Chlorophyll f synthesis by a super-rogue photosystem II complex

Trinugroho, Joko Pebrianto; Bečková, Martina; Shao, Shengxi; Yu, Jianfeng; Zhao, Ziyu; Murray, James W.; Sobotka, Roman; Komenda, Josef; Nixon, Peter J.

doi:10.1038/s41477-020-0616-4

Cited by 35 publications

(51 citation statements)

References 44 publications

(37 reference statements)

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“…What is more, these structural and functional features, together with the ASR analysis (Supplementary Fig. S8 and S9) suggest that the atypical forms of D1, lacking ligands to the Mn 4 CaO 5 cluster, such as the chlorophyll f synthase [ 33 , 75 ], or the “rogue” or “sentinel” D1 [ 32 , 76 ], diverged from forms of D1 that were able to support water oxidation, but that could antedate the MRCA of Cyanobacteria [ 2 ].…”

Section: Discussionmentioning

confidence: 99%

Time-resolved comparative molecular evolution of oxygenic photosynthesis

Oliver

Sánchez‐Baracaldo

Larkum

et al. 2021

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Oxygenic photosynthesis starts with the oxidation of water to O 2 , a light-driven reaction catalysed by photosystem II. Cyanobacteria are the only prokaryotes capable of water oxidation and therefore, it is assumed that the origin of oxygenic photosynthesis is a late innovation relative to the origin of life and bioenergetics. However, when exactly water oxidation originated remains an unanswered question. Here we use phylogenetic analysis to study a gene duplication event that is unique to photosystem II: the duplication that led to the evolution of the core antenna subunits CP43 and CP47. We compare the changes in the rates of evolution of this duplication with those of some of the oldest well-described events in the history of life: namely, the duplication leading to the Alpha and Beta subunits of the catalytic head of ATP synthase, and the divergence of archaeal and bacterial RNA polymerases and ribosomes. We also compare it with more recent events such as the duplication of Cyanobacteria-specific FtsH metalloprotease subunits and the radiation leading to Margulisbacteria, Sericytochromatia, Vampirovibrionia, and other clades containing anoxygenic phototrophs. We demonstrate that the ancestral core duplication of photosystem II exhibits patterns in the rates of protein evolution through geological time that are nearly identical to those of the ATP synthase, RNA polymerase, or the ribosome. Furthermore, we use ancestral sequence reconstruction in combination with comparative structural biology of photosystem subunits, to provide additional evidence supporting the premise that water oxidation had originated before the ancestral core duplications. Our work suggests that photosynthetic water oxidation originated closer to the origin of life and bioenergetics than can be documented based on phylogenetic or phylogenomic species trees alone.

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Section: Discussionmentioning

confidence: 99%

Time-resolved comparative molecular evolution of oxygenic photosynthesis

Oliver

Sánchez‐Baracaldo

Larkum

et al. 2021

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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“…It would be difficult to reconcile these unique structural and genetic features with a scenario in which PSII evolved water oxidation at a late stage, or starting as a purple anoxygenic type II RC, once the heterodimerization process was well underway or completed, or in the absence of core antenna domains, given that these interact directly with the electron donor side of PSII, in a manner strikingly similar to that of the homodimeric type I RC of the Firmicutes [19]. What is more, these structural and functional features also suggest that the atypical forms of D1, lacking ligands to the Mn4CaO5 cluster, such as the so-called chlorophyll f synthase [32, 71], or the so-called “rogue” or “sentinel” D1 [31, 72], diverged from forms of D1 that were able to support water oxidation. Even if they originated from early duplications that could have antedated the MRCA of Cyanobacteria [2] and as additionally supported by ASR analysis (Supplementary Figure S9 and S10).…”

Section: Discussionmentioning

confidence: 99%

Time-resolved comparative molecular evolution of oxygenic photosynthesis

Oliver

Sánchez‐Baracaldo²,

Larkum

et al. 2020

Preprint

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13Oxygenic photosynthesis starts with the oxidation of water to O 2. Cyanobacteria are the only 14 known prokaryotes capable of oxygenic photosynthesis and therefore, it is assumed that 15 water oxidation is a late innovation relative to the origin of life. However, when exactly 16 oxygenic photosynthesis originated remains lively debated. Here we show that the origin of 17 photosystem II, the water-splitting enzyme, occurred at an early stage during the evolution of 18 life and long before the origin of Cyanobacteria. We use relaxed molecular clocks, ancestral 19 sequence reconstruction, and comparative structural biology to demonstrate that photosystem 20 II exhibits patterns of evolution through geological time that are indistinguishable from those 21 of ATP synthase, RNA polymerase, or the ribosome-some of the oldest known enzymes. 22Our work suggests that water oxidation originated during the establishment of bioenergetics 23 reaching farther into the past than can be documented based on species trees alone. 24 25 extant species 2 . Thus, the origin of oxygenic photosynthesis antedates the MRCA of 34 Cyanobacteria by an undetermined amount of time. Cyanobacteria's closest living relatives 35 are the clades known as Vampirovibrionia (formerly Melainabacteria) 3,4 , followed by 36 Sericytochromatia 5 and Margulisbacteria 6 . Currently, no photosynthetic strains have been 37 described in these groups of uncultured bacteria and this has led to the hypothesis that 38 oxygenic photosynthesis arose during the time spanning the divergence of Vampirovibrionia 39 and the MRCA of Cyanobacteria starting from an entirely non-photosynthetic ancestral 40 state 5,7 . Molecular clock studies have suggested that the span of time between Cyanobacteria 41 and Vampirovibrionia could be of several hundred million years 8,9 . However, it is still 42 unclear from molecular clock analyses and the microfossil record when exactly the MRCA of 43 Cyanobacteria started to diversify 10 . Alternatively, it is possible that these novel clades 44 emerged from photosynthetic ancestors. In agreement with this, we recently showed that the 45 span of time between the origin of a water-splitting photosystem and the MRCA of 46 Cyanobacteria, a period of time that we refer to as ΔT, could be well over a billion years 11 . 47 heterodimeric PSII, but also that it split water and had evolved protective mechanisms against 67 the formation of reactive oxygen species 11,16,17 . 68 Here, to help in timing the evolution of oxygenic photosynthesis, Cyanobacteria and 69 MSV, we compared the duplication leading to the RC antenna subunits, CP43 and CP47, to 70 several well-defined ancient and more recent events: including, but not limited to, the 71 duplication of the core catalytic subunits of ATP synthase, a very ancient event generally 72 accepted to have occurred before the last universal common ancestor (LUCA) [18][19][20][21][22] ; the 73 evolution of RNA polymerase catalytic subunit β (RpoB) and ribosomal proteins, which are 74 universally conserve...

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“…D2 subunit of PSII to synthesize Chl f [28]. Remarkably, it was shown that, by engineering chimeric D1/ChlF proteins in Synechocystis sp.…”

Section: Co2mentioning

confidence: 99%

“…Remarkably, it was shown that, by engineering chimeric D1/ChlF proteins in Synechocystis sp. PCC 6803, which natively does not harbor Chl f pigments, the engineered strain could synthesize Chl f pigments [28]. The chimera strategy could potentially be interesting to enable Chl f synthesis in microalgae.…”

Section: Co2mentioning

confidence: 99%