MIBiG 3.0: a community-driven effort to annotate experimentally validated biosynthetic gene clusters

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Abstract

With an ever-increasing amount of (meta)genomic data being deposited in sequence databases, (meta)genome mining for natural product biosynthetic pathways occupies a critical role in the discovery of novel pharmaceutical drugs, crop protection agents and biomaterials. The genes that encode these pathways are often organised into biosynthetic gene clusters (BGCs). In 2015, we defined the Minimum Information about a Biosynthetic Gene cluster (MIBiG): a standardised data format that describes the minimally required information to uniquely characterise a BGC. We simultaneously constructed an accompanying online database of BGCs, which has since been widely used by the community as a reference dataset for BGCs and was expanded to 2021 entries in 2019 (MIBiG 2.0). Here, we describe MIBiG 3.0, a database update comprising large-scale validation and re-annotation of existing entries and 661 new entries. Particular attention was paid to the annotation of compound structures and biological activities, as well as protein domain selectivities. Together, these new features keep the database up-to-date, and will provide new opportunities for the scientific community to use its freely available data, e.g. for the training of new machine learning models to predict sequence-structure-function relationships for diverse natural products. MIBiG 3.0 is accessible online at https://mibig.secondarymetabolites.org/.

Graphical Abstract

MIBiG version 3.0 provides an updated database of experimentally characterized biosynthetic gene clusters. It includes 661 new entries, as well as new structures, bioactivities and enzyme domain substrate specificities.

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Author and article information

Contributors

Barbara R Terlouw:

ORCID: https://orcid.org/0000-0002-4058-6718

Kai Blin:

ORCID: https://orcid.org/0000-0003-3764-6051

Jorge C Navarro-Muñoz:

ORCID: https://orcid.org/0000-0003-2992-1607

Nicole E Avalon:

ORCID: https://orcid.org/0000-0003-3588-892X

Marc G Chevrette:

ORCID: https://orcid.org/0000-0002-7209-0717

Susan Egbert:

ORCID: https://orcid.org/0000-0001-5458-1099

Sanghoon Lee:

ORCID: https://orcid.org/0000-0002-1377-3913

David Meijer:

ORCID: https://orcid.org/0000-0001-6406-4394

Michael J J Recchia:

ORCID: https://orcid.org/0000-0002-1450-0941

Zachary L Reitz:

ORCID: https://orcid.org/0000-0003-1964-8221

Jeffrey A van Santen:

ORCID: https://orcid.org/0000-0002-5424-804X

Nelly Selem-Mojica:

ORCID: https://orcid.org/0000-0003-1697-3862

Thomas Tørring:

ORCID: https://orcid.org/0000-0001-5257-2121

Liana Zaroubi:

ORCID: https://orcid.org/0000-0001-8218-7216

Mohammad Alanjary:

ORCID: https://orcid.org/0000-0001-8420-1325

Gajender Aleti:

ORCID: https://orcid.org/0000-0002-1867-9758

César Aguilar:

ORCID: https://orcid.org/0000-0001-7044-2419

Suhad A A Al-Salihi:

ORCID: https://orcid.org/0000-0001-7665-7904

Hannah E Augustijn:

ORCID: https://orcid.org/0000-0002-1862-6699

J Abraham Avelar-Rivas

Luis A Avitia-Domínguez:

ORCID: https://orcid.org/0000-0002-5902-2410

Francisco Barona-Gómez:

ORCID: https://orcid.org/0000-0003-1492-9497

Jordan Bernaldo-Agüero:

ORCID: https://orcid.org/0000-0002-7753-5527

Vincent A Bielinski:

ORCID: https://orcid.org/0000-0002-8107-8752

Friederike Biermann:

ORCID: https://orcid.org/0000-0002-9152-2562

Thomas J Booth:

ORCID: https://orcid.org/0000-0002-6134-1488

Victor J Carrion Bravo:

ORCID: https://orcid.org/0000-0002-4093-0355

Raquel Castelo-Branco

Fernanda O Chagas:

ORCID: https://orcid.org/0000-0001-9534-3521

Pablo Cruz-Morales:

ORCID: https://orcid.org/0000-0002-6751-8897

Chao Du:

