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      100 years of anthropogenic impact causes changes in freshwater functional biodiversity

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          Abstract

          Despite efforts from scientists and regulators, biodiversity is declining at an alarming rate. Unless we find transformative solutions to preserve biodiversity, future generations may not be able to enjoy nature’s services. We have developed a conceptual framework that establishes the links between biodiversity dynamics and abiotic change through time and space using artificial intelligence. Here, we apply this framework to a freshwater ecosystem with a known history of human impact and study 100 years of community-level biodiversity, climate change and chemical pollution trends. We apply explainable network models with multimodal learning to community-level functional biodiversity measured with multilocus metabarcoding, to establish correlations with biocides and climate change records. We observed that the freshwater community assemblage and functionality changed over time without returning to its original state, even if the lake partially recovered in recent times. Insecticides and fungicides, combined with extreme temperature events and precipitation, explained up to 90% of the functional biodiversity changes. The community-level biodiversity approach used here reliably explained freshwater ecosystem shifts. These shifts were not observed when using traditional quality indices (e.g. Trophic Diatom Index). Our study advocates the use of high-throughput systemic approaches on long-term trends over species-focused ecological surveys to identify the environmental factors that cause loss of biodiversity and disrupt ecosystem functions.

          eLife digest

          Over long periods of time, environmental changes – such as chemical pollution and climate change – affect the diversity of organisms that live in an ecosystem, known as ‘biodiversity’. Understanding the impact of these changes is challenging because they can happen slowly, their effect is only measurable after years, and historical records are limited. This can make it difficult to determine when specific changes happened, what might have driven them and what impact they might be having.

          One way to measure changes in biodiversity over time is by analysing traces of DNA shed by organisms. Plants, animals, and bacteria living in lakes leave behind genetic material that gets trapped and buried in the sediment at the bottom of lakes. Similarly, biocides – substances used to kill or control populations of living organisms – that run-off into lakes leach into the sediment and can be measured years later. Therefore, this sediment holds a record of life and environmental impacts in the lake over past centuries.

          Eastwood, Zhou et al. wanted to understand the relationship between environmental changes (such as the use of biocides and climate change) and shifts in lake biodiversity. To do so, the researchers studied a lake community that had experienced major environmental impacts over the last century (including nutrient pollution, chemical pollution and climate change), but which appeared to improve over the last few years of the 20 th century.

          Using machine learning to find connections over time between biodiversity and non-living environmental changes, Eastwood, Zhou et al. showed that, despite apparent recovery in water quality, the biodiversity of the lake was not restored to its original state. A combination of climate factors (such as rainfall levels and extreme temperatures) and biocide application (particularly insecticides and fungicides) explained up to 90% of the biodiversity changes that occurred in the lake. These changes had not been identified before using traditional techniques. The functional roles microorganisms played in the ecosystem (such as degradation and nitrogen metabolism) were also altered, suggesting that loss of biodiversity may lead to loss of ecosystem functions.

          The findings described by Eastwood, Zhou et al. can be used by environmental regulators to identify species or ecosystems at risk from environmental change and prioritise them for intervention. The approach can also be used to identify which chemicals pose the greatest threat to biodiversity. Additionally, the use of environmental DNA from sediment can provide rich historical biodiversity data, which can be used to train artificial intelligence-based models to improve predictions of how ecosystems will respond to complex environmental changes.

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          Most cited references83

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          DADA2: High resolution sample inference from Illumina amplicon data

          We present DADA2, a software package that models and corrects Illumina-sequenced amplicon errors. DADA2 infers sample sequences exactly, without coarse-graining into OTUs, and resolves differences of as little as one nucleotide. In several mock communities DADA2 identified more real variants and output fewer spurious sequences than other methods. We applied DADA2 to vaginal samples from a cohort of pregnant women, revealing a diversity of previously undetected Lactobacillus crispatus variants.
            • Record: found
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            Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.

            The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                07 November 2023
                2023
                : 12
                : RP86576
                Affiliations
                [1 ] Environmental Genomics Group, School of Biosciences, University of Birmingham ( https://ror.org/03angcq70) Birmingham United Kingdom
                [2 ] School of Geography, Earth & Environmental Sciences, University of Birmingham ( https://ror.org/03angcq70) Birmingham United Kingdom
                [3 ] Department Evolutionary Ecology & Environmental Toxicology, Faculty of Biological Sciences, Goethe University Frankfurt ( https://ror.org/04cvxnb49) Frankfurt Germany
                [4 ] Lake Group, Department of Ecoscience, Aarhus University ( https://ror.org/01aj84f44) Aarhus Denmark
                [5 ] School of Natural Sciences, Environment Centre Wales, Deiniol Road, Bangor University ( https://ror.org/006jb1a24) Bangor United Kingdom
                [6 ] Department Marine Sciences and Institute of Bioinformatics, University of Georgia ( https://ror.org/00te3t702) Athens United States
                [7 ] LOEWE Centre for Translational Biodiversity Genomics (LOEWE‐TBG) ( https://ror.org/0396gab88) Frankfurt Germany
                [8 ] Department Media-related Toxicology, Institute for Molecular Biology and Applied Ecology (IME) ( https://ror.org/03j85fc72) Frankfurt Germany
                [9 ] The Alan Turing Institute, British Library ( https://ror.org/035dkdb55) London United Kingdom
                Escuela Politécnica Nacional ( https://ror.org/02b4apg34) Ecuador
                Max Planck Institute for Biology Tübingen ( https://ror.org/0243gzr89) Germany
                Escuela Politécnica Nacional Ecuador
                University of Birmingham Birmingham United Kingdom
                University of Birmingham Birmingham United Kingdom
                University of Birmingham Birmingham United Kingdom
                University of Birmingham Birmingham United Kingdom
                University of Birmingham Birmingham United Kingdom
                Goethe University Frankfurt Frankfurt Germany
                Goethe University Frankfurt Frankfurt Germany
                Aarhus University Aarhus Denmark
                University of Birmingham Birmingham United Kingdom
                Bangor University Bangor United Kingdom
                University of Georgia Athens Greece
                Goethe University Frankfurt Frankfurt Germany
                University of Birmingham Birmingham United Kingdom
                Author notes
                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0003-2969-6091
                https://orcid.org/0000-0002-1025-718X
                https://orcid.org/0000-0002-4624-4073
                https://orcid.org/0000-0002-8538-4693
                https://orcid.org/0000-0003-2326-1564
                https://orcid.org/0000-0003-3124-3550
                https://orcid.org/0000-0002-1716-5624
                Article
                86576
                10.7554/eLife.86576
                10629823
                37933221
                f9c00298-b19c-40bc-88d2-26a8adab7a95
                © 2023, Eastwood, Zhou et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 26 February 2023
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100012338, Alan Turing Institute;
                Award ID: R-BIR-001
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000270, Natural Environment Research Council;
                Award ID: NE/N005716/1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100005687, Goethe-Universität Frankfurt am Main;
                Award ID: RobustNature Cluster of Excellence Initiative
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BB/M01116X/1
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Computational and Systems Biology
                Ecology
                Custom metadata
                High-throughput systemic approaches on long-term trends identify the environmental factors that cause loss of biodiversity and disrupt ecosystem functions.
                prc

                Life sciences
                sedadna,machine learning,freshwater,multilocus metabarcoding,functional biodiversity,none

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