Evolution Of Oxygenic Photosynthesis Research Articles

Simulating biosignatures from pre-oxygen photosynthesizing life on TRAPPIST-1e

ABSTRACT In order to assess observational evidence for potential atmospheric biosignatures on exoplanets, it will be essential to test whether spectral fingerprints from multiple gases can be explained by abiotic or biotic-only processes. Here, we develop and apply a coupled 1D atmosphere-ocean-ecosystem model to understand how primitive biospheres, which exploit abiotic sources of H$_2$, CO, and O$_2$, could influence the atmospheric composition of rocky terrestrial exoplanets. We apply this to the Earth at 3.8 Ga and to TRAPPIST-1e. We focus on metabolisms that evolved before the evolution of oxygenic photosynthesis, which consume H$_2$ and CO and produce potentially detectable levels of CH$_4$. O$_2$-consuming metabolisms are also considered for TRAPPIST-1e, as abiotic O$_2$ production is predicted on M-dwarf orbiting planets. We show that these biospheres can lead to high levels of surface O$_2$ (approximately 1–5 per cent) as a result of CO consumption, which could allow high O$_2$ scenarios, by removing the main loss mechanisms of atomic oxygen. Increasing stratospheric temperatures, which increases atmospheric OH can reduce the likelihood of such a state forming. O$_2$-consuming metabolisms could also lower O$_2$ levels to around 10 ppm and support a productive biosphere at low reductant inputs. Using predicted transmission spectral features from CH$_4$, CO, O$_2$/O$_3$, and CO$_2$ across the hypothesis space for tectonic reductant input, we show that biotically produced CH$_4$ may only be detectable at high reductant inputs. CO is also likely to be a dominant feature in transmission spectra for planets orbiting M-dwarfs, which could reduce the confidence in any potential biosignature observations linked to these biospheres.

From cyanobacteria and cyanophages to chloroplasts: the fate of the genomes of oxyphototrophs and the genes encoding photosystem II proteins.

Chloroplasts are the result of endosymbiosis of cyanobacterial organisms with proto-eukaryotes. The psbA, psbD and psbO genes are present in all oxyphototrophs and encode the D1/D2 proteins of photosystem II (PSII) and PsbO, respectively. PsbO is a peripheral protein that stabilizes the O2-evolving complex in PSII. Of these genes, psbA and psbD remained in the chloroplastic genome, while psbO was transferred to the nucleus. The genomes of selected cyanobacteria, chloroplasts and cyanophages carrying psbA and psbD, respectively, were analysed. The highest density of genes and coding sequences (CDSs) was estimated for the genomes of cyanophages, cyanobacteria and chloroplasts. The synonymous mutation rate (rS) of psbA and psbD in chloroplasts remained almost unchanged and is lower than that of psbO. The results indicate that the decreasing genome size in chloroplasts is more similar to the genome reduction observed in contemporary endosymbiotic organisms than in streamlined genomes of free-living cyanobacteria. The rS of atpA, which encodes the α-subunit of ATP synthase in chloroplasts, suggests that psbA and psbD, and to a lesser extent psbO, are ancient and conservative and arose early in the evolution of oxygenic photosynthesis. The role of cyanophages in the evolution of oxyphototrophs and chloroplastic genomes is discussed.

Chapter 5: Major Biological Innovations in the History of Life on Earth.

All organisms living on Earth descended from a single, common ancestral population of cells, known as LUCA-the last universal common ancestor. Since its emergence, the diversity and complexity of life have increased dramatically. This chapter focuses on four key biological innovations throughout Earth's history that had a significant impact on the expansion of phylogenetic diversity, organismal complexity, and ecospace habitation. First is the emergence of the last universal common ancestor, LUCA, which laid the foundation for all life-forms on Earth. Second is the evolution of oxygenic photosynthesis, which resulted in global geochemical and biological transformations. Third is the appearance of a new type of cell-the eukaryotic cell-which led to the origin of a new domain of life and the basis for complex multicellularity. Fourth is the multiple independent origins of multicellularity, resulting in the emergence of a new level of complex individuality. A discussion of these four key events will improve our understanding of the intertwined history of our planet and its inhabitants and better inform the extent to which we can expect life at different degrees of diversity and complexity elsewhere.