ORCID: https://orcid.org/0000-0003-3447-5293

Katherine R Duncan:

ORCID: https://orcid.org/0000-0002-3670-4849

Athina Gavriilidou:

ORCID: https://orcid.org/0000-0002-6805-3868

Damien Gayrard:

ORCID: https://orcid.org/0000-0002-1447-9548

Karina Gutiérrez-García:

ORCID: https://orcid.org/0000-0002-6077-7490

Kristina Haslinger:

ORCID: https://orcid.org/0000-0003-1361-1508

Eric J N Helfrich:

ORCID: https://orcid.org/0000-0001-8751-3279

Justin J J van der Hooft:

ORCID: https://orcid.org/0000-0002-9340-5511

Afif P Jati:

ORCID: https://orcid.org/0000-0002-3147-6293

Edward Kalkreuter:

ORCID: https://orcid.org/0000-0002-8241-4455

Nikolaos Kalyvas:

ORCID: https://orcid.org/0000-0002-5676-1859

Kyo Bin Kang:

ORCID: https://orcid.org/0000-0003-3290-1017

Satria Kautsar:

ORCID: https://orcid.org/0000-0002-9815-511X

Wonyong Kim:

ORCID: https://orcid.org/0000-0002-9094-8908

Aditya M Kunjapur:

ORCID: https://orcid.org/0000-0001-6869-9530

Yong-Xin Li:

ORCID: https://orcid.org/0000-0003-4422-2302

Geng-Min Lin:

ORCID: https://orcid.org/0000-0001-8123-0921

Catarina Loureiro:

ORCID: https://orcid.org/0000-0002-6258-2080

Joris J R Louwen:

ORCID: https://orcid.org/0000-0003-4887-9109

Nico L L Louwen:

ORCID: https://orcid.org/0000-0002-4431-5499

George Lund:

ORCID: https://orcid.org/0000-0001-9099-3461

Jonathan Parra:

ORCID: https://orcid.org/0000-0001-7273-0406

Benjamin Philmus:

ORCID: https://orcid.org/0000-0003-2085-0873

Bita Pourmohsenin:

ORCID: https://orcid.org/0000-0002-5754-7221

Lotte J U Pronk:

ORCID: https://orcid.org/0000-0002-3083-954X

Adriana Rego:

ORCID: https://orcid.org/0000-0001-9647-1197

Devasahayam Arokia Balaya Rex:

ORCID: https://orcid.org/0000-0002-9556-3150

Serina Robinson:

ORCID: https://orcid.org/0000-0001-6947-7913

L Rodrigo Rosas-Becerra:

ORCID: https://orcid.org/0000-0002-4105-1563

Eve T Roxborough:

ORCID: https://orcid.org/0000-0002-4573-1670

Michelle A Schorn:

ORCID: https://orcid.org/0000-0001-8144-6052

Darren J Scobie:

ORCID: https://orcid.org/0000-0002-9858-9444

Kumar Saurabh Singh:

ORCID: https://orcid.org/0000-0001-8352-5897

Nika Sokolova:

ORCID: https://orcid.org/0000-0003-4129-2890

Xiaoyu Tang:

ORCID: https://orcid.org/0000-0002-7855-5984

Daniel Udwary:

ORCID: https://orcid.org/0000-0002-3491-0198

Aruna Vigneshwari:

ORCID: https://orcid.org/0000-0002-8131-1518

Kristiina Vind:

ORCID: https://orcid.org/0000-0001-6307-1461

Sophie P J M Vromans:

ORCID: https://orcid.org/0000-0002-7482-5721

Valentin Waschulin:

ORCID: https://orcid.org/0000-0002-8905-1263

Sam E Williams:

ORCID: https://orcid.org/0000-0002-6949-426X

Jaclyn M Winter:

ORCID: https://orcid.org/0000-0001-6273-5377

Thomas E Witte:

ORCID: https://orcid.org/0000-0002-6385-3655

Huali Xie:

ORCID: https://orcid.org/0000-0002-6581-9573

Dong Yang:

ORCID: https://orcid.org/0000-0003-2917-0663

Jingwei Yu:

ORCID: https://orcid.org/0000-0003-4268-436X

Mitja Zdouc:

