scholarly journals Time-resolved comparative molecular evolution of oxygenic photosynthesis

2020 ◽  
Author(s):  
Thomas Oliver ◽  
Patricia Sánchez-Baracaldo ◽  
Anthony W. Larkum ◽  
A. William Rutherford ◽  
Tanai Cardona
Keyword(s):  
Photosystem Ii ◽  
Origin Of Life ◽  
Atp Synthase ◽  
Water Oxidation ◽  
Oxygenic Photosynthesis ◽  
Molecular Clocks ◽  
Species Trees ◽  
Geological Time ◽  
Anoxygenic Phototrophs ◽  
The Origin Of Life

AbstractOxygenic photosynthesis starts with the oxidation of water to O2, a light-driven reaction catalysed by photosystem II. Cyanobacteria are the only prokaryotes capable of water oxidation and therefore, it is assumed that relative to the origin of life and bioenergetics, the origin of oxygenic photosynthesis is a late innovation. However, when exactly water oxidation originated remains an unanswered question. Here we use relaxed molecular clocks to compare one of the two ancestral core duplications that are unique to water-oxidizing photosystem II, that leading to CP43 and CP47, with 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, of CP43 variants used in a variety of photoacclimation responses, and the speciation events 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 species trees alone.

scholarly journals Early Archean origin of Photosystem II

2017 ◽  
Author(s):  
Tanai Cardona ◽  
Patricia Sánchez-Baracaldo ◽  
A. William Rutherford ◽  
Anthony W. D. Larkum
Keyword(s):  
Photosystem Ii ◽  
Reaction Center ◽  
Water Oxidation ◽  
Photochemical Reaction ◽  
Early Stage ◽  
Oxygenic Photosynthesis ◽  
Recent Common Ancestor ◽  
Molecular Clocks ◽  
Most Recent Common Ancestor ◽  
History Of

AbstractPhotosystem 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 and had already evolved some level of protection against the formation of reactive oxygen species, which would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.

scholarly journals Untangling the sequence of events during the S2→ S3transition in photosystem II and implications for the water oxidation mechanism

2020 ◽  
Vol 117 (23) ◽  
pp. 12624-12635 ◽  
Author(s):  
Mohamed Ibrahim ◽  
Thomas Fransson ◽  
Ruchira Chatterjee ◽  
Mun Hon Cheah ◽  
Rana Hussein ◽  
...  
Keyword(s):  
Photosystem Ii ◽  
Water Oxidation ◽  
Donor Site ◽  
Oxidation Mechanism ◽  
Oxygenic Photosynthesis ◽  
Acceptor Site ◽  
Oxygen Evolving Complex ◽  
Ps Ii ◽  
Sequence Of Events ◽  
Large Channel

In oxygenic photosynthesis, light-driven oxidation of water to molecular oxygen is carried out by the oxygen-evolving complex (OEC) in photosystem II (PS II). Recently, we reported the room-temperature structures of PS II in the four (semi)stable S-states, S1, S2, S3, and S0, showing that a water molecule is inserted during the S2→ S3transition, as a new bridging O(H)-ligand between Mn1 and Ca. To understand the sequence of events leading to the formation of this last stable intermediate state before O2formation, we recorded diffraction and Mn X-ray emission spectroscopy (XES) data at several time points during the S2→ S3transition. At the electron acceptor site, changes due to the two-electron redox chemistry at the quinones, QAand QB, are observed. At the donor site, tyrosine YZand His190 H-bonded to it move by 50 µs after the second flash, and Glu189 moves away from Ca. This is followed by Mn1 and Mn4 moving apart, and the insertion of OX(H) at the open coordination site of Mn1. This water, possibly a ligand of Ca, could be supplied via a “water wheel”-like arrangement of five waters next to the OEC that is connected by a large channel to the bulk solvent. XES spectra show that Mn oxidation (τ of ∼350 µs) during the S2→ S3transition mirrors the appearance of OXelectron density. This indicates that the oxidation state change and the insertion of water as a bridging atom between Mn1 and Ca are highly correlated.

scholarly journals Mediator-assisted water oxidation by the ruthenium “blue dimer” cis,cis-[(bpy)2(H2O)RuORu(OH2)(bpy)2]4+

2008 ◽  
Vol 105 (46) ◽  
pp. 17632-17635 ◽  
Author(s):  
Javier J. Concepcion ◽  
Jonah W. Jurss ◽  
Joseph L. Templeton ◽  
Thomas J. Meyer
Keyword(s):  
Carbon Dioxide ◽  
Electron Transfer ◽  
Renewable Energy ◽  
Photosystem Ii ◽  
Water Splitting ◽  
Water Oxidation ◽  
Oxygenic Photosynthesis ◽  
Reduced Water ◽  
Insight Into ◽  
Recent Insight