The greening ashore.

More than half a billion years ago a streptophyte algal lineage began terraforming the terrestrial habitat and the Earth's atmosphere. This pioneering step enabled the subsequent evolution of all complex life on land, and the past decade has uncovered that many traits, both morphological and genetic, once thought to be unique to land plants, are conserved across some streptophyte algae. They provided the common ancestor of land plants with a repertoire of genes, of which many were adapted to overcome the new biotic and abiotic challenges. Exploring these molecular adaptations in non-tracheophyte species may help us to better prepare all green life, including our crops, for the challenges precipitated by the climate change of the Anthropocene because the challenges mostly differ by the speed with which they are now being met.

High nitrite–nitrogen stress intensity drives nitrite anaerobic oxidation to nitrate and inhibits methanogenesis

Nitrite is an important intermediate in nitrogen metabolism. We explored the effect of nitrite–nitrogen stress intensity (NNSI) on nitrite metabolism and methanogenesis in anaerobic digestion. The results showed that the NNSI regulated microbial diversity, composition, and functions, and microbial community assembly was primarily shaped by stochastic processes. Moreover, the NNSI was negatively correlated with α-diversity and positively correlated with non-metric multi-dimensional scaling distance. Denitrification gradually increased with increasing NNSI; however, methanogenesis was gradually inhibited, which was primarily due to the inhibition of the aceticlastic methanogenesis pathway (i.e., Methanosaeta) and methylotrophic methanogenesis pathway (i.e., Candidatus_Methanofastidiosum). High NNSI (1882 ± 98.99 mg/L NO2−-N) promoted nitrite anaerobic oxidation to nitrate and was favorable for dissimilatory nitrate reduction to ammonia (DNRA). We present evidence for the microbial transformation of nitrite under anaerobic conditions, with potential geochemical and evolutionary importance. As nitrogen oxides were already present on early Earth, our finding presents the possibility of a nitrogen cycle before the evolution of oxygenic photosynthesis.

The Great Oxidation Event preceded a Paleoproterozoic “snowball Earth”

The inability to resolve the exact temporal relationship between two pivotal events in Earth history, the Paleoproterozoic Great Oxidation Event (GOE) and the first "snowball Earth" global glaciation, has precluded assessing causality between changing atmospheric composition and ancient climate change. Here we present temporally resolved quadruple sulfur isotope measurements (δ34S, ∆33S, and ∆36S) from the Paleoproterozoic Seidorechka and Polisarka Sedimentary Formations on the Fennoscandian Shield, northwest Russia, that address this issue. Sulfides in the former preserve evidence of mass-independent fractionation of sulfur isotopes (S-MIF) falling within uncertainty of the Archean reference array with a ∆36S/∆33S slope of -1.8 and have small negative ∆33S values, whereas in the latter mass-dependent fractionation of sulfur isotopes (S-MDF) is evident, with a ∆36S/∆33S slope of -8.8. These trends, combined with geochronological constraints, place the S-MIF/S-MDF transition, the key indicator of the GOE, between 2,501.5 ± 1.7 Ma and 2,434 ± 6.6 Ma. These are the tightest temporal and stratigraphic constraints yet for the S-MIF/S-MDF transition and show that its timing in Fennoscandia is consistent with the S-MIF/S-MDF transition in North America and South Africa. Further, the glacigenic part of the Polisarka Formation occurs 60 m above the sedimentary succession containing S-MDF signals. Hence, our findings confirm unambiguously that the S-MIF/S-MDF transition preceded the Paleoproterozoic snowball Earth. Resolution of this temporal relationship constrains cause-and-effect drivers of Earth's oxygenation, specifically ruling out conceptual models in which global glaciation precedes or causes the evolution of oxygenic photosynthesis.

