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

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.

2020 ◽  
Author(s):  
Thomas Oliver ◽  
Patricia Sánchez-Baracaldo ◽  
Anthony W. Larkum ◽  
A. William Rutherford ◽  
Tanai Cardona

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.


2017 ◽  
Vol 114 (40) ◽  
pp. 10749-10754 ◽  
Author(s):  
Patrick M. Shih ◽  
Lewis M. Ward ◽  
Woodward W. Fischer

Various lines of evidence from both comparative biology and the geologic record make it clear that the biochemical machinery for anoxygenic photosynthesis was present on early Earth and provided the evolutionary stock from which oxygenic photosynthesis evolved ca. 2.3 billion years ago. However, the taxonomic identity of these early anoxygenic phototrophs is uncertain, including whether or not they remain extant. Several phototrophic bacterial clades are thought to have evolved before oxygenic photosynthesis emerged, including the Chloroflexi, a phylum common across a wide range of modern environments. Although Chloroflexi have traditionally been thought to be an ancient phototrophic lineage, genomics has revealed a much greater metabolic diversity than previously appreciated. Here, using a combination of comparative genomics and molecular clock analyses, we show that phototrophic members of the Chloroflexi phylum are not particularly ancient, having evolved well after the rise of oxygen (ca. 867 million years ago), and thus cannot be progenitors of oxygenic photosynthesis. Similarly, results show that the carbon fixation pathway that defines this clade—the 3-hydroxypropionate bicycle—evolved late in Earth history as a result of a series of horizontal gene transfer events, explaining the lack of geological evidence for this pathway based on the carbon isotope record. These results demonstrate the role of horizontal gene transfer in the recent metabolic innovations expressed within this phylum, including its importance in the development of a novel carbon fixation pathway.


2010 ◽  
Vol 365 (1541) ◽  
pp. 693-698 ◽  
Author(s):  
Michael L. Ginger ◽  
Geoffrey I. McFadden ◽  
Paul A. M. Michels

Metabolic innovation has facilitated the radiation of microbes into almost every niche environment on the Earth, and over geological time scales transformed the planet on which we live. A notable example of innovation is the evolution of oxygenic photosynthesis which was a prelude to the gradual transformation of an anoxic Earth into a world with oxygenated oceans and an oxygen-rich atmosphere capable of supporting complex multicellular organisms. The influence of microbial innovation on the Earth's history and the timing of pivotal events have been addressed in other recent themed editions of Philosophical Transactions of Royal Society B ( Cavalier-Smith et al . 2006 ; Bendall et al . 2008 ). In this issue, our contributors provide a timely history of metabolic innovation and adaptation within unicellular eukaryotes. In eukaryotes, diverse metabolic portfolios are compartmentalized across multiple membrane-bounded compartments (or organelles). However, as a consequence of pathway retargeting, organelle degeneration or novel endosymbiotic associations, the metabolic repertoires of protists often differ extensively from classic textbook descriptions of intermediary metabolism. These differences are often important in the context of niche adaptation or the structure of microbial communities. Fundamentally interesting in its own right, the biochemical, cell biological and phylogenomic investigation of organellar metabolism also has wider relevance. For instance, in some pathogens, notably those causing some of the most significant tropical diseases, including malaria, unusual organellar metabolism provides important new drug targets. Moreover, the study of organellar metabolism in protists continues to provide critical insight into our understanding of eukaryotic evolution.


2020 ◽  
Author(s):  
Tim Hahn ◽  
Jonas Kley ◽  
Diethelm Kaiser ◽  
Thomas Spies ◽  
Jörg Schlittenhardt ◽  
...  

<p>Seismotectonic regions are a basic input in seismic hazard assessment. Several seismotectonic regionalizations for Germany were proposed in the past. We are presently developing a new regionalization based on the definition in the Safety Standard of the Nuclear Safety Standards Commission KTA 2201.1 (2011-11): “A seismotectonic unit is a region for which uniformity is assumed regarding seismic activity, geological structure and development and, in particular, regarding neotectonic conditions. A seismotectonic unit may also be an earthquake source region.” Our new concept focusses on a transparent implementation of the required geological criteria. Our approach is to initially analyze those separately from present-day seismicity. Compared to existing source area models we strive for a better documentation and justification of the geological elements used to delimit seismotectonic regions. This includes an analysis of the geological history of structures in six time slices from the Permian to the Present that will be considered in the regionalization. The time slices are (1) Permian, (2) Triassic, (3) Jurassic to Early Cretaceous, (4) Late Cretaceous, (5) Cenozoic > 20 Ma and (6) Recent (< 20 Ma). They were chosen because they are separated by marked changes of stress and kinematic regimes and were associated with the evolution of new fault systems or reactivation of existing ones. The tectonic characteristics of the time slices are briefly described.</p><p>The present-day observable fault network comprises faults from all time slices. For each time slice, a subset of active faults will be extracted based on geological evidence for fault activity at that time, e.g. syntectonic deposits. The uncertainties of these age assignments will be documented. The fault subset will be used to estimate overall kinematics, a paleo-stress field and to delimit little deformed or stable areas. Faults, kinematics, stress and stable areas can then be compared to present-day seismicity/active faults, slip directions, stress and undeformed areas as well as other parameters such as crustal and lithospheric thickness. These steps are repeated for each time slice. The superposition of active faults and stable regions across all time slices will identify faults prone to reactivation and regions that remained undeformed over geological time, potentially indicating areas of increased or reduced present-day seismic hazard.</p><p>A comparison with seismicity of the last 1000 years shows partial agreement between regions of strong (or repeated) deformation and regions of higher seismicity. On the other hand, stronger earthquakes occasionally cluster in regions appearing stable since Permian time, the Anglo-Brabant Massif being a prominent example of this type.</p>