Light-driven water oxidation occurs in oxygenic photosynthesis in photosystem II and provides redox equivalents directed to photosystem I, in which carbon dioxide is reduced. Water oxidation is also essential in artificial photosynthesis and solar fuel-forming reactions, such as water splitting into hydrogen and oxygen (2 H2O + 4 hν → O2 + 2 H2) or water reduction of CO2 to methanol (2 H2O + CO2 + 6 hν → CH3OH + 3/2 O2), or hydrocarbons, which could provide clean, renewable energy. The “blue ruthenium dimer,” cis,cis-[(bpy)2(H2O)RuIIIORuIII(OH2)(bpy)2]4+, was the first well characterized molecule to catalyze water oxidation. On the basis of recent insight into the mechanism, we have devised a strategy for enhancing catalytic rates by using kinetically facile electron-transfer mediators. Rate enhancements by factors of up to ≈30 have been obtained, and preliminary electrochemical experiments have demonstrated that mediator-assisted electrocatalytic water oxidation is also attainable.

scholarly journals Heimdallarchaeota harness light energy through photosynthesis

2020 ◽  
Author(s):  
Rui Liu ◽  
Ruining Cai ◽  
Jing Zhang ◽  
Chaomin Sun
Keyword(s):  
Molecular Evolution ◽  
Origin Of Life ◽  
Metabolic Pathways ◽  
Evolutionary History ◽  
Waste Product ◽  
Photosynthetic Apparatus ◽  
Strong Support ◽  
Oxygenic Photosynthesis ◽  
Photosynthetic Organisms ◽  
The Origin Of Life

AbstractPhotosynthesis is an ancient process that originated after the origin of life, and has only been found in the Bacterial and Eukaryotic kingdoms, but has never been reported in any member of the domain Archaea. Heimdallarchaeota, a member of Asgard archaea, are supposed as the most probable candidates (to date) for the archaeal protoeukaryote ancestor and might exist in light-exposed habitats during their evolutionary history. Here we describe the discovery that Heimdallarchaeota genomes are enriched for proteins formerly considered specific to photosynthetic apparatus and are suggestive performing oxygenic photosynthesis. Our results provide strong support for hypotheses in which Heimdallarchaeota harvest light by bacteriochlorophyll and/or carotenoid, then transport electron from photosystems to Calvin-Benson-Bassham cycle along with CO2 fixation and ATP biosynthesis, and release oxygen as a waste product. Given the possessing of phototrophic lifestyle together with other anaerobic and aerobic metabolic pathways, Heimdallarchaeota are firmly believed to be photomixotrophic and have a facultative aerobic metabolism. Our results expand our knowledge that archaea have played an important role in the molecular evolution of eukaryotic photosynthesis and raise the significant possibility that Heimdallarchaeota might be ancestor of eukaryotic photosynthetic organisms.

scholarly journals Palaeoproterozoic ice houses and the evolution of oxygen-mediating enzymes: the case for a late origin of photosystem II

2008 ◽  
Vol 363 (1504) ◽  
pp. 2755-2765 ◽  
Author(s):  
Joseph L Kirschvink ◽  
Robert E Kopp
Keyword(s):  
Causal Link ◽  
Oxygenic Photosynthesis ◽  
Sterol Synthesis ◽  
Redox Potentials ◽  
Geological Time ◽  
Geological Evidence ◽  
Evolutionary Pattern ◽  
Anoxygenic Phototrophs ◽  
Late Origin ◽  
Evolution Of Oxygen

Two major geological problems regarding the origin of oxygenic photosynthesis are (i) identifying a source of oxygen pre-dating the biological oxygen production and capable of driving the evolution of oxygen tolerance, and (ii) determining when oxygenic photosynthesis evolved. One solution to the first problem is the accumulation of photochemically produced H 2 O 2 at the surface of the glaciers and its subsequent incorporation into ice. Melting at the glacier base would release H 2 O 2 , which interacts with seawater to produce O 2 in an environment shielded from the lethal levels of ultraviolet radiation needed to produce H 2 O 2 . Answers to the second problem are controversial and range from 3.8 to 2.2 Gyr ago. A sceptical view, based on the metals that have the redox potentials close to oxygen, argues for the late end of the range. The preponderance of geological evidence suggests little or no oxygen in the Late Archaean atmosphere (less than 1 ppm). The main piece of evidence for an earlier evolution of oxygenic photosynthesis comes from lipid biomarkers. Recent work, however, has shown that 2-methylhopanes, once thought to be unique biomarkers for cyanobacteria, are also produced anaerobically in significant quantities by at least two strains of anoxygenic phototrophs. Sterane biomarkers provide the strongest evidence for a date 2.7 Gyr ago or above, and could also be explained by the common evolutionary pattern of replacing anaerobic enzymes with oxygen-dependent ones. Although no anaerobic sterol synthesis pathway has been identified in the modern biosphere, enzymes that perform the necessary chemistry do exist. This analysis suggests that oxygenic photosynthesis could have evolved close in geological time to the Makganyene Snowball Earth Event and argues for a causal link between the two.