Two Distinct Photoprocesses in Cyanobacterial Bilin Pigments: Energy Migration in Light‐Harvesting Phycobiliproteins versus Photoisomerization in Phytochromes

The evolution of oxygenic photosynthesis, respiration and photoperception are connected with the appearance of cyanobacteria. The key compounds, which are involved in these processes, are tetrapyrroles: open chain - bilins and cyclic - chlorophylls and heme. The latter are characterized by their covalent bond with the apoprotein resulting in the formation of biliproteins. This type of photoreceptors is unique in that it can perform important and opposite functions-light-harvesting in photosynthesis with the participation of phycobiliproteins and photoperception mediated by phycochromes and phytochromes. In this review, cyanobacterial phycobiliproteins and phytochrome Cph1 are considered from a comparative point of view. Structural features of these pigments, which provide their contrasting photophysical and photochemical characteristics, are analyzed. The determining factor in the case of energy migration with the participation of phycobiliproteins is blocking the torsional relaxations of the chromophore, its D-ring, in the excited state and their freedom, in the case of phytochrome photoisomerization. From the energetics point of view, this distinction is preconditioned by the height of the activation barrier for the photoreaction and relaxation in the excited state, which depends on the degree of the chromophore fixation by its protein surroundings.

Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen.

The balance between sources and sinks of molecular oxygen in the oceans has greatly impacted the composition of Earth's atmosphere since the evolution of oxygenic photosynthesis, thereby exerting key influence on Earth's climate and the redox state of (sub)surface Earth. The canonical source and sink terms of the marine oxygen budget include photosynthesis, respiration, photorespiration, the Mehler reaction, and other smaller terms. However, recent advances in understanding cryptic oxygen cycling, namely the ubiquitous one-electron reduction of O2 to superoxide by microorganisms outside the cell, remains unexplored as a potential player in global oxygen dynamics. Here we show that dark extracellular superoxide production by marine microbes represents a previously unconsidered global oxygen flux and sink comparable in magnitude to other key terms. We estimate that extracellular superoxide production represents a gross oxygen sink comprising about a third of marine gross oxygen production, and a net oxygen sink amounting to 15 to 50% of that. We further demonstrate that this total marine dark extracellular superoxide flux is consistent with concentrations of superoxide in marine environments. These findings underscore prolific marine sources of reactive oxygen species and a complex and dynamic oxygen cycle in which oxygen consumption and corresponding carbon oxidation are not necessarily confined to cell membranes or exclusively related to respiration. This revised model of the marine oxygen cycle will ultimately allow for greater reconciliation among estimates of primary production and respiration and a greater mechanistic understanding of redox cycling in the ocean.

Widespread deposition of greenalite to form Banded Iron Formations before the Great Oxidation Event

Banded Iron Formations (BIFs) are Precambrian sedimentary rocks interpreted to have been precipitated from anoxic seawater prior to the first permanent rise in atmospheric oxygen in the Great Oxidation Event at ca. 2.45–2.32 Ga. BIFs hold the key to understanding the chemistry of the oceans and atmosphere, and how these interacted with microbial life, prior to and during the evolution of oxygenic photosynthesis. To unlock this information, it is essential to know how BIFs formed, that is, what minerals were precipitated, by what mechanisms and in which environments. BIFs are found in almost all depositional settings at times when input of clastic detritus was lacking, for example, submarine proximal volcanic environments, basin floor, slope, deep marine shelf and shallow shelf settings. High-resolution electron microscopy of finely laminated BIFs and ferruginous cherts that range in age from 3.45 to ca. 2.4 Ga and that preserve depositional features indicates that the original sediment was a very fine mud composed of nanoparticles of the iron-silicate greenalite. In places, the greenalite mud experienced very early silicification on the sea floor enabling preservation of the mineral and its depositional textures. Very fine grained siderite and hematite in laminated BIFs post-date dehydration of the early silica cement and are not primary minerals. Greenalite nanoparticles are found in BIFs from all depositional settings indicating a common origin, likely precipitation resulting from mixing of plume water from hydrothermal vents with ambient seawater. The nanoparticles were carried throughout the oceans and were deposited on the seafloor and on continental margins to form the primary sediments of BIFs.

