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      Cyanobacteria evolution: Insight from the fossil record

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          Abstract

          Cyanobacteria played an important role in the evolution of Early Earth and the biosphere. They are responsible for the oxygenation of the atmosphere and oceans since the Great Oxidation Event around 2.4 Ga, debatably earlier. They are also major primary producers in past and present oceans, and the ancestors of the chloroplast. Nevertheless, the identification of cyanobacteria in the early fossil record remains ambiguous because the morphological criteria commonly used are not always reliable for microfossil interpretation. Recently, new biosignatures specific to cyanobacteria were proposed. Here, we review the classic and new cyanobacterial biosignatures. We also assess the reliability of the previously described cyanobacteria fossil record and the challenges of molecular approaches on modern cyanobacteria. Finally, we suggest possible new calibration points for molecular clocks, and strategies to improve our understanding of the timing and pattern of the evolution of cyanobacteria and oxygenic photosynthesis.

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          Highlights

          • Origin and evolution of cyanobacteria, oxygenic photosynthesis and plasts are debated.

          • Cyanobacterial fossil record starts unambiguously at 1.89–1.84 Ga.

          • Classic and new cyanobacterial signatures, and their fossil record are reassessed.

          • Challenges of molecular phylogenies and clocks are reviewed.

          • New possible calibration points for molecular clocks are suggested.

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          Most cited references221

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          Dating the rise of atmospheric oxygen.

          Several lines of geological and geochemical evidence indicate that the level of atmospheric oxygen was extremely low before 2.45 billion years (Gyr) ago, and that it had reached considerable levels by 2.22 Gyr ago. Here we present evidence that the rise of atmospheric oxygen had occurred by 2.32 Gyr ago. We found that syngenetic pyrite is present in organic-rich shales of the 2.32-Gyr-old Rooihoogte and Timeball Hill formations, South Africa. The range of the isotopic composition of sulphur in this pyrite is large and shows no evidence of mass-independent fractionation, indicating that atmospheric oxygen was present at significant levels (that is, greater than 10(-5) times that of the present atmospheric level) during the deposition of these units. The presence of rounded pebbles of sideritic iron formation at the base of the Rooihoogte Formation and an extensive and thick ironstone layer consisting of haematitic pisolites and oölites in the upper Timeball Hill Formation indicate that atmospheric oxygen rose significantly, perhaps for the first time, during the deposition of the Rooihoogte and Timeball Hill formations. These units were deposited between what are probably the second and third of the three Palaeoproterozoic glacial events.
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            Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing.

            The cyanobacterial phylum encompasses oxygenic photosynthetic prokaryotes of a great breadth of morphologies and ecologies; they play key roles in global carbon and nitrogen cycles. The chloroplasts of all photosynthetic eukaryotes can trace their ancestry to cyanobacteria. Cyanobacteria also attract considerable interest as platforms for "green" biotechnology and biofuels. To explore the molecular basis of their different phenotypes and biochemical capabilities, we sequenced the genomes of 54 phylogenetically and phenotypically diverse cyanobacterial strains. Comparison of cyanobacterial genomes reveals the molecular basis for many aspects of cyanobacterial ecophysiological diversity, as well as the convergence of complex morphologies without the acquisition of novel proteins. This phylum-wide study highlights the benefits of diversity-driven genome sequencing, identifying more than 21,000 cyanobacterial proteins with no detectable similarity to known proteins, and foregrounds the diversity of light-harvesting proteins and gene clusters for secondary metabolite biosynthesis. Additionally, our results provide insight into the distribution of genes of cyanobacterial origin in eukaryotic nuclear genomes. Moreover, this study doubles both the amount and the phylogenetic diversity of cyanobacterial genome sequence data. Given the exponentially growing number of sequenced genomes, this diversity-driven study demonstrates the perspective gained by comparing disparate yet related genomes in a phylum-wide context and the insights that are gained from it.
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              A whiff of oxygen before the great oxidation event?

              High-resolution chemostratigraphy reveals an episode of enrichment of the redox-sensitive transition metals molybdenum and rhenium in the late Archean Mount McRae Shale in Western Australia. Correlations with organic carbon indicate that these metals were derived from contemporaneous seawater. Rhenium/osmium geochronology demonstrates that the enrichment is a primary sedimentary feature dating to 2501 +/- 8 million years ago (Ma). Molybdenum and rhenium were probably supplied to Archean oceans by oxidative weathering of crustal sulfide minerals. These findings point to the presence of small amounts of O2 in the environment more than 50 million years before the start of the Great Oxidation Event.
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                Author and article information

                Contributors
                Journal
                Free Radic Biol Med
                Free Radic. Biol. Med
                Free Radical Biology & Medicine
                Elsevier Science
                0891-5849
                1873-4596
                20 August 2019
                20 August 2019
                : 140
                : 206-223
                Affiliations
                [a ]Early Life Traces & Evolution - Astrobiology, UR ASTROBIOLOGY, Geology Department, University of Liège, Liège, Belgium
                [b ]Eukaryotic Phylogenomics, InBioS-PhytoSYSTEMS, University of Liège, Liège, Belgium
                [c ]BCCM/ULC Cyanobacteria Collection, InBioS-CIP, Centre for Protein Engineering, University of Liège, Liège, Belgium
                Author notes
                []Corresponding author. cdemoulin@ 123456uliege.be
                [1]

                These authors contributed equally to this work.

                Article
                S0891-5849(18)32484-5
                10.1016/j.freeradbiomed.2019.05.007
                6880289
                31078731
                f9ab1eb9-70e2-4e28-af72-cdb36c7aac93
                © 2019 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 29 November 2018
                : 13 March 2019
                : 5 May 2019
                Categories
                Article

                Molecular biology
                biosignatures,cyanobacteria,evolution,microfossils,molecular clocks,precambrian
                Molecular biology
                biosignatures, cyanobacteria, evolution, microfossils, molecular clocks, precambrian

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