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      Environmental DNA from Seawater Samples Correlate with Trawl Catches of Subarctic, Deepwater Fishes

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          Abstract

          Remote polar and deepwater fish faunas are under pressure from ongoing climate change and increasing fishing effort. However, these fish communities are difficult to monitor for logistic and financial reasons. Currently, monitoring of marine fishes largely relies on invasive techniques such as bottom trawling, and on official reporting of global catches, which can be unreliable. Thus, there is need for alternative and non-invasive techniques for qualitative and quantitative oceanic fish surveys. Here we report environmental DNA (eDNA) metabarcoding of seawater samples from continental slope depths in Southwest Greenland. We collected seawater samples at depths of 188–918 m and compared seawater eDNA to catch data from trawling. We used Illumina sequencing of PCR products to demonstrate that eDNA reads show equivalence to fishing catch data obtained from trawling. Twenty-six families were found with both trawling and eDNA, while three families were found only with eDNA and two families were found only with trawling. Key commercial fish species for Greenland were the most abundant species in both eDNA reads and biomass catch, and interpolation of eDNA abundances between sampling sites showed good correspondence with catch sizes. Environmental DNA sequence reads from the fish assemblages correlated with biomass and abundance data obtained from trawling. Interestingly, the Greenland shark ( Somniosus microcephalus) showed high abundance of eDNA reads despite only a single specimen being caught, demonstrating the relevance of the eDNA approach for large species that can probably avoid bottom trawls in most cases. Quantitative detection of marine fish using eDNA remains to be tested further to ascertain whether this technique is able to yield credible results for routine application in fisheries. Nevertheless, our study demonstrates that eDNA reads can be used as a qualitative and quantitative proxy for marine fish assemblages in deepwater oceanic habitats. This relates directly to applied fisheries as well as to monitoring effects of ongoing climate change on marine biodiversity—especially in polar ecosystems.

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          Most cited references23

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          obitools: a unix-inspired software package for DNA metabarcoding.

          DNA metabarcoding offers new perspectives in biodiversity research. This recently developed approach to ecosystem study relies heavily on the use of next-generation sequencing (NGS) and thus calls upon the ability to deal with huge sequence data sets. The obitools package satisfies this requirement thanks to a set of programs specifically designed for analysing NGS data in a DNA metabarcoding context. Their capacity to filter and edit sequences while taking into account taxonomic annotation helps to set up tailor-made analysis pipelines for a broad range of DNA metabarcoding applications, including biodiversity surveys or diet analyses. The obitools package is distributed as an open source software available on the following website: http://metabarcoding.org/obitools. A Galaxy wrapper is available on the GenOuest core facility toolshed: http://toolshed.genouest.org.
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            Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding.

            Global biodiversity in freshwater and the oceans is declining at high rates. Reliable tools for assessing and monitoring aquatic biodiversity, especially for rare and secretive species, are important for efficient and timely management. Recent advances in DNA sequencing have provided a new tool for species detection from DNA present in the environment. In this study, we tested whether an environmental DNA (eDNA) metabarcoding approach, using water samples, can be used for addressing significant questions in ecology and conservation. Two key aquatic vertebrate groups were targeted: amphibians and bony fish. The reliability of this method was cautiously validated in silico, in vitro and in situ. When compared with traditional surveys or historical data, eDNA metabarcoding showed a much better detection probability overall. For amphibians, the detection probability with eDNA metabarcoding was 0.97 (CI = 0.90-0.99) vs. 0.58 (CI = 0.50-0.63) for traditional surveys. For fish, in 89% of the studied sites, the number of taxa detected using the eDNA metabarcoding approach was higher or identical to the number detected using traditional methods. We argue that the proposed DNA-based approach has the potential to become the next-generation tool for ecological studies and standardized biodiversity monitoring in a wide range of aquatic ecosystems.
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              Detection of a Diverse Marine Fish Fauna Using Environmental DNA from Seawater Samples