Evolutionary trends in RuBisCO kinetics and their co-evolution with CO2 concentrating mechanisms.

RuBisCO-catalyzed CO2 fixation is the main source of organic carbon in the biosphere. This enzyme is present in all domains of life in different forms (III, II, and I) and its origin goes back to 3500Mya, when the atmosphere was anoxygenic. However, the RuBisCO active site also catalyzes oxygenation of ribulose 1,5-bisphosphate, therefore, the development of oxygenic photosynthesis and the subsequent oxygen-rich atmosphere promoted the appearance of CO2 concentrating mechanisms (CCMs) and/or the evolution of a more CO2 -specific RuBisCO enzyme. The wide variability in RuBisCO kinetic traits of extant organisms reveals a history of adaptation to the prevailing CO2 /O2 concentrations and the thermal environment throughout evolution. Notable differences in the kinetic parameters are found among the different forms of RuBisCO, but the differences are also associated with the presence and type of CCMs within each form, indicative of co-evolution of RuBisCO and CCMs. Trade-offs between RuBisCO kinetic traits vary among the RuBisCO forms and also among phylogenetic groups within the same form. These results suggest that different biochemical and structural constraints have operated on each type of RuBisCO during evolution, probably reflecting different environmental selective pressures. In a similar way, variations in carbon isotopic fractionation of the enzyme point to significant differences in its relationship to the CO2 specificity among different RuBisCO forms. A deeper knowledge of the natural variability of RuBisCO catalytic traits and the chemical mechanism of RuBisCO carboxylation and oxygenation reactions raises the possibility of finding unrevealed landscapes in RuBisCO evolution.

Great Oxidation and Lomagundi events linked by deep cycling and enhanced degassing of carbon.

For approximately the first 2 billion years of Earth history, atmospheric oxygen levels were extremely low. It wasn’t until at least half a billion years after the evolution of oxygenic photosynthesis, perhaps as early as 3 billion years ago, that oxygen rose to appreciable levels during the Great Oxidation event. Shortly after, marine carbonates experienced a large positive spike in carbon isotope ratios known as the Lomagundi event. The mechanisms responsible for the Great Oxidation and Lomagundi events remain debated. Using a carbon-oxygen box model which tracks surface and interior C fluxes and reservoirs while also tracking C isotopes and atmospheric oxygen levels we demonstrate that about 2.5 billion years ago a tectonic transition resulting in increased volcanic CO2 emissions could have led to increased deposition of both carbonates and organic carbon via enhanced weathering and nutrient delivery to oceans. Increased burial of carbonates and organic carbon would have allowed accumulation of atmospheric oxygen while also increasing delivery of carbon to subduction zones. Coupled with preferential release of carbonates at arc volcanoes and deep recycling of organic C to ocean island volcanoes we find such a tectonic transition can simultaneously explain the Great Oxidation and Lomagundi events without any change in the fraction of carbon buried as organic carbon relative to carbonate, which is often invoked to explain carbon isotope excursions.

Bound manganese oxides capable of reducing the bacteriochlorophyll dimer of modified reaction centers from Rhodobacter sphaeroides