ORCID: https://orcid.org/0000-0001-6534-6609

Zheng Zhong:

ORCID: https://orcid.org/0000-0002-1262-4115

Jérôme Collemare:

ORCID: https://orcid.org/0000-0001-8152-6642

Roger G Linington:

ORCID: https://orcid.org/0000-0003-1818-4971

Tilmann Weber:

ORCID: https://orcid.org/0000-0002-8260-5120

Marnix H Medema:

ORCID: https://orcid.org/0000-0002-2191-2821

Journal

Journal ID (nlm-ta): Nucleic Acids Res

Journal ID (iso-abbrev): Nucleic Acids Res

Journal ID (publisher-id): nar

Title: Nucleic Acids Research

Publisher: Oxford University Press

ISSN (Print): 0305-1048

ISSN (Electronic): 1362-4962

Publication date Collection: 06 January 2023

Publication date (Electronic): 18 November 2022

Publication date PMC-release: 18 November 2022

Volume: 51

Issue: D1

Pages: D603-D610

Affiliations

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark , Kgs. Lyngby, Denmark

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Westerdijk Fungal Biodiversity Institute , Uppsalalaan 8, 3584 CT Utrecht, The Netherlands

Scripps Institution of Oceanography, University of California San Diego , 9500 Gilman Drive, La Jolla, CA 92093-0212, USA

Department of Microbiology and Cell Science, University of Florida , Gainesville, FL 32611, USA

Department of Chemistry, University of Manitoba , 66 Chancellors Cir, Winnipeg, MB R3T 2N2, Canada

Department of Chemistry, Simon Fraser University, 8888 University Drive , Burnaby, British Columbia V5A 1S6, Canada

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Department of Chemistry, Simon Fraser University, 8888 University Drive , Burnaby, British Columbia V5A 1S6, Canada

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Department of Chemistry, Simon Fraser University, 8888 University Drive , Burnaby, British Columbia V5A 1S6, Canada

Unnatural Products , 2161 Delaware Ave. Suite A, Santa Cruz, CA 95060, USA

Centro de Ciencias Matemáticas UNAM , Morelia, México

Department of Biological and Chemical Engineering, Aarhus University , Denmark

Department of Chemistry, Simon Fraser University, 8888 University Drive , Burnaby, British Columbia V5A 1S6, Canada

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Food and Animal Sciences, Department of Agricultural and Environmental Sciences, Tennessee State University , Nashville, TN 37209, USA

Department of Chemistry, Purdue University , West Lafayette, IN, USA

Department of Applied Sciences, University of Technology , Iraq

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Institute of Biology, Leiden University , Sylviusweg 72, 2333BE Leiden, The Netherlands

Laboratorio Nacional de Genómica para la Biodiversidad-Unidad de Genómica Avanzada , Cinvestav. Km 9.6 Libramiento Norte Carretera Irapuato-León, CP 36824 Irapuato, Gto., México

Institute of Biology, Leiden University , Sylviusweg 72, 2333BE Leiden, The Netherlands

Laboratorio Nacional de Genómica para la Biodiversidad-Unidad de Genómica Avanzada , Cinvestav. Km 9.6 Libramiento Norte Carretera Irapuato-León, CP 36824 Irapuato, Gto., México

Institute of Biology, Leiden University , Sylviusweg 72, 2333BE Leiden, The Netherlands

Laboratorio Nacional de Genómica para la Biodiversidad-Unidad de Genómica Avanzada , Cinvestav. Km 9.6 Libramiento Norte Carretera Irapuato-León, CP 36824 Irapuato, Gto., México

Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México , Cuernavaca, Morelos, México

Synthetic Biology and Bioenergy Group, J. Craig Venter Institute , La Jolla, CA 92037, USA

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Institute of Molecular Bio Science, Goethe-University Frankfurt , D-60438 Frankfurt am Main, Germany

LOEWE Center for Translational Biodiversity Genomics (TBG) , Senckenberganlage 25, 60325 Frankfurt am Main, Germany

The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark , Kgs. Lyngby, Denmark

School of Molecular Sciences, University of Western Australia , Perth, Australia

Institute of Biology, Leiden University , Sylviusweg 72, 2333BE Leiden, The Netherlands