Author(s):  
Olga Chernomor ◽  
Lena Peters ◽  
Judith Schneidewind ◽  
Anita Loeschcke ◽  
Esther Knieps-Grünhagen ◽  
...  

Abstract Light-dependent protochlorophyllide oxidoreductase (LPOR) and dark-operative protochlorophyllide oxidoreductase are evolutionary and structurally distinct enzymes that are essential for the synthesis of (bacterio)chlorophyll, the primary pigment needed for both anoxygenic and oxygenic photosynthesis. In contrast to the long-held hypothesis that LPORs are only present in oxygenic phototrophs, we recently identified a functional LPOR in the aerobic anoxygenic phototrophic bacterium (AAPB) Dinoroseobacter shibae and attributed its presence to a single horizontal gene transfer event from cyanobacteria. Here, we provide evidence for the more widespread presence of genuine LPOR enzymes in AAPBs. An exhaustive bioinformatics search identified 36 putative LPORs outside of oxygenic phototrophic bacteria (cyanobacteria) with the majority being AAPBs. Using in vitro and in vivo assays, we show that the large majority of the tested AAPB enzymes are genuine LPORs. Solution structural analyses, performed for two of the AAPB LPORs, revealed a globally conserved structure when compared with a well-characterized cyanobacterial LPOR. Phylogenetic analyses suggest that LPORs were transferred not only from cyanobacteria but also subsequently between proteobacteria and from proteobacteria to Gemmatimonadetes. Our study thus provides another interesting example for the complex evolutionary processes that govern the evolution of bacteria, involving multiple horizontal gene transfer events that likely occurred at different time points and involved different donors.


2008 ◽  
Vol 363 (1504) ◽  
pp. 2705-2716 ◽  
Author(s):  
Paul G Falkowski ◽  
Linda V Godfrey

The biogeochemical cycles of H, C, N, O and S are coupled via biologically catalysed electron transfer (redox) reactions. The metabolic processes responsible for maintaining these cycles evolved over the first ca 2.3 Ga of Earth's history in prokaryotes and, through a sequence of events, led to the production of oxygen via the photobiologically catalysed oxidation of water. However, geochemical evidence suggests that there was a delay of several hundred million years before oxygen accumulated in Earth's atmosphere related to changes in the burial efficiency of organic matter and fundamental alterations in the nitrogen cycle. In the latter case, the presence of free molecular oxygen allowed ammonium to be oxidized to nitrate and subsequently denitrified. The interaction between the oxygen and nitrogen cycles in particular led to a negative feedback, in which increased production of oxygen led to decreased fixed inorganic nitrogen in the oceans. This feedback, which is supported by isotopic analyses of fixed nitrogen in sedimentary rocks from the Late Archaean, continues to the present. However, once sufficient oxygen accumulated in Earth's atmosphere to allow nitrification to out-compete denitrification, a new stable electron ‘market’ emerged in which oxygenic photosynthesis and aerobic respiration ultimately spread via endosymbiotic events and massive lateral gene transfer to eukaryotic host cells, allowing the evolution of complex (i.e. animal) life forms. The resulting network of electron transfers led a gas composition of Earth's atmosphere that is far from thermodynamic equilibrium (i.e. it is an emergent property), yet is relatively stable on geological time scales. The early coevolution of the C, N and O cycles, and the resulting non-equilibrium gaseous by-products can be used as a guide to search for the presence of life on terrestrial planets outside of our Solar System.