A biohybrid model system is described that interfaces synthetic Mn-oxides with bacterial reaction centers to gain knowledge concerning redox reactions by metal clusters in proteins, in particular the Mn4CaO5 cluster of photosystem II. The ability of Mn-oxides to bind to modified bacterial reaction centers and transfer an electron to the light-induced oxidized bacteriochlorophyll dimer, P+, was characterized using optical spectroscopy. The environment of P was altered to obtain a high P/P+ midpoint potential. In addition, different metal-binding sites were introduced by substitution of amino acid residues as well as extension of the C-terminus of the M subunit with the C-terminal region of the D1 subunit of photosystem II. The Mn-compounds MnO2, αMn2O3, Mn3O4, CaMn2O4, and Mn3(PO4)2 were tested and compared to MnCl2. In general, addition of the Mn-compounds resulted in a decrease in the amount of P+ while the reduced quinone was still present, demonstrating that the Mn-compounds can serve as secondary electron donors. The extent of P+ reduction for the Mn-oxides was largest for αMn2O3 and CaMn2O4 and smallest for Mn3O4 and MnO2. The addition of Mn3(PO4)2 resulted in nearly complete P+ reduction, similar to MnCl2. Overall, the activity was correlated with the initial oxidation state of the Mn-compound. Transient optical measurements showed a fast kinetic component, assigned to reduction of P+ by the Mn-oxide, in addition to a slow component due to charge recombination. The results support the conjecture that the incorporation of Mn-oxides by ancient anoxygenic phototrophs was a step in the evolution of oxygenic photosynthesis.

Can organic haze and O2 plumes explain patterns of sulfur mass-independent fractionation during the Archean?

The existence of mass-independently fractionated sulfur in Archean rocks is almost universally accepted as evidence for low atmospheric O2 and O3 concentrations at that time. But the detailed patterns of the Δ33S values and of the ratios Δ33S/δ34S and Δ36S/Δ33S remain to be explained, and the mechanism for producing the mass-independent fractionation remains controversial. Here, we explore the hypothesis that the relatively low Δ33S values seen during the Mid-Archean, 2.7-3.5 Ga, were caused by the presence of organic haze produced from photolysis of methane. This haze helped shield SO2 from photolysis, while at the same time providing surfaces on which unfractionated short-chain sulfur species could condense. The evolution of oxygenic photosynthesis, and the concomitant disappearance of organic haze towards the end of the Archean allowed more negatively fractionated S4 and S8 to form, thereby generating large positive fractionations in other sulfur species, including sulfate and H2S. Reduction of this sulfate to H2S by bacteria, followed by incorporation of H2S into pyrite, produced the large positive Δ33S values observed in the Neoarchean rock record, 2.5-2.7 Ga.

Cysteine, glutathione and a new genetic code: biochemical adaptations of the primordial cells that spread into open water and survived biospheric oxygenation.

Life most likely developed under hyperthermic and anaerobic conditions in close vicinity to a stable geochemical source of energy. Epitomizing this conception, the first cells may have arisen in submarine hydrothermal vents in the middle of a gradient established by the hot and alkaline hydrothermal fluid and the cooler and more acidic water of the ocean. To enable their escape from this energy-providing gradient layer, the early cells must have overcome a whole series of obstacles. Beyond the loss of their energy source, the early cells had to adapt to a loss of external iron-sulfur catalysis as well as to a formidable temperature drop. The developed solutions to these two problems seem to have followed the principle of maximum parsimony: Cysteine was introduced into the genetic code to anchor iron-sulfur clusters, and fatty acid unsaturation was installed to maintain lipid bilayer viscosity. Unfortunately, both solutions turned out to be detrimental when the biosphere became more oxidizing after the evolution of oxygenic photosynthesis. To render cysteine thiol groups and fatty acid unsaturation compatible with life under oxygen, numerous counter-adaptations were required including the advent of glutathione and the addition of the four latest amino acids (methionine, tyrosine, tryptophan, selenocysteine) to the genetic code. In view of the continued diversification of derived antioxidant mechanisms, it appears that modern life still struggles with the initially developed strategies to escape from its hydrothermal birthplace. Only archaea may have found a more durable solution by entirely exchanging their lipid bilayer components and rigorously restricting cysteine usage.