Departamento de Microbiología, Instituto de Hortofruticultura Subtropical y Mediterránea ‘La Mayora’, Universidad de Málaga-Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Universidad de Málaga , Málaga, Spain

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW) , Wageningen, The Netherlands

Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto , Portugal

Faculty of Sciences, University of Porto , 4150-179 Porto, Portugal

Instituto de Pesquisas de Produtos Naturais Walter Mors, Universidade Federal do Rio de Janeiro , Rio de Janeiro, RJ, 21941-599, Brazil

The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark , Kgs. Lyngby, Denmark

Institute of Biology, Leiden University , Sylviusweg 72, 2333BE Leiden, The Netherlands

University of Strathclyde, Strathclyde Institute of Pharmacy and Biomedical Sciences , 141 Cathedral Street, Glasgow, G4 ORE UK

Translational Genome Mining for Natural Products, Interfaculty Institute of Microbiology and Infection Medicine Tübingen (IMIT), University of Tübingen , Tübingen, Germany

Interfaculty Institute for Biomedical Informatics (IBMI), University of Tübingen , Tübingen, Germany

Department of Molecular Microbiology , John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK

Department of Embryology, Carnegie Institution for Science , 3520 San Martin Drive, Baltimore, MD 21218, USA

Department of Chemical and Pharmaceutical Biology, Groningen Research Institute of Pharmacy, University of Groningen , Antonius Deusinglaan 1, 9713 AV Groningen, The Netherlands

Institute of Molecular Bio Science, Goethe-University Frankfurt , D-60438 Frankfurt am Main, Germany

LOEWE Center for Translational Biodiversity Genomics (TBG) , Senckenberganlage 25, 60325 Frankfurt am Main, Germany

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Department of Biochemistry, University of Johannesburg , Auckland Park, Johannesburg 2006, South Africa

Indonesian Society of Bioinformatics And Biodiversity , Indonesia

Department of Chemistry, University of Florida Scripps Biomedical Research , 110 Scripps Way, Jupiter, FL 33458, USA

Westerdijk Fungal Biodiversity Institute , Uppsalalaan 8, 3584 CT Utrecht, The Netherlands

College of Pharmacy, Sookmyung Women's University , Seoul, South Korea

Department of Chemistry, University of Florida Scripps Biomedical Research , 110 Scripps Way, Jupiter, FL 33458, USA

Korean Lichen Research Institute, Sunchon National Universtiy , Suncheon, South Korea

Department of Chemical & Biomolecular Engineering, University of Delaware , Newark, DE 19716, USA

Department of Chemistry, The University of Hong Kong , Pokfulam Road, Hong Kong, P.R. China

Department of Biological Engineering, Massachusetts Institute of Technology , Cambridge, MA, USA

Laboratory of Microbiology, Wageningen University , Stippeneng 4, 6708WE, Wageningen, The Netherlands

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Sustainable Soils and Crops, Rothamsted Research , Harpenden, Hertfordshire, UK

Instituto de Investigaciones Farmacéuticas (INIFAR), Facultad de Farmacia, Universidad de Costa Rica , San José, 11501-2060, Costa Rica

Centro de Investigaciones en Productos Naturales (CIPRONA), Universidad de Costa Rica , San José, 11501-2060, Costa Rica

Centro Nacional de Innovaciones Biotecnológicas (CENIBiot) , CeNAT-CONARE, 1174-1200, San José, Costa Rica

Department of Pharmaceutical Sciences, Oregon State University , USA

Translational Genome Mining for Natural Products, Interfaculty Institute of Microbiology and Infection Medicine Tübingen (IMIT), University of Tübingen , Tübingen, Germany

Interfaculty Institute for Biomedical Informatics (IBMI), University of Tübingen , Tübingen, Germany

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto , Portugal

Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto , Portugal

Centre for Integrative Omics Data Science, Yenepoya (Deemed to be University) , Mangalore 575018, India

Department of Environmental Microbiology, Eawag: Swiss Federal Institute for Aquatic Science and Technology , Überlandstrasse 133, CH-8600 Dübendorf, Switzerland

