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      Dead or alive: sediment DNA archives as tools for tracking aquatic evolution and adaptation

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          Abstract

          DNA can be preserved in marine and freshwater sediments both in bulk sediment and in intact, viable resting stages. Here, we assess the potential for combined use of ancient, environmental, DNA and timeseries of resurrected long-term dormant organisms, to reconstruct trophic interactions and evolutionary adaptation to changing environments. These new methods, coupled with independent evidence of biotic and abiotic forcing factors, can provide a holistic view of past ecosystems beyond that offered by standard palaeoecology, help us assess implications of ecological and molecular change for contemporary ecosystem functioning and services, and improve our ability to predict adaptation to environmental stress.

          Abstract

          Ellegaard et al. discuss the potential for using ancient environmental DNA (eDNA), combined with resurrection ecology, to analyse trophic interactions and evolutionary adaptation to changing environments. Their Review suggests that these techniques will improve our ability to predict genetic and phenotypic adaptation to environmental stress.

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          Most cited references73

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          Host-parasite 'Red Queen' dynamics archived in pond sediment.

          Antagonistic interactions between hosts and parasites are a key structuring force in natural populations, driving coevolution. However, direct empirical evidence of long-term host-parasite coevolution, in particular 'Red Queen' dynamics--in which antagonistic biotic interactions such as host-parasite interactions can lead to reciprocal evolutionary dynamics--is rare, and current data, although consistent with theories of antagonistic coevolution, do not reveal the temporal dynamics of the process. Dormant stages of both the water flea Daphnia and its microparasites are conserved in lake sediments, providing an archive of past gene pools. Here we use this fact to reconstruct rapid coevolutionary dynamics in a natural setting and show that the parasite rapidly adapts to its host over a period of only a few years. A coevolutionary model based on negative frequency-dependent selection, and designed to mimic essential aspects of our host-parasite system, corroborated these experimental results. In line with the idea of continuing host-parasite coevolution, temporal variation in parasite infectivity changed little over time. In contrast, from the moment the parasite was first found in the sediments, we observed a steady increase in virulence over time, associated with higher fitness of the parasite.
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            The half-life of DNA in bone: measuring decay kinetics in 158 dated fossils.

            Claims of extreme survival of DNA have emphasized the need for reliable models of DNA degradation through time. By analysing mitochondrial DNA (mtDNA) from 158 radiocarbon-dated bones of the extinct New Zealand moa, we confirm empirically a long-hypothesized exponential decay relationship. The average DNA half-life within this geographically constrained fossil assemblage was estimated to be 521 years for a 242 bp mtDNA sequence, corresponding to a per nucleotide fragmentation rate (k) of 5.50 × 10(-6) per year. With an effective burial temperature of 13.1°C, the rate is almost 400 times slower than predicted from published kinetic data of in vitro DNA depurination at pH 5. Although best described by an exponential model (R(2) = 0.39), considerable sample-to-sample variance in DNA preservation could not be accounted for by geologic age. This variation likely derives from differences in taphonomy and bone diagenesis, which have confounded previous, less spatially constrained attempts to study DNA decay kinetics. Lastly, by calculating DNA fragmentation rates on Illumina HiSeq data, we show that nuclear DNA has degraded at least twice as fast as mtDNA. These results provide a baseline for predicting long-term DNA survival in bone.
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              DEEP BIOSPHERE. Exploring deep microbial life in coal-bearing sediment down to ~2.5 km below the ocean floor.

              Microbial life inhabits deeply buried marine sediments, but the extent of this vast ecosystem remains poorly constrained. Here we provide evidence for the existence of microbial communities in ~40° to 60°C sediment associated with lignite coal beds at ~1.5 to 2.5 km below the seafloor in the Pacific Ocean off Japan. Microbial methanogenesis was indicated by the isotopic compositions of methane and carbon dioxide, biomarkers, cultivation data, and gas compositions. Concentrations of indigenous microbial cells below 1.5 km ranged from <10 to ~10(4) cells cm(-3). Peak concentrations occurred in lignite layers, where communities differed markedly from shallower subseafloor communities and instead resembled organotrophic communities in forest soils. This suggests that terrigenous sediments retain indigenous community members tens of millions of years after burial in the seabed.
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                Author and article information

                Contributors
                mell@kp.dk
                Journal
                Commun Biol
                Commun Biol
                Communications Biology
                Nature Publishing Group UK (London )
                2399-3642
                7 April 2020
                7 April 2020
                2020
                : 3
                : 169
                Affiliations
                [1 ]ISNI 0000 0001 0674 042X, GRID grid.5254.6, Department of Plant and Environmental Sciences, , University of Copenhagen, ; Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark
                [2 ]ISNI 0000 0004 1936 8411, GRID grid.9918.9, Department of Genetics and Genome Biology, , University of Leicester, ; University Road, Leicester, LE1 7RH UK
                [3 ]ISNI 0000 0001 0668 7884, GRID grid.5596.f, Ecology, Evolution and Biodiversity Conservation, KU-Leuven, ; Charles Deberiotstraat 32 - box 2439, 3000 Leuven, Belgium
                [4 ]ISNI 0000 0004 1936 7486, GRID grid.6572.6, University of Birmingham, School of Biosciences, ; Birmingham, B15 2TT UK
                [5 ]ISNI 0000 0000 9919 9582, GRID grid.8761.8, Department of Marine Sciences, , University of Gothenburg, ; Box 461, SE 405 30 Göteborg, Sweden
                [6 ]ISNI 0000 0001 1019 1419, GRID grid.410381.f, Finnish Environment Institute (SYKE), Marine Research Centre, ; P.O.Box 140, 00251 Helsinki, Finland
                [7 ]ISNI 0000 0001 2192 9124, GRID grid.4886.2, Winogradsky Institute of Microbiology RAS, ; prospect 60-letiya Oktyabrya 7/2, 117312 Moscow, Russia
                [8 ]ISNI 0000 0001 0942 6946, GRID grid.8356.8, School of Life Sciences, , University of Essex, ; Wivenhoe Park, Colchester, CO4 3SQ UK
                [9 ]ISNI 0000 0001 1017 5662, GRID grid.13508.3f, Glaciology and Climate Department, , Geological Survey of Denmark and Greenland (GEUS), ; Øster Voldgade 10, 1350 KBH-K København, Denmark
                [10 ]ISNI 0000 0004 1936 8542, GRID grid.6571.5, Department of Geography, , Loughborough University, ; Loughborough, Leicestershire LE11 3TU UK
                [11 ]Present Address: University College Copenhagen, Humletorvet 3, 1799 Copenhagen, Denmark
                [12 ]ISNI 0000 0001 2188 0463, GRID grid.423940.8, Present Address: Leibniz Institute for Baltic Sea Research Warnemünde, Department of Biological Oceanography, ; Seestraße 15, 18119 Rostock, Germany
                Author information
                http://orcid.org/0000-0002-6032-3376
                http://orcid.org/0000-0001-7655-2897
                http://orcid.org/0000-0001-9310-2230
                http://orcid.org/0000-0002-1497-8822
                http://orcid.org/0000-0003-0672-9161
                Article
                899
                10.1038/s42003-020-0899-z
                7138834
                32265485
                77d54ec8-9329-430a-b63a-bc21ff0e7e06
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 22 October 2019
                : 10 March 2020
                Categories
                Review Article
                Custom metadata
                © The Author(s) 2020

                ecosystem ecology,palaeontology,applied microbiology

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