On the origin of oxygenic photosynthesis and Cyanobacteria

Sánchez‐Baracaldo, Patricia; Cardona, Tanai

doi:10.1111/nph.16249

Cited by 186 publications

(103 citation statements)

References 58 publications

(164 reference statements)

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“…Photosystem II (PSII) is the only enzyme that catalyzes the light-driven oxidation of water, a thermodynamically demanding reaction that drives photosynthesis, sustaining life on our planet (Hohmann-Marriott and Blankenship, 2011;Sanchez-Baracaldo and Cardona, 2020;Vinyard et al, 2013). This multi-subunit membrane protein complex is located in the thylakoid membranes of cyanobacteria, algae and plants.…”

Section: Introductionmentioning

confidence: 99%

How to build a water-splitting machine: structural insights into photosystem II assembly

Zabret

Bohn

Schuller

et al. 2020

Preprint

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Biogenesis of photosystem II (PSII), nature’s water splitting catalyst, is assisted by auxiliary proteins that form transient complexes with PSII components to facilitate stepwise assembly events. Using cryo-electron microscopy, we solved the structure of such a PSII assembly intermediate with 2.94 Å resolution. It contains three assembly factors (Psb27, Psb28, Psb34) and provides detailed insights into their molecular function. Binding of Psb28 induces large conformational changes at the PSII acceptor side, which distort the binding pocket of the mobile quinone (QB) and replace bicarbonate with glutamate as a ligand of the non-heme iron, a structural motif found in reaction centers of non-oxygenic photosynthetic bacteria. These results reveal novel mechanisms that protect PSII from damage during biogenesis until water splitting is activated. Our structure further demonstrates how the PSII active site is prepared for the incorporation of the Mn4CaO5 cluster, which performs the unique water splitting reaction.One Sentence HighlightThe high-resolution Cryo-EM structure of the photosystem II assembly intermediate PSII-I reveals how nature’s water splitting catalyst is assembled, protected and prepared for photoactivation by help of the three assembly factors Psb27, Psb28 and Psb34.

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Section: Introductionmentioning

confidence: 99%

How to build a water-splitting machine: structural insights into photosystem II assembly

Zabret

Bohn

Schuller

et al. 2020

Preprint

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“…The origin of oxygenic photosynthesis is considered a turning point in the history of life, marking the transition from the ancient world of anaerobes into a productive aerobic world that permitted the emergence of complex life [1]. Oxygenic photosynthesis starts with photosystem II (PSII), the water-oxidising and O 2 -evolving enzyme of Cyanobacteria and photosynthetic eukaryotes.…”

Section: Introductionmentioning

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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“…The closest modern descendants of the ancestral cyanobacteria that evolved into modern marine plankton cyanobacteria are filamentous non-heterocystous Synechococcales (Sánchez-Baracaldo, 2015; Sánchez-Baracaldo and Cardona, 2020). KatG was likely present in ancestors of marine cyanobacteria (Bernroitner et al, 2009; Zamocky et al, 2012), whereas KatE was likely horizontally transferred from Proteobacteria and Planctomycetes to some cyanobacterial linages (e.g.…”

Section: Discussionmentioning

confidence: 99%