Institute of Biology, Leiden University , Sylviusweg 72, 2333BE Leiden, The Netherlands

Laboratorio Nacional de Genómica para la Biodiversidad-Unidad de Genómica Avanzada , Cinvestav. Km 9.6 Libramiento Norte Carretera Irapuato-León, CP 36824 Irapuato, Gto., México

School of Chemistry, University of Nottingham, University Park , Nottingham NG7 2RD, UK

Laboratory of Microbiology, Wageningen University , Stippeneng 4, 6708WE, Wageningen, The Netherlands

University of Strathclyde, Strathclyde Institute of Pharmacy and Biomedical Sciences , 141 Cathedral Street, Glasgow, G4 ORE UK

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Department of Chemical and Pharmaceutical Biology, Groningen Research Institute of Pharmacy, University of Groningen , Antonius Deusinglaan 1, 9713 AV Groningen, The Netherlands

Institute of Chemical Biology, Shenzhen Bay Laboratory , Shenzhen 518132, China

DOE Joint Genome Institute , Lawrence Berkeley National Lab, Berkeley, CA, USA

Department of Microbiology, University of Szeged , Hungary

Host-Microbe Interactomics Group, Wageningen University , 6708 WD Wageningen, The Netherlands

NAICONS Srl , 20139 Milan, Italy

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

School of Life Sciences, The University of Warwick , Coventry CV4 7AL, UK

School of Biochemistry, University of Bristol, University Walk , Bristol BS8 1TD, UK

Department of Medicinal Chemistry, University of Utah , Salt Lake City, UT 84112, USA

Department of Chemistry and Biomolecular Sciences, University of Ottawa , Ottawa, Canada

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Key laboratory of Detection for Biotoxins, Ministry of Agriculture and Rural Affairs and Oil Crops Research Institute, Chinese Academy of Agricultural Sciences , Wuhan 430061, China

Department of Chemistry and Natural Products Discovery Center, UF Scripps Biomedical Research, University of Florida , Jupiter, FL 33458, USA

SUSTech-PKU Institute of Plant and Food Science, Department of Biology, School of Life Sciences, Southern University of Science and Technology , Shenzhen, Guangdong 518055, China

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Laboratory of Microbiology, Wageningen University , Stippeneng 4, 6708WE, Wageningen, The Netherlands

Westerdijk Fungal Biodiversity Institute , Uppsalalaan 8, 3584 CT Utrecht, The Netherlands

Department of Chemistry, Simon Fraser University, 8888 University Drive , Burnaby, British Columbia V5A 1S6, Canada

The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark , Kgs. Lyngby, Denmark

Bioinformatics Group, Wageningen University , Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

Institute of Biology, Leiden University , Sylviusweg 72, 2333BE Leiden, The Netherlands

Author notes

To whom correspondence should be addressed. Tel: +31 317484706; Email: marnix.medema@ 123456wur.nl

Correspondence may also be addressed to Tilmann Weber. Tel: +45 24896132; Email: tiwe@ 123456biosustain.dtu.dk

The authors wish it to be known that, in their opinion, the first two authors should be regarded as Joint First Authors.