scholarly journals Light-driven formation of manganese oxide by today’s photosystem II supports evolutionarily ancient manganese-oxidizing photosynthesis

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Petko Chernev ◽  
Sophie Fischer ◽  
Jutta Hoffmann ◽  
Nicholas Oliver ◽  
Ricardo Assunção ◽  
...  
Keyword(s):  
Photosystem Ii ◽  
Manganese Oxide ◽  
Water Oxidation ◽  
Manganese Oxides ◽  
Early Stage ◽  
Oxygenic Photosynthesis ◽  
Oxide Nanoparticles ◽  
Manganese Ions ◽  
Oxide Particles ◽  
Photosynthetic Water Oxidation

AbstractWater oxidation and concomitant dioxygen formation by the manganese-calcium cluster of oxygenic photosynthesis has shaped the biosphere, atmosphere, and geosphere. It has been hypothesized that at an early stage of evolution, before photosynthetic water oxidation became prominent, light-driven formation of manganese oxides from dissolved Mn(2+) ions may have played a key role in bioenergetics and possibly facilitated early geological manganese deposits. Here we report the biochemical evidence for the ability of photosystems to form extended manganese oxide particles. The photochemical redox processes in spinach photosystem-II particles devoid of the manganese-calcium cluster are tracked by visible-light and X-ray spectroscopy. Oxidation of dissolved manganese ions results in high-valent Mn(III,IV)-oxide nanoparticles of the birnessite type bound to photosystem II, with 50-100 manganese ions per photosystem. Having shown that even today’s photosystem II can form birnessite-type oxide particles efficiently, we propose an evolutionary scenario, which involves manganese-oxide production by ancestral photosystems, later followed by down-sizing of protein-bound manganese-oxide nanoparticles to finally yield today’s catalyst of photosynthetic water oxidation.

The Origin of Life

2014 ◽  
Author(s):  
S. Blair Hedges
Keyword(s):  
Origin Of Life ◽  
Hydrothermal Vents ◽  
Biological Evolution ◽  
Early Time ◽  
Molecular Clocks ◽  
Time Period ◽  
A Cell ◽  
The Origin Of Life ◽  
Successive Generations ◽  
Life On Earth

Biological evolution begins with the origin of life, but the subject is the perhaps the most interdisciplinary of any in science. Understanding how life began on Earth requires knowledge of the astronomical, geological, and atmospheric settings. However, those settings are in turn dependent on knowing the time period when life arose, which comes from the fossil and molecular records, including molecular clocks based on genetic mutations. Interrelated with the setting is the chemistry that generates the organic molecules used to assemble the first cells and carry the genetic information to successive generations of cells. But holding the chemical reactions and products together in a cell requires a membrane, and the assembly of that involves biophysics. Thus, we have all of the fields of science coming together to understand a single event that happened about four billion years ago and initiated the Tree of Life on Earth. Because little evidence of anything has remained from this early time, there have been enormous amounts of published speculation on this subject. Narratives on how life originated can be grouped by location (surface versus submarine hydrothermal vents), temperature (cold versus hot), source of energy (heterotrophic versus autotrophic), and evolutionary order (genetics-first versus metabolism-first). I use the last dichotomy here, only because it has a long history and renewed focus in recent years. Currently there is no consensus on any one theory for the origin of life, but this is an active field that has made great strides in recent decades.

scholarly journals Habitable worlds with no signs of life

2014 ◽  
Vol 372 (2014) ◽  
pp. 20130082 ◽  
Author(s):  
Charles S. Cockell
Keyword(s):  
Origin Of Life ◽  
Oxygenic Photosynthesis ◽  
Detailed Knowledge ◽  
Atmospheric Gases ◽  
Habitable Planets ◽  
Negative Results ◽  
The Origin Of Life ◽  
The Universe

