Photosystem II is a Chimera of Reaction Centers

Cardona, Tanai

doi:10.1007/s00239-017-9784-x

Cited by 27 publications

(33 citation statements)

References 17 publications

(18 reference statements)

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“…However, recent detailed analysis of the phylogeny of RC proteins indicates that HGT of RCs to an ancestral nonphotosynthetic cyanobacterium from anoxygenic phototrophic bacteria is unlikely (Cardona 2016b); furthermore, the evolution of RC proteins shows that the last common ancestor to all phototrophic bacteria had already evolved Type I and Type II RC proteins from an earlier gene duplication event (Sousa et al 2013, Harel et al 2015. In addition, it has been argued that the evolution of the structural complexity of PSII and the origin of the oxygenevolving manganese cluster can only be explained if both types of RC had been evolving in cooperation since the dawn of photosynthesis and that water oxidation might therefore have occurred at a far earlier stage of evolution that previously thought (Cardona 2016b(Cardona , 2017. This translates to the phylogeny of RC subunits in PSII and PSI showing a significant phylogenetic distance to those in anoxygenic phototrophs assuming similar rates of evolution (Cardona 2015.…”

Section: Discussionmentioning

confidence: 99%

Early emergence of the FtsH proteases involved in photosystem II repair

Shao¹,

Cardona²,

Nixon³

2018

Photosynt.

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Efficient degradation of damaged D1 during the repair of PSII is carried out by a set of dedicated FtsH proteases in the thylakoid membrane. Here we investigated whether the evolution of FtsH could hold clues to the origin of oxygenic photosynthesis. A phylogenetic analysis of over 6000 FtsH protease sequences revealed that there are three major groups of FtsH proteases originating from gene duplication events in the last common ancestor of bacteria, and that the FtsH proteases involved in PSII repair form a distinct clade branching out before the divergence of FtsH proteases found in all groups of anoxygenic phototrophic bacteria. Furthermore, we showed that the phylogenetic tree of FtsH proteases in phototrophic bacteria is similar to that for Type I and Type II reaction centre proteins. We conclude that the phylogeny of FtsH proteases is consistent with an early origin of photosynthetic water oxidation chemistry.

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Section: Discussionmentioning

confidence: 99%

Early emergence of the FtsH proteases involved in photosystem II repair

Shao¹,

Cardona²,

Nixon³

2018

Photosynt.

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Section: Discussionmentioning

confidence: 99%

“…The reason why CP47, and in particular CP43, interact with the donor side of PSII is an unsolved mystery given the fact that their main role is that of light harvesting. It can be rationalized however if water oxidation started in a homodimeric reaction center early during the evolution of photosynthesis (Cardona, 2017) [Colour figure can be viewed at wileyonlinelibrary.com] ChlZ D1 and ChlZ D2 . These peripheral pigments are absent in anoxygenic Type II reaction centers but are present in Type I reaction centers indicating that they existed before the divergence of D1 and D2 (Cardona, 2015).…”

Section: A Protein Fold Between the 1st And 2nd Transmembrane Helicmentioning

confidence: 99%

Early Archean origin of Photosystem II

et al. 2018

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Photosystem II is a photochemical reaction center that catalyzes the light‐driven oxidation of water to molecular oxygen. Water oxidation is the distinctive photochemical reaction that permitted the evolution of oxygenic photosynthesis and the eventual rise of eukaryotes. At what point during the history of life an ancestral photosystem evolved the capacity to oxidize water still remains unknown. Here, we study the evolution of the core reaction center proteins of Photosystem II using sequence and structural comparisons in combination with Bayesian relaxed molecular clocks. Our results indicate that a homodimeric photosystem with sufficient oxidizing power to split water had already appeared in the early Archean about a billion years before the most recent common ancestor of all described Cyanobacteria capable of oxygenic photosynthesis, and well before the diversification of some of the known groups of anoxygenic photosynthetic bacteria. Based on a structural and functional rationale, we hypothesize that this early Archean photosystem was capable of water oxidation to oxygen and had already evolved protection mechanisms against the formation of reactive oxygen species. This would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.

