ-3P2 isolate. The absence of other BChls in [39][40][41][42][43]. We used values from the absorbance spectra of Figure 3A to calculate the ratio of Chl f : Chl a in G-MTQ-3P2 cells grown in FRL.…”

Section: Pigments From Frl-grown Chroococcidiopsis Contained Chl F An...mentioning

confidence: 99%

Adaptation of Cyanobacteria to the Endolithic Light Spectrum in Hyper-Arid Deserts

et al. 2022

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In hyper-arid deserts, endolithic microbial communities survive in the pore spaces and cracks of rocks, an environment that enhances water retention and filters UV radiation. The rock colonization zone is enriched in far-red light (FRL) and depleted in visible light. This poses a challenge to cyanobacteria, which are the primary producers of endolithic communities. Many species of cyanobacteria are capable of Far-Red-Light Photoacclimation (FaRLiP), a process in which FRL induces the synthesis of specialized chlorophylls and remodeling of the photosynthetic apparatus, providing the ability to grow in FRL. While FaRLiP has been reported in cyanobacteria from various low-light environments, our understanding of light adaptations for endolithic cyanobacteria remains limited. Here, we demonstrated that endolithic Chroococcidiopsis isolates from deserts around the world synthesize chlorophyll f, an FRL-specialized chlorophyll when FRL is the sole light source. The metagenome-assembled genomes of these isolates encoded chlorophyll f synthase and all the genes required to implement the FaRLiP response. We also present evidence of FRL-induced changes to the major light-harvesting complexes of a Chroococcidiopsis isolate. These findings indicate that endolithic cyanobacteria from hyper-arid deserts use FRL photoacclimation as an adaptation to the unique light transmission spectrum of their rocky habitat.

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“…FRL-activated photosystems were reported to have 7 Chl f out of 90 Chls in PSI and 4 Chl f and 1 Chl d out of 35 Chls in PSII [39–43]. We used values from the absorbance spectra of Fig.…”

Section: Resultsmentioning

confidence: 99%

Adaptation of cyanobacteria to the endolithic light spectrum in hyper-arid deserts

Murray

Ertekin

Dailey

et al. 2022

Preprint

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In hyper-arid deserts, endolithic microbial communities survive in the pore spaces and cracks of rocks, an environment that enhances water retention and filters UV radiation. The rock coloniza-tion zone is enriched in far-red light (FRL) and depleted in visible light. This poses a challenge to cyanobacteria, which are the primary producers of endolithic communities. Many species of cya-nobacteria are capable of Far-Red Light Photoacclimation (FaRLiP), a process in which FRL in-duces the synthesis of specialized chlorophylls and remodeling of the photosynthetic apparatus, providing the ability to grow in FRL. While FaRLiP has been reported in cyanobacteria from various low-light environments, our understanding of light adaptations for endolithic cyanobac-teria remains limited. Here, we demonstrated that endolithic Chroococidiopsis isolates from de-serts around the world synthesize chlorophyll f, an FRL-specialized chlorophyll when FRL is the sole light source. The metagenome-assembled genomes of these isolates encoded chlorophyll f synthase and all the genes required to implement the FaRLiP response. We also present evidence of FRL-induced changes to the major light-harvesting complexes of a Chroococidiopsis isolate. These findings indicate that endolithic cyanobacteria from hyper-arid deserts use FRL pho-to-acclimation as an adaptation to the unique light transmission spectrum of their rocky habitat.

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Structure of a photosystem I-ferredoxin complex from a marine cyanobacterium provides insights into far-red light photoacclimation

Cited by 24 publications

References 74 publications

Molecular Evolution of Far-Red Light-Acclimated Photosystem II

Molecular Evolution of Far-Red Light-Acclimated Photosystem II

Adaptation of Cyanobacteria to the Endolithic Light Spectrum in Hyper-Arid Deserts

Adaptation of cyanobacteria to the endolithic light spectrum in hyper-arid deserts

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