              Marine ecosystems worldwide are under threat with many fish species and populations suffering from human over-exploitation. This is greatly impacting global biodiversity, economy and human health. Intriguingly, marine fish are largely surveyed using selective and invasive methods, which are mostly limited to commercial species, and restricted to particular areas with favourable conditions. Furthermore, misidentification of species represents a major problem. Here, we investigate the potential of using metabarcoding of environmental DNA (eDNA) obtained directly from seawater samples to account for marine fish biodiversity. This eDNA approach has recently been used successfully in freshwater environments, but never in marine settings. We isolate eDNA from ½-litre seawater samples collected in a temperate marine ecosystem in Denmark. Using next-generation DNA sequencing of PCR amplicons, we obtain eDNA from 15 different fish species, including both important consumption species, as well as species rarely or never recorded by conventional monitoring. We also detect eDNA from a rare vagrant species in the area; European pilchard (Sardina pilchardus). Additionally, we detect four bird species. Records in national databases confirmed the occurrence of all detected species. To investigate the efficiency of the eDNA approach, we compared its performance with 9 methods conventionally used in marine fish surveys. Promisingly, eDNA covered the fish diversity better than or equal to any of the applied conventional methods. Our study demonstrates that even small samples of seawater contain eDNA from a wide range of local fish species. Finally, in order to examine the potential dispersal of eDNA in oceans, we performed an experiment addressing eDNA degradation in seawater, which shows that even small (100-bp) eDNA fragments degrades beyond detectability within days. Although further studies are needed to validate the eDNA approach in varying environmental conditions, our findings provide a strong proof-of-concept with great perspectives for future monitoring of marine biodiversity and resources.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                16 November 2016
                2016
                : 11
                : 11
                : e0165252
                Affiliations
                [1 ]Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark
                [2 ]Section for EvoGenomics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark
                [3 ]Technical University of Denmark, National Institute of Aquatic Resources, Charlottenlund, Denmark
                [4 ]Greenland Institute of Natural Resources, Nuuk, Greenland
                [5 ]Department of Zoology, University of Cambridge, Cambridge, United Kingdom
                [6 ]Wellcome Trust Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge, United Kingdom
                Central Michigan University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: PFT PRM OAJ EW.

                • Data curation: PFT PRM OAJ EES.

                • Formal analysis: PFT PRM OAJ EES SWK.

                • Funding acquisition: PFT PRM OAJ EW.

                • Investigation: PFT PRM OAJ.

                • Methodology: PFT PRM OAJ.

                • Project administration: PFT PRM OAJ EW.

                • Resources: PFT PRM OAJ EES SWK EW.

                • Software: PFT EES SWK.

                • Supervision: PFT PRM OAJ EW.

                • Validation: PFT PRM EES SWK.

                • Visualization: PFT PRM EES SWK.

                • Writing – original draft: PFT PRM OAJ.

                • Writing – review & editing: PFT PRM OAJ EW EES SWK.

                Article
                PONE-D-16-27987
                10.1371/journal.pone.0165252
                5112899
                27851757
                3f533709-efbe-4b13-92b1-6bd78c6a7f60
                © 2016 Thomsen et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 13 July 2016
                : 7 October 2016
                Page count
                Figures: 6, Tables: 1, Pages: 22
                Funding
                Danish National Research Foundation funded the work. Greenland Institute of Natural Resources, Greenland Self-government, Department for education and research funded the work. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Fishes
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Fishes
                Marine Fish
                Biology and Life Sciences
                Marine Biology
                Marine Fish
                Earth Sciences
                Marine and Aquatic Sciences
                Marine Biology
                Marine Fish
                Research and Analysis Methods
                Database and Informatics Methods
                Biological Databases
                Sequence Databases
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Sequencing Techniques
                Sequence Analysis
                Sequence Databases
                Research and Analysis Methods
                Molecular Biology Techniques
                Sequencing Techniques
                Sequence Analysis
                Sequence Databases
                Earth Sciences
                Hydrology
                Sea Water
                Biology and Life Sciences
                Taxonomy
                Computer and Information Sciences
                Data Management
                Taxonomy
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Fishes
                Chondrichthyes
                Elasmobranchii
                Sharks
                Biology and Life Sciences
                Agriculture
                Fisheries
                Custom metadata
                Illumina MiSeq raw sequence data are available from the Dryad Digital Repository ( http://dx.doi.org/10.5061/dryad.ch576). Full sequences for reference Greenlandic fish species generated from tissue samples have been added to Genbank (NCBI Accession no. KX929879-KX929923).

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