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“…9 10 In the vicinity of YD in D2 there is no metal cluster and instead of ligands, several "space filling" 11 phenylalanine residues are found ( Figure 2). Like CP43, the CP47 subunit also has an extrinsic domain that 12 reaches into D2, but instead of ligands, phenylalanine residues are also present, one of them located just 3.4 13 Å from YD. These structural observations indicate that water oxidation could have originated in a 14 homodimeric system before the duplication of the protein ancestral to D1 and D2, and that D2 evolved a 15 unique hydrophobic space-filling plug to prevent the access of Mn and bulk water to YD, thereby eliminating 16 high potential catalysis on the D2 side of PSII.…”

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confidence: 99%

“…The presence of a divalent metal site in homodimeric Type I reaction centres so 8 distant from PSII, yet in a manner so similar to the Mn4CaO5 cluster, is intriguing and potentially significant 9 from an evolutionary perspective. 10 Structural parallels between the Ca 2+ -binding site in the homodimeric Type I reaction centre and the 11 Mn4CaO5 cluster in PSII indicate that their most recent common ancestor had a site that was readily 12 accessible to divalent cations at the donor side and near the photochemical pigments (P). The most recent 13 common ancestor of homodimeric Type I reaction centres and PSII is the ancestral photosystem existing 14 before the divergence of Type I and Type II reaction centres.…”

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confidence: 99%

Evolution of photochemical reaction centres: more twists?

Cardona

Rutherford

2018

Preprint

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8The earliest event recorded in the molecular evolution of photosynthesis is the structural and 9 functional specialisation of Type I (ferredoxin-reducing) and Type II (quinone-reducing) reaction 10 centres. Here we point out that the homodimeric Type I reaction centre of Heliobacteria has a Ca 2+ -11 binding site with a number of striking parallels to the Mn4CaO5 cluster of cyanobacterial 12 Photosystem II. This structural parallels indicate that water oxidation chemistry originated at the 13 divergence of Type I and Type II reaction centres. We suggests that this divergence was triggered by 14 a structural rearrangement of a core transmembrane helix resulting in a shift of the redox potential 15 of the electron donor side and electron acceptor side at the same time and in the same redox direction. 16 17 There is no consensus on when and how oxygenic photosynthesis originated. Both the timing and the 22 evolutionary mechanism are disputed. The timing ranges from the early Archean, 3.7 billion years ago [1-23 4] to immediately before the Great Oxidation Event (see Glossary), 2.4 billion years ago [5, 6]. 24 Mechanisms proposed range from ancient gene duplication events involving the photosystems in 25 protocyanobacteria [7, 8], to more recent horizontal gene transfer events into a non-photosynthetic 26 ancestor of Cyanobacteria [9,10]. However a complete scenario for the evolution of oxygenic 27 photosynthesis should first explain how and when water oxidation to oxygen originated at the level of the 28 photochemical reaction centre. That is, how and when Photosystem II (PSII) evolved the Mn4CaO5 29 cluster and the oxidising photochemistry required to split water (Figure 1). 30 In PSII the Mn4CaO5 cluster is coordinated by D1 and CP43 ( Figure 2) [11]. The carboxylic C-terminus 31 of A344 of D1 acts as a bidentate ligand that bridges the Ca 2+ and a Mn atom [13], numbered Mn2 in Figure 32 2. Several Mn ligands, D342, E333, and H332 are also provided from the C-terminal domain of D1. In the 33 same region, H337 provides a hydrogen-bond to a bridging oxygen (O3). In addition, two more ligands are 34 provided from the inner part of D1, D170 and E189, located in the region connecting the 3 rd and 4 th 35 transmembrane helices of D1. Furthermore, E354 from CP43 provides a bidentate ligand bridging to Mn2 36 and Mn3, and R357 provides a hydrogen-bond to O4 and is within 4.2 Å of the Ca 2+ . These two residues 37 are located in an extrinsic protein domain between the 5 th and 6 th helices of CP43 that reaches into the 38 electron donor-side of D1. 39 After charge separation the oxidised chlorophyll (PD1 + ) extracts an electron from the kinetically 40 competent redox active tyrosine, D1-Y161, known as YZ, forming the neutral tyrosyl radical, which in turn 41 oxidises the Mn4CaO5 cluster. YZ is hydrogen-bonded to H190 and the electron transfer step to PD1 + is 42 coupled to a movement of the hydroxyl proton to H190. There is no Mn4CaO5 cluster in D2 (Figure 2), 43 however the tyrosine-histidine pair is cons...

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Photosystem II is a Chimera of Reaction Centers

Cited by 27 publications

References 17 publications

Early emergence of the FtsH proteases involved in photosystem II repair

Early emergence of the FtsH proteases involved in photosystem II repair

Early Archean origin of Photosystem II

Evolution of photochemical reaction centres: more twists?

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