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      Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origins

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          Abstract

          Establishing a unified timescale for the early evolution of Earth and Life is challenging and mired in controversy because of the paucity of fossil evidence, the difficulty of interpreting it, and dispute over the deepest branching relationships in the tree of life. Surprisingly, it remains perhaps the only episode in the history of Life where literal interpretations of the fossil record hold sway, revised with every new discovery and reinterpretation. We derive a timescale of life, combining a reappraisal of the fossil material with new molecular clock analyses. We find that the last universal common ancestor of cellular life (LUCA) predated the end of late heavy bombardment (>3.9 Ga). The crown clades of the two primary divisions of life, Eubacteria and Archaebacteria, emerged much later (<3.4 Ga), relegating the oldest fossil evidence for life to their stem lineages. The Great Oxidation Event significantly predates the origin of modern Cyanobacteria, indicating that photosynthesis evolved within the cyanobacterial stem-lineage. Modern eukaryotes emerged late in Earth history (<1.84 Ga), falsifying the hypothesis that the GOE facilitated their radiation. The symbiotic origin of mitochondria, at 2.053 – 1.21 Ga reflects a late origin of the eukaryotes, that do not constitute a primary linage of life.

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          Estimating the timing of early eukaryotic diversification with multigene molecular clocks.

          Although macroscopic plants, animals, and fungi are the most familiar eukaryotes, the bulk of eukaryotic diversity is microbial. Elucidating the timing of diversification among the more than 70 lineages is key to understanding the evolution of eukaryotes. Here, we use taxon-rich multigene data combined with diverse fossils and a relaxed molecular clock framework to estimate the timing of the last common ancestor of extant eukaryotes and the divergence of major clades. Overall, these analyses suggest that the last common ancestor lived between 1866 and 1679 Ma, consistent with the earliest microfossils interpreted with confidence as eukaryotic. During this interval, the Earth's surface differed markedly from today; for example, the oceans were incompletely ventilated, with ferruginous and, after about 1800 Ma, sulfidic water masses commonly lying beneath moderately oxygenated surface waters. Our time estimates also indicate that the major clades of eukaryotes diverged before 1000 Ma, with most or all probably diverging before 1200 Ma. Fossils, however, suggest that diversity within major extant clades expanded later, beginning about 800 Ma, when the oceans began their transition to a more modern chemical state. In combination, paleontological and molecular approaches indicate that long stems preceded diversification in the major eukaryotic lineages.
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            Evidence for life on Earth before 3,800 million years ago.

            It is unknown when life first appeared on Earth. The earliest known microfossils (approximately 3,500 Myr before present) are structurally complex, and if it is assumed that the associated organisms required a long time to develop this degree of complexity, then the existence of life much earlier than this can be argued. But the known examples of crustal rocks older than 3,500 Myr have experienced intense metamorphism, which would have obliterated any fragile microfossils contained therein. It is therefore necessary to search for geochemical evidence of past biotic activity that has been preserved within minerals that are resistant to metamorphism. Here we report ion-microprobe measurements of the carbon-isotope composition of carbonaceous inclusions within grains of apatite (basic calcium phosphate) from the oldest known sediment sequences--a approximately 3,800-Myr-old banded iron formation from the Isua supracrustal belt, West Greenland, and a similar formation from the nearby Akilia island that is possibly older than 3,850 Myr. The carbon in the carbonaceous inclusions is isotopically light, indicative of biological activity; no known abiotic process can explain the data. Unless some unknown abiotic process exists which is able both to create such isotopically light carbon and then selectively incorporate it into apatite grains, our results provide evidence for the emergence of life on Earth by at least 3,800 Myr before present.
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              Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics.

              Methanogenic and methanotrophic archaea play important roles in the global flux of methane. Culture-independent approaches are providing deeper insight into the diversity and evolution of methane-metabolizing microorganisms, but, until now, no compelling evidence has existed for methane metabolism in archaea outside the phylum Euryarchaeota. We performed metagenomic sequencing of a deep aquifer, recovering two near-complete genomes belonging to the archaeal phylum Bathyarchaeota (formerly known as the Miscellaneous Crenarchaeotal Group). These genomes contain divergent homologs of the genes necessary for methane metabolism, including those that encode the methyl-coenzyme M reductase (MCR) complex. Additional non-euryarchaeotal MCR-encoding genes identified in a range of environments suggest that unrecognized archaeal lineages may also contribute to global methane cycling. These findings indicate that methane metabolism arose before the last common ancestor of the Euryarchaeota and Bathyarchaeota.
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                Author and article information

                Journal
                101698577
                46074
                Nat Ecol Evol
                Nat Ecol Evol
                Nature ecology & evolution
                2397-334X
                24 July 2018
                20 August 2018
                October 2018
                20 February 2019
                : 2
                : 10
                : 1556-1562
                Affiliations
                [1 ]School of Earth Sciences, University of Bristol, Life Sciences Building, Tyndall Avenue, Bristol BS8 1TQ, UK
                [2 ]School of Biological Sciences, University of Bristol, Life Sciences Building, Tyndall Avenue, Bristol BS8 1TQ, UK
                Author notes
                [* ]Author for correspondence davide.pisani@ 123456bristol.ac.uk
                Article
                EMS78644
                10.1038/s41559-018-0644-x
                6152910
                30127539
                21900195-3998-4ec5-8578-803fe18b1a63

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