Methane in the Precambrian atmosphere

Biological methane production occurs in anoxic terrestrial wetlands and in sulfate depleted marine sediments. It has been suggested that methanogens may have flourished in the anoxic and sulfate-poor environments of the Precambrian ocean, generating large amounts of methane that would have accumulated in the atmosphere and warmed the early Earth. However, modern ferruginous and sulfate-poor environments such as Lake Matano are not very efficient at generating methane, converting only about 5% of organic carbon to CH4 despite the lack of alternative remineralization pathways. We apply this restriction to a simple model of marine carbon cycling in order to generate new estimates of methane concentrations in the Precambrian atmosphere. Our results suggest that, if the ancient biosphere were similarly inefficient, atmospheric methane concentrations did not exceed 1 ppm, or about twice the pre-industrial value, at any time during the Proterozoic. Following the evolution of oxygenic photosynthesis, the maximum methane concentration in the Archean atmosphere was order 100 ppm, but no more than 1 ppm if steady state oxygen concentrations were greater than 10−8 present atmospheric levels. Substantially larger methane concentrations are only possible before the evolution of oxygenic photosynthesis.

Geobiological feedbacks and the evolution of thermoacidophiles

Oxygen-dependent microbial oxidation of sulfur compounds leads to the acidification of natural waters. How acidophiles and their acidic habitats evolved, however, is largely unknown. Using 16S rRNA gene abundance and composition data from 72 hot springs in Yellowstone National Park, Wyoming, we show that hyperacidic (pH<3.0) hydrothermal ecosystems are dominated by a limited number of archaeal lineages with an inferred ability to respire O2. Phylogenomic analyses of 584 existing archaeal genomes revealed that hyperacidophiles evolved independently multiple times within the Archaea, each coincident with the emergence of the ability to respire O2, and that these events likely occurred in the recent evolutionary past. Comparative genomic analyses indicated that archaeal thermoacidophiles from independent lineages are enriched in similar protein-coding genes, consistent with convergent evolution aided by horizontal gene transfer. Because the generation of acidic environments and their successful habitation characteristically require O2, these results suggest that thermoacidophilic Archaea and the acidity of their habitats co-evolved after the evolution of oxygenic photosynthesis. Moreover, it is likely that dissolved O2 concentrations in thermal waters likely did not reach levels capable of sustaining aerobic thermoacidophiles and their acidifying activity until ~0.8 Ga, when present day atmospheric levels were reached, a time period that is supported by our estimation of divergence times for archaeal thermoacidophilic clades.

Depth-dependent δ13C trends in platform and slope settings of the Campbellrand-Malmani carbonate platform and possible implications for Early Earth oxygenation

The evolution of oxygenic photosynthesis is widely seen as the major biological factor for the profound shift from reducing to slightly oxidizing conditions in Earth’s atmosphere during the Archean-Proterozoic transition period. The delay from the first biogenic production of oxygen and the permanent oxidation of Earth’s atmosphere during the early Paleoproteorozoic Great Oxidation Event (GOE) indicates that significant environmental modifications were necessary for an effective accumulation of metabolically produced oxygen. Here we report a distinct temporal shift to heavier carbon isotope signatures in lagoonal and intertidal carbonates (δ13Ccarb from −1.6 to +0.4‰, relative to VPDB) and organic matter (δ13Corg from about −40 to −25‰, relative to VPDB) from the 2.58–2.50Gy old shallow-marine Campbellrand-Malmani carbonate platform (South Africa). This indicates an enhanced primary production and lateral transport of organic material offshore to greater depths as well as a change from an anaerobic to an aerobic ecosystem. Trace element data indicate limited influx of reducing species from deep open ocean water into the platform and an increased supply of nutrients from the continent, both supporting primary production and an increasing oxidation state of the platform interior. These restricted conditions allowed that the dissolved inorganic carbon (DIC) pool in the platform interior developed differently than the open ocean. This is supported by coeval carbonates from the marginal slope setting, which had a higher interaction with open ocean water and do not record a comparable shift in δ13Ccarb throughout the sequence. We propose that the emergence of stable shallow-water carbonate platforms in the Neoarchean provided ideal conditions for the evolution of early aerobic ecosystems, which finally led to the full oxidation of Earth’s atmosphere during the GOE.