Author(s):  
Donald Eugene Canfield

This chapter discusses the evolution of oxygen-producing organisms by considering the evolution and assembly of its basic constituent parts. It focuses on the following key questions: (1) What is the evolutionary history of chlorophyll? (2) What are the evolutionary histories of photosystem I and photosystem II (PSII)? (3) What is the origin of the oxygen-evolving complex in PSII? And finally, (4) what is the evolutionary history of Rubisco? In addressing these, the chapter seeks to understand the complex path leading to the evolution of oxygenic photosynthesis on Earth. This event was one of the major transforming events in the history of life. With no oxygenic photosynthesis, there would be no oxygen in the atmosphere; there would also be no plants, no animals, and nobody to tell this story.


2006 ◽  
Vol 361 (1474) ◽  
pp. 1819-1836 ◽  
Author(s):  
Don E Canfield ◽  
Minik T Rosing ◽  
Christian Bjerrum

Before the advent of oxygenic photosynthesis, the biosphere was driven by anaerobic metabolisms. We catalogue and quantify the source strengths of the most probable electron donors and electron acceptors that would have been available to fuel early-Earth ecosystems. The most active ecosystems were probably driven by the cycling of H 2 and Fe 2+ through primary production conducted by anoxygenic phototrophs. Interesting and dynamic ecosystems would have also been driven by the microbial cycling of sulphur and nitrogen species, but their activity levels were probably not so great. Despite the diversity of potential early ecosystems, rates of primary production in the early-Earth anaerobic biosphere were probably well below those rates observed in the marine environment. We shift our attention to the Earth environment at 3.8 Gyr ago, where the earliest marine sediments are preserved. We calculate, consistent with the carbon isotope record and other considerations of the carbon cycle, that marine rates of primary production at this time were probably an order of magnitude (or more) less than today. We conclude that the flux of reduced species to the Earth surface at this time may have been sufficient to drive anaerobic ecosystems of sufficient activity to be consistent with the carbon isotope record. Conversely, an ecosystem based on oxygenic photosynthesis was also possible with complete removal of the oxygen by reaction with reduced species from the mantle.


2018 ◽  
Vol 84 (16) ◽  
Author(s):  
Casey Bryce ◽  
Mirita Franz-Wachtel ◽  
Nicolas C. Nalpas ◽  
Jennyfer Miot ◽  
Karim Benzerara ◽  
...  

ABSTRACTThe oxidation of Fe(II) by anoxygenic photosynthetic bacteria was likely a key contributor to Earth's biosphere prior to the evolution of oxygenic photosynthesis and is still found in a diverse range of modern environments. All known phototrophic Fe(II) oxidizers can utilize a wide range of substrates, thus making them very metabolically flexible. However, the underlying adaptations required to oxidize Fe(II), a potential stressor, are not completely understood. We used a combination of quantitative proteomics and cryogenic transmission electron microscopy (cryo-TEM) to compare cells ofRhodopseudomonas palustrisTIE-1 grown photoautotrophically with Fe(II) or H2and photoheterotrophically with acetate. We observed unique proteome profiles for each condition, with differences primarily driven by carbon source. However, these differences were not related to carbon fixation but to growth and light harvesting processes, such as pigment synthesis. Cryo-TEM showed stunted development of photosynthetic membranes in photoautotrophic cultures. Growth on Fe(II) was characterized by a response typical of iron homeostasis, which included an increased abundance of proteins required for metal efflux (particularly copper) and decreased abundance of iron import proteins, including siderophore receptors, with no evidence of further stressors, such as oxidative damage. This study suggests that the main challenge facing anoxygenic phototrophic Fe(II) oxidizers comes from growth limitations imposed by autotrophy, and, once this challenge is overcome, iron stress can be mitigated using iron management mechanisms common to diverse bacteria (e.g., by control of iron influx and efflux).IMPORTANCEThe cycling of iron between redox states leads to the precipitation and dissolution of minerals, which can in turn impact other major biogeochemical cycles, such as those of carbon, nitrogen, phosphorus and sulfur. Anoxygenic phototrophs are one of the few drivers of Fe(II) oxidation in anoxic environments and are thought to contribute significantly to iron cycling in both modern and ancient environments. These organisms thrive at high Fe(II) concentrations, yet the adaptations required to tolerate the stresses associated with this are unclear. Despite the general consensus that high Fe(II) concentrations pose numerous stresses on these organisms, our study of the large-scale proteome response of a model anoxygenic phototroph to Fe(II) oxidation demonstrates that common iron homeostasis strategies are adequate to manage this. The bulk of the proteome response is not driven by adaptations to Fe(II) stress but to adaptations required to utilize an inorganic carbon source. Such a global overview of the adaptation of these organisms to Fe(II) oxidation provides valuable insights into the physiology of these biogeochemically important organisms and suggests that Fe(II) oxidation may not pose as many challenges to anoxygenic phototrophs as previously thought.


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