Author information

Barbara R Terlouw https://orcid.org/0000-0002-4058-6718

Kai Blin https://orcid.org/0000-0003-3764-6051

Jorge C Navarro-Muñoz https://orcid.org/0000-0003-2992-1607

Nicole E Avalon https://orcid.org/0000-0003-3588-892X

Marc G Chevrette https://orcid.org/0000-0002-7209-0717

Susan Egbert https://orcid.org/0000-0001-5458-1099

Sanghoon Lee https://orcid.org/0000-0002-1377-3913

David Meijer https://orcid.org/0000-0001-6406-4394

Michael J J Recchia https://orcid.org/0000-0002-1450-0941

Zachary L Reitz https://orcid.org/0000-0003-1964-8221

Jeffrey A van Santen https://orcid.org/0000-0002-5424-804X

Nelly Selem-Mojica https://orcid.org/0000-0003-1697-3862

Thomas Tørring https://orcid.org/0000-0001-5257-2121

Liana Zaroubi https://orcid.org/0000-0001-8218-7216

Mohammad Alanjary https://orcid.org/0000-0001-8420-1325

Gajender Aleti https://orcid.org/0000-0002-1867-9758

César Aguilar https://orcid.org/0000-0001-7044-2419

Suhad A A Al-Salihi https://orcid.org/0000-0001-7665-7904

Hannah E Augustijn https://orcid.org/0000-0002-1862-6699

Luis A Avitia-Domínguez https://orcid.org/0000-0002-5902-2410

Francisco Barona-Gómez https://orcid.org/0000-0003-1492-9497

Jordan Bernaldo-Agüero https://orcid.org/0000-0002-7753-5527

Vincent A Bielinski https://orcid.org/0000-0002-8107-8752

Friederike Biermann https://orcid.org/0000-0002-9152-2562

Thomas J Booth https://orcid.org/0000-0002-6134-1488

Victor J Carrion Bravo https://orcid.org/0000-0002-4093-0355

Fernanda O Chagas https://orcid.org/0000-0001-9534-3521

Pablo Cruz-Morales https://orcid.org/0000-0002-6751-8897

Chao Du https://orcid.org/0000-0003-3447-5293

Katherine R Duncan https://orcid.org/0000-0002-3670-4849

Athina Gavriilidou https://orcid.org/0000-0002-6805-3868

Damien Gayrard https://orcid.org/0000-0002-1447-9548

Karina Gutiérrez-García https://orcid.org/0000-0002-6077-7490

Kristina Haslinger https://orcid.org/0000-0003-1361-1508

Eric J N Helfrich https://orcid.org/0000-0001-8751-3279

Justin J J van der Hooft https://orcid.org/0000-0002-9340-5511

Afif P Jati https://orcid.org/0000-0002-3147-6293

Edward Kalkreuter https://orcid.org/0000-0002-8241-4455

Nikolaos Kalyvas https://orcid.org/0000-0002-5676-1859

Kyo Bin Kang https://orcid.org/0000-0003-3290-1017

Satria Kautsar https://orcid.org/0000-0002-9815-511X

Wonyong Kim https://orcid.org/0000-0002-9094-8908

Aditya M Kunjapur https://orcid.org/0000-0001-6869-9530

Yong-Xin Li https://orcid.org/0000-0003-4422-2302

Geng-Min Lin https://orcid.org/0000-0001-8123-0921

Catarina Loureiro https://orcid.org/0000-0002-6258-2080

Joris J R Louwen https://orcid.org/0000-0003-4887-9109

Nico L L Louwen https://orcid.org/0000-0002-4431-5499

George Lund https://orcid.org/0000-0001-9099-3461

Jonathan Parra https://orcid.org/0000-0001-7273-0406

Benjamin Philmus https://orcid.org/0000-0003-2085-0873

Bita Pourmohsenin https://orcid.org/0000-0002-5754-7221

Lotte J U Pronk https://orcid.org/0000-0002-3083-954X

Adriana Rego https://orcid.org/0000-0001-9647-1197

Devasahayam Arokia Balaya Rex https://orcid.org/0000-0002-9556-3150

Serina Robinson https://orcid.org/0000-0001-6947-7913

L Rodrigo Rosas-Becerra https://orcid.org/0000-0002-4105-1563

Eve T Roxborough https://orcid.org/0000-0002-4573-1670

Michelle A Schorn https://orcid.org/0000-0001-8144-6052

Darren J Scobie https://orcid.org/0000-0002-9858-9444

Kumar Saurabh Singh https://orcid.org/0000-0001-8352-5897

Nika Sokolova https://orcid.org/0000-0003-4129-2890

Xiaoyu Tang https://orcid.org/0000-0002-7855-5984

Daniel Udwary https://orcid.org/0000-0002-3491-0198

Aruna Vigneshwari https://orcid.org/0000-0002-8131-1518

Kristiina Vind https://orcid.org/0000-0001-6307-1461

