Ecosystems monitoring powered by environmental genomics: A review of current strategies with an implementation roadmap

A decade after environmental scientists integrated high‐throughput sequencing technologies in their toolbox, the genomics‐based monitoring of anthropogenic impacts on the biodiversity and functioning of ecosystems is yet to be implemented by regulatory frameworks. Despite the broadly acknowledged po...

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Vydáno v:	Molecular ecology Ročník 30; číslo 13; s. 2937 - 2958
Hlavní autoři:	Cordier, Tristan, Alonso‐Sáez, Laura, Apothéloz‐Perret‐Gentil, Laure, Aylagas, Eva, Bohan, David A., Bouchez, Agnès, Chariton, Anthony, Creer, Simon, Frühe, Larissa, Keck, François, Keeley, Nigel, Laroche, Olivier, Leese, Florian, Pochon, Xavier, Stoeck, Thorsten, Pawlowski, Jan, Lanzén, Anders
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	England Blackwell Publishing Ltd 01.07.2021 Wiley John Wiley and Sons Inc
Témata:	Anthropogenic factors Biodiversity Bioindicators Biomonitoring Ecological monitoring ecosystem management Ecosystems environmental DNA environmental monitoring Environmental Sciences fauna Genomics Human influences implementation strategy Indicator species Meiofauna metabarcoding Metagenomics Microorganisms NOVEL APPROACHES TO MONITOR ECOSYSTEMS Special Issue species identification Taxonomy transcriptomics implementation strategy metabarcoding biodiversity biomonitoring ecosystem management environmental DNA Biomonitoring
ISSN:	0962-1083, 1365-294X, 1365-294X
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Abstract	A decade after environmental scientists integrated high‐throughput sequencing technologies in their toolbox, the genomics‐based monitoring of anthropogenic impacts on the biodiversity and functioning of ecosystems is yet to be implemented by regulatory frameworks. Despite the broadly acknowledged potential of environmental genomics to this end, technical limitations and conceptual issues still stand in the way of its broad application by end‐users. In addition, the multiplicity of potential implementation strategies may contribute to a perception that the routine application of this methodology is premature or “in development”, hence restraining regulators from binding these tools into legal frameworks. Here, we review recent implementations of environmental genomics‐based methods, applied to the biomonitoring of ecosystems. By taking a general overview, without narrowing our perspective to particular habitats or groups of organisms, this paper aims to compare, review and discuss the strengths and limitations of four general implementation strategies of environmental genomics for monitoring: (a) Taxonomy‐based analyses focused on identification of known bioindicators or described taxa; (b) De novo bioindicator analyses; (c) Structural community metrics including inferred ecological networks; and (d) Functional community metrics (metagenomics or metatranscriptomics). We emphasise the utility of the three latter strategies to integrate meiofauna and microorganisms that are not traditionally utilised in biomonitoring because of difficult taxonomic identification. Finally, we propose a roadmap for the implementation of environmental genomics into routine monitoring programmes that leverage recent analytical advancements, while pointing out current limitations and future research needs.
AbstractList	A decade after environmental scientists integrated high-throughput sequencing technologies in their toolbox, the genomics-based monitoring of anthropogenic impacts on the biodiversity and functioning of ecosystems is yet to be implemented by regulatory frameworks. Despite the broadly acknowledged potential of environmental genomics to this end, technical limitations and conceptual issues still stand in the way of its broad application by end-users. In addition, the multiplicity of potential implementation strategies may contribute to a perception that the routine application of this methodology is premature or "in development", hence restraining regulators from binding these tools into legal frameworks. Here, we review recent implementations of environmental genomics-based methods, applied to the biomonitoring of ecosystems. By taking a general overview, without narrowing our perspective to particular habitats or groups of organisms, this paper aims to compare, review and discuss the strengths and limitations of four general implementation strategies of environmental genomics for monitoring: (a) Taxonomy-based analyses focused on identification of known bioindicators or described taxa; (b) De novo bioindicator analyses; (c) Structural community metrics including inferred ecological networks; and (d) Functional community metrics (metagenomics or metatranscriptomics). We emphasise the utility of the three latter strategies to integrate meiofauna and microorganisms that are not traditionally utilised in biomonitoring because of difficult taxonomic identification. Finally, we propose a roadmap for the implementation of environmental genomics into routine monitoring programmes that leverage recent analytical advancements, while pointing out current limitations and future research needs.A decade after environmental scientists integrated high-throughput sequencing technologies