Red-edge position of habitable exoplanets around M-dwarfs

One of the possible signs of life on distant habitable exoplanets is the red-edge, which is a rise in the reflectivity of planets between visible and near-infrared (NIR) wavelengths. Previous studies suggested the possibility that the red-edge position for habitable exoplanets around M-dwarfs may be shifted to a longer wavelength than that for Earth. We investigated plausible red-edge position in terms of the light environment during the course of the evolution of phototrophs. We show that phototrophs on M-dwarf habitable exoplanets may use visible light when they first evolve in the ocean and when they first colonize the land. The adaptive evolution of oxygenic photosynthesis may eventually also use NIR radiation, by one of two photochemical reaction centers, with the other center continuing to use visible light. These “two-color” reaction centers can absorb more photons, but they will encounter difficulty in adapting to drastically changing light conditions at the boundary between land and water. NIR photosynthesis can be more productive on land, though its evolution would be preceded by the Earth-type vegetation. Thus, the red-edge position caused by photosynthetic organisms on habitable M-dwarf exoplanets could initially be similar to that on Earth and later move to a longer wavelength.

Algal light sensing and photoacclimation in aquatic environments.

Anoxygenic photosynthetic prokaryotes arose in ancient oceans ~3.5 billion years ago. The evolution of oxygenic photosynthesis by cyanobacteria followed soon after, enabling eukaryogenesis and the evolution of complex life. The Archaeplastida lineage dates back ~1.5 billion years to the domestication of a cyanobacterium. Eukaryotic algae have subsequently radiated throughout oceanic/freshwater/terrestrial environments, adopting distinctive morphological and developmental strategies for adaptation to diverse light environments. Descendants of the ancestral photosynthetic alga remain challenged by a typical diurnally fluctuating light supply ranging from ~0 to ~2000μEm-2 s-1 . Such extreme changes in light intensity and variations in light quality have driven the evolution of novel photoreceptors, light-harvesting complexes and photoprotective mechanisms in photosynthetic eukaryotes. This minireview focuses on algal light sensors, highlighting the unexpected roles for linear tetrapyrroles (bilins) in the maintenance of functional chloroplasts in chlorophytes, sister species to streptophyte algae and land plants.

Evolution of the acceptor side of photosystem I: ferredoxin, flavodoxin, and ferredoxin-NADP+ oxidoreductase.

The development of oxygenic photosynthesis by primordial cyanobacteria ~2.7billion years ago led to major changes in the components and organization of photosynthetic electron transport to cope with the challenges of an oxygen-enriched atmosphere. We review herein, following the seminal contributions as reported by Jaganathan et al. (Functional genomics and evolution of photosynthetic systems, vol 33, advances in photosynthesis and respiration, Springer, Dordrecht, 2012), how these changes affected carriers and enzymes at the acceptor side of photosystem I (PSI): the electron shuttle ferredoxin (Fd), its isofunctional counterpart flavodoxin (Fld), their redox partner ferredoxin-NADP+ reductase (FNR), and the primary PSI acceptors F x and F A/F B. Protection of the [4Fe-4S] centers of these proteins from oxidative damage was achieved by strengthening binding between the F A/F B polypeptide and the reaction center core containing F x, therefore impairing O2 access to the clusters. Immobilization of F A/F B in the PSI complex led in turn to the recruitment of new soluble electron shuttles. This function was fulfilled by oxygen-insensitive [2Fe-2S] Fd, in which the reactive sulfide atoms of the cluster are shielded from solvent by the polypeptide backbone, and in some algae and cyanobacteria by Fld, which employs a flavin as prosthetic group and is tolerant to oxidants and iron limitation. Tight membrane binding of FNR allowed solid-state electron transfer from PSI bridged by Fd/Fld. Fine tuning of FNR catalytic mechanism led to formidable increases in turnover rates compared with FNRs acting in heterotrophic pathways, favoring Fd/Fld reduction instead of oxygen reduction.