‘Most habitable worlds in the cosmos will have no remotely detectable signs of life’ is proposed as a biological hypothesis to be tested in the study of exoplanets. Habitable planets could be discovered elsewhere in the Universe, yet there are many hypothetical scenarios whereby the search for life on them could yield negative results. Scenarios for habitable worlds with no remotely detectable signatures of life include: planets that are habitable, but have no biosphere (Uninhabited Habitable Worlds); planets with life, but lacking any detectable surface signatures of that life (laboratory examples are provided); and planets with life, where the concentrations of atmospheric gases produced or removed by biota are impossible to disentangle from abiotic processes because of the lack of detailed knowledge of planetary conditions (the ‘problem of exoplanet thermodynamic uncertainty’). A rejection of the hypothesis would require that the origin of life usually occurs on habitable planets, that spectrally detectable pigments and/or metabolisms that produce unequivocal biosignature gases (e.g. oxygenic photosynthesis) usually evolve and that the organisms that harbour them usually achieve a sufficient biomass to produce biosignatures detectable to alien astronomers.

scholarly journals Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions

2019 ◽  
Vol 116 (38) ◽  
pp. 18917-18922 ◽  
Author(s):  
David J. Vinyard ◽  
Syed Lal Badshah ◽  
M. Rita Riggio ◽  
Divya Kaur ◽  
Annaliesa R. Fanguy ◽  
...  
Keyword(s):  
Amino Acid ◽  
Photosystem Ii ◽  
Isotope Effect ◽  
Water Oxidation ◽  
Oxygenic Photosynthesis ◽  
Oxygen Evolving Complex ◽  
Solvent Isotope Effect ◽  
Solvent Isotope ◽  
Oxygen Evolving ◽  
Protein Environment

Photosystem II (PSII) performs the solar-driven oxidation of water used to fuel oxygenic photosynthesis. The active site of water oxidation is the oxygen-evolving complex (OEC), a Mn4CaO5 cluster. PSII requires degradation of key subunits and reassembly of the OEC as frequently as every 20 to 40 min. The metals for the OEC are assembled within the PSII protein environment via a series of binding events and photochemically induced oxidation events, but the full mechanism is unknown. A role of proton release in this mechanism is suggested here by the observation that the yield of in vitro OEC photoassembly is higher in deuterated water, D2O, compared with H2O when chloride is limiting. In kinetic studies, OEC photoassembly shows a significant lag phase in H2O at limiting chloride concentrations with an apparent H/D solvent isotope effect of 0.14 ± 0.05. The growth phase of OEC photoassembly shows an H/D solvent isotope effect of 1.5 ± 0.2. We analyzed the protonation states of the OEC protein environment using classical Multiconformer Continuum Electrostatics. Combining experiments and simulations leads to a model in which protons are lost from amino acid that will serve as OEC ligands as metals are bound. Chloride and D2O increase the proton affinities of key amino acid residues. These residues tune the binding affinity of Mn2+/3+ and facilitate the deprotonation of water to form a proposed μ-hydroxo bridged Mn2+Mn3+ intermediate.

scholarly journals Light-driven formation of high-valent manganese oxide by photosystem II supports evolutionary role in early bioenergetics

2020 ◽  
Author(s):  
Petko Chernev ◽  
Sophie Fischer ◽  
Jutta Hoffmann ◽  
Nicholas Oliver ◽  
Robert L. Burnap ◽  
...  
Keyword(s):  
Photosystem Ii ◽  
Water Oxidation ◽  
Early Stage ◽  
Oxygenic Photosynthesis ◽  
Oxide Nanoparticles ◽  
Mn Oxide ◽  
Oxide Particles ◽  
High Valent ◽  
Photosynthetic Water Oxidation ◽  
Mn Oxides

AbstractWater oxidation and concomitant O2-formation by the Mn4Ca cluster of oxygenic photosynthesis has shaped the biosphere, atmosphere, and geosphere. It has been hypothesized that at an early stage of evolution, before photosynthetic water oxidation became prominent, photosynthetic formation of Mn oxides from dissolved Mn(2+) ions may have played a key role in bioenergetics and possibly facilitated early geological manganese deposits. The biochemical evidence for the ability of photosystems to form extended Mn oxide particles, lacking until now, is provided herein. We tracked the light-driven redox processes in spinach photosystem II (PSII) particles devoid of the Mn4Ca clusters by UV-vis and X-ray spectroscopy. We find that oxidation of aqueous Mn(2+) ions results in PSII-bound Mn(III,IV)-oxide nanoparticles of the birnessite type comprising 50-100 Mn ions per PSII. Having shown that even today’s photosystem-II can form birnessite-type oxide particles efficiently, we propose an evolutionary scenario, which involves Mn-oxide production by ancestral photosystems, later followed by down-sizing of protein-bound Mn-oxide nanoparticles to finally yield today’s Mn4CaO5 cluster of photosynthetic water oxidation.

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