in their toolbox, the genomics-based monitoring of anthropogenic impacts on the biodiversity and functioning of ecosystems is yet to be implemented by regulatory frameworks. Despite the broadly acknowledged potential of environmental genomics to this end, technical limitations and conceptual issues still stand in the way of its broad application by end-users. In addition, the multiplicity of potential implementation strategies may contribute to a perception that the routine application of this methodology is premature or "in development", hence restraining regulators from binding these tools into legal frameworks. Here, we review recent implementations of environmental genomics-based methods, applied to the biomonitoring of ecosystems. By taking a general overview, without narrowing our perspective to particular habitats or groups of organisms, this paper aims to compare, review and discuss the strengths and limitations of four general implementation strategies of environmental genomics for monitoring: (a) Taxonomy-based analyses focused on identification of known bioindicators or described taxa; (b) De novo bioindicator analyses; (c) Structural community metrics including inferred ecological networks; and (d) Functional community metrics (metagenomics or metatranscriptomics). We emphasise the utility of the three latter strategies to integrate meiofauna and microorganisms that are not traditionally utilised in biomonitoring because of difficult taxonomic identification. Finally, we propose a roadmap for the implementation of environmental genomics into routine monitoring programmes that leverage recent analytical advancements, while pointing out current limitations and future research needs. A decade after environmental scientists integrated high‐throughput sequencing technologies in their toolbox, the genomics‐based monitoring of anthropogenic impacts on the biodiversity and functioning of ecosystems is yet to be implemented by regulatory frameworks. Despite the broadly acknowledged potential of environmental genomics to this end, technical limitations and conceptual issues still stand in the way of its broad application by end‐users. In addition, the multiplicity of potential implementation strategies may contribute to a perception that the routine application of this methodology is premature or “in development”, hence restraining regulators from binding these tools into legal frameworks. Here, we review recent implementations of environmental genomics‐based methods, applied to the biomonitoring of ecosystems. By taking a general overview, without narrowing our perspective to particular habitats or groups of organisms, this paper aims to compare, review and discuss the strengths and limitations of four general implementation strategies of environmental genomics for monitoring: (a) Taxonomy‐based analyses focused on identification of known bioindicators or described taxa; (b) De novo bioindicator analyses; (c) Structural community metrics including inferred ecological networks; and (d) Functional community metrics (metagenomics or metatranscriptomics). We emphasise the utility of the three latter strategies to integrate meiofauna and microorganisms that are not traditionally utilised in biomonitoring because of difficult taxonomic identification. Finally, we propose a roadmap for the implementation of environmental genomics into routine monitoring programmes that leverage recent analytical advancements, while pointing out current limitations and future research needs. A decade after environmental scientists integrated high-throughput sequencing technologies in their toolbox, the genomics-based monitoring of anthropogenic impacts on the biodiversity and functioning of ecosystems is yet to be implemented by regulatory frameworks. Despite the broadly acknowledged potential of environmental genomics to this end, technical limitations and conceptual issues still stand in the way of its broad application by end-users. In addition, the multiplicity of potential implementation strategies may contribute to a perception that the routine application of this methodology is premature or "in development", hence restraining regulators from binding these tools into legal frameworks. Here, we review recent implementations of environmental genomics-based methods, applied to the biomonitoring of ecosystems. By taking a general overview, without narrowing our perspective to particular habitats or groups of organisms, this paper aims to compare, review and discuss the strengths and limitations of four general implementation strategies of environmental genomics for monitoring: (A) Taxonomy-based analyses focused on identification of known bioindicators or described taxa; (B) De novo bioindicator analyses; (C) Structural community metrics including inferred ecological networks; and (D) Functional community metrics (metagenomics or metatranscriptomics). We emphasise the utility of the three latter strategies to integrate meiofauna and microorganisms that are not traditionally utilised in biomonitoring because of difficult taxonomic identification. Finally, we propose a roadmap for the implementation of environmental genomics into routine monitoring programs that leverage recent analytical advancements, while pointing out current limitations and future research needs.