Sophie P J M Vromans https://orcid.org/0000-0002-7482-5721

Valentin Waschulin https://orcid.org/0000-0002-8905-1263

Sam E Williams https://orcid.org/0000-0002-6949-426X

Jaclyn M Winter https://orcid.org/0000-0001-6273-5377

Thomas E Witte https://orcid.org/0000-0002-6385-3655

Huali Xie https://orcid.org/0000-0002-6581-9573

Dong Yang https://orcid.org/0000-0003-2917-0663

Jingwei Yu https://orcid.org/0000-0003-4268-436X

Mitja Zdouc https://orcid.org/0000-0001-6534-6609

Zheng Zhong https://orcid.org/0000-0002-1262-4115

Jérôme Collemare https://orcid.org/0000-0001-8152-6642

Roger G Linington https://orcid.org/0000-0003-1818-4971

Tilmann Weber https://orcid.org/0000-0002-8260-5120

Marnix H Medema https://orcid.org/0000-0002-2191-2821

Article

Publisher ID: gkac1049

DOI: 10.1093/nar/gkac1049

PMC ID: 9825592

PubMed ID: 36399496

SO-VID: 9d2e59a2-748d-4151-aaae-f3343c8008c9

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date accepted : 21 October 2022

Date revision received : 07 October 2022

Date received : 15 September 2022

Page count

Pages: 8

Funding

Funded by: ERC Starting;

Award ID: 948770-DECIPHER

Funded by: Novo Nordisk Foundation, DOI 10.13039/501100009708;

Award ID: NNF20CC0035580

Award ID: NNF16OC0021746

Funded by: Danish National Research Foundation, DOI 10.13039/501100001732;

Award ID: DNRF137

Award ID: U24AT010811

Award ID: F32AT011475

Funded by: Natural Sciences and Engineering Council of Canada;

Funded by: Netherlands Organization for Scientific Research (NWO) Veni Science;

Award ID: VI.Veni.202.130

Funded by: CARTNET;

Award ID: 765147

Funded by: SECRETed;

Award ID: 101000794

Funded by: MARBLES;

Award ID: 101000392

Funded by: Horizon 2020 Marie Skłodowska-Curie Actions;

Award ID: 893122

Funded by: Horizon 2020 Marie Sklodowska-Curie Individual Fellowship;

Award ID: MSCA-IF-EF-ST-897121

Funded by: U.S. Department of Energy, DOI 10.13039/100000015;

Award ID: DE-AC02-05CH11231

Funded by: University of Strathclyde, DOI 10.13039/100008078;

Funded by: Consejo Nacional de Ciencia y Tecnología, DOI 10.13039/501100003141;

Award ID: 757173

Funded by: Portuguese Science and Technology Foundation, DOI 10.13039/501100001871;

Award ID: SFRH/BD/140567/2018

Funded by: National Science Foundation, DOI 10.13039/100000001;

Award ID: CBET-2032243

Funded by: National Research Foundation of Korea, DOI 10.13039/501100003725;

Award ID: NRF-2022R1C1C2004118

Award ID: NRF-2020R1C1C1004046

Funded by: National Institutes of Health, DOI 10.13039/100000002;

Award ID: GM134688

Award ID: 1R01AI155694

Funded by: Netherlands eScience Center, DOI 10.13039/100013407;

Award ID: ASDI.2017.030

Funded by: Deutsche Forschungsgemeinschaft, DOI 10.13039/501100001659;

Award ID: 398967434-TRR 261

Funded by: Biotechnology and Biological Sciences Research Council, DOI 10.13039/501100000268;

Award ID: BBSRC

Award ID: BB/R022054/1

Award ID: BB/W013959/1

Funded by: UK government Department for Environment, Food and Rural Affairs;

Funded by: Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro, DOI 10.13039/501100004586;

Award ID: E-26/211.314/2019

Funded by: Fundaçao para a Ciencia e Tecnologia (FCT);

Award ID: SFRH/BD/136367/2018

Funded by: German Chemical Industry scholarship;

Funded by: Cooperative Research Centres Projects scheme;

Award ID: CRCPFIVE000119

Funded by: Consejo Nacional de Ciencia y Tecnología, DOI 10.13039/501100003141;

Award ID: 735867

Funded by: Natural Sciences and Engineering Council of Canada PGSD;

Funded by: Odo van Vloten foundation;

Funded by: LOEWE Center for Translational Biodiversity Genomics (LOEWE TBG);

Funded by: Rothamsted Science Initiatives Catalyst Award;

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