Author	Bohan, David A. Cordier, Tristan Apothéloz‐Perret‐Gentil, Laure Bouchez, Agnès Frühe, Larissa Keeley, Nigel Pochon, Xavier Stoeck, Thorsten Alonso‐Sáez, Laura Laroche, Olivier Leese, Florian Pawlowski, Jan Creer, Simon Aylagas, Eva Keck, François Lanzén, Anders Chariton, Anthony
AuthorAffiliation	5 UMR CARRTEL, INRA USMB Thonon-les-Bains France 2 AZTI Marine Research Basque Research and Technology Alliance (BRTA) Spain 14 ID‐Gene Ecodiagnostics Geneva Switzerland 10 Aquatic Ecosystem Research Faculty of Biology University of Duisburg‐Essen Essen Germany 11 Centre for Water and Environmental Research (ZWU) University of Duisburg‐Essen Essen Germany 4 Agroécologie INRAE University of Bourgogne University Bourgogne Franche‐Comté Dijon France 9 Benthic Resources and Processes Group Institute of Marine Research Tromsø Norway 1 Department of Genetics and Evolution Science III University of Geneva Geneva Switzerland 16 Basque Foundation for Science IKERBASQUE Bilbao Spain 12 Coastal & Freshwater Group Cawthron Institute Nelson New Zealand 13 Institute of Marine Science University of Auckland Warkworth New Zealand 8 Department of Ecology Technische Universität Kaiserslautern Kaiserslautern Germany 15 Institute of Oceanology Polish Academy of Sciences Sopot Poland 6 Department of Biological Sciences
AuthorAffiliation_xml	– name: 6 Department of Biological Sciences Macquarie University Sydney NSW Australia – name: 15 Institute of Oceanology Polish Academy of Sciences Sopot Poland – name: 16 Basque Foundation for Science IKERBASQUE Bilbao Spain – name: 8 Department of Ecology Technische Universität Kaiserslautern Kaiserslautern Germany – name: 12 Coastal & Freshwater Group Cawthron Institute Nelson New Zealand – name: 2 AZTI Marine Research Basque Research and Technology Alliance (BRTA) Spain – name: 9 Benthic Resources and Processes Group Institute of Marine Research Tromsø Norway – name: 5 UMR CARRTEL, INRA USMB Thonon-les-Bains France – name: 7 School of Natural Sciences Bangor University Gwynedd UK – name: 13 Institute of Marine Science University of Auckland Warkworth New Zealand – name: 14 ID‐Gene Ecodiagnostics Geneva Switzerland – name: 3 Red Sea Research Center (RSRC) Biological and Environmental Sciences and Engineering (BESE) King Abdullah University of Science and Technology (KAUST) Thuwal Saudi Arabia – name: 11 Centre for Water and Environmental Research (ZWU) University of Duisburg‐Essen Essen Germany – name: 4 Agroécologie INRAE University of Bourgogne University Bourgogne Franche‐Comté Dijon France – name: 1 Department of Genetics and Evolution Science III University of Geneva Geneva Switzerland – name: 10 Aquatic Ecosystem Research Faculty of Biology University of Duisburg‐Essen Essen Germany
Author_xml	– sequence: 1 givenname: Tristan orcidid: 0000-0001-7398-4790 surname: Cordier fullname: Cordier, Tristan email: tristan.cordier@gmail.com organization: University of Geneva – sequence: 2 givenname: Laura surname: Alonso‐Sáez fullname: Alonso‐Sáez, Laura organization: Basque Research and Technology Alliance (BRTA) – sequence: 3 givenname: Laure orcidid: 0000-0002-8592-3079 surname: Apothéloz‐Perret‐Gentil fullname: Apothéloz‐Perret‐Gentil, Laure organization: University of Geneva – sequence: 4 givenname: Eva orcidid: 0000-0001-9792-8451 surname: Aylagas fullname: Aylagas, Eva organization: King Abdullah University of Science and Technology (KAUST) – sequence: 5 givenname: David A. surname: Bohan fullname: Bohan, David A. organization: University Bourgogne Franche‐Comté – sequence: 6 givenname: Agnès surname: Bouchez fullname: Bouchez, Agnès organization: USMB – sequence: 7 givenname: Anthony orcidid: 0000-0002-5809-3372 surname: Chariton fullname: Chariton, Anthony organization: Macquarie University – sequence: 8 givenname: Simon surname: Creer fullname: Creer, Simon organization: Bangor University – sequence: 9 givenname: Larissa surname: Frühe fullname: Frühe, Larissa organization: Technische Universität Kaiserslautern – sequence: 10 givenname: François orcidid: 0000-0002-3323-4167 surname: Keck fullname: Keck, François organization: USMB – sequence: 11 givenname: Nigel surname: Keeley fullname: Keeley, Nigel organization: Institute of Marine Research – sequence: 12 givenname: Olivier surname: Laroche fullname: Laroche, Olivier organization: Institute of Marine Research – sequence: 13 givenname: Florian orcidid: 0000-0002-5465-913X surname: Leese fullname: Leese, Florian organization: University of Duisburg‐Essen – sequence: 14 givenname: Xavier surname: Pochon fullname: Pochon, Xavier organization: University of Auckland – sequence: 15 givenname: Thorsten orcidid: 0000-0001-5180-5659 surname: Stoeck fullname: Stoeck, Thorsten organization: Technische Universität Kaiserslautern – sequence: 16 givenname: Jan surname: Pawlowski fullname: Pawlowski, Jan organization: Polish Academy of Sciences – sequence: 17 givenname: Anders orcidid: 0000-0002-7138-6364 surname: Lanzén fullname: Lanzén, Anders organization: IKERBASQUE
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/32416615$$D View this record in MEDLINE/PubMed https://hal.inrae.fr/hal-02860583$$DView record in HAL
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SubjectTerms	Anthropogenic factors Biodiversity Bioindicators Biomonitoring Ecological monitoring ecosystem management Ecosystems environmental DNA environmental monitoring Environmental Sciences fauna Genomics Human influences implementation strategy Indicator species Meiofauna metabarcoding Metagenomics Microorganisms NOVEL APPROACHES TO MONITOR ECOSYSTEMS Special Issue species identification Taxonomy transcriptomics
Title	Ecosystems monitoring powered by environmental genomics: A review of current strategies with an implementation roadmap
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