Toward a Universal Unit for Quantification of Antibiotic Resistance Genes in Environmental Samples

Xiaole Yin¹, Xi Chen¹, Xiao-Tao Jiang², Ying Yang³, Bing Li⁴, Marcus Ho-Hin Shum⁵, Tommy T Y Lam⁵, Gabriel M Leung⁶, Joan Rose⁷, Concepcion Sanchez-Cid⁸, Timothy M Vogel⁸, Fiona Walsh⁹, Thomas U Berendonk¹⁰, Janet Midega¹¹, Chibuzor Uchea¹¹, Dominic Frigon¹², Gerard D Wright¹³, Carlos Bezuidenhout¹⁴, Renata C Picão¹⁵, Shaikh Z Ahammad¹⁶, Per Halkjær Nielsen¹⁷, Philip Hugenholtz¹⁸, Nicholas J Ashbolt¹⁹, Gianluca Corno²⁰, Despo Fatta-Kassinos²¹, Helmut Bürgmann²², Heike Schmitt^{23

24}, Chang-Jun Cha²⁵, Amy Pruden²⁶, Kornelia Smalla²⁷, Eddie Cytryn²⁸, Yu Zhang²⁹, Min Yang²⁹, Yong-Guan Zhu³⁰, Arnaud Dechesne³¹, Barth F Smets³¹, David W Graham³², Michael R Gillings³³, William H Gaze³⁴, Célia M Manaia³⁵, Mark C M van Loosdrecht³⁶, Pedro J J Alvarez³⁷, Martin J Blaser³⁸, James M Tiedje³⁹, Edward Topp⁴⁰, Tong Zhang¹

Affiliations

¹ Environmental Microbiome Engineering and Biotechnology Laboratory, Center for Environmental Engineering Research, Department of Civil Engineering, The University of Hong Kong, Pokfulam, 99077 Hong Kong, China.
² Microbiome Research Centre, St George and Sutherland Clinical School, University of New South Wales, 2052 Sydney, Australia.
³ School of Marine Sciences, Sun Yat-sen University, 519082 Zhuhai, China.
⁴ State Environmental Protection Key Laboratory of Microorganism Application and Risk Control, Tsinghua Shenzhen International Graduate School, Tsinghua University, F518055 Shenzhen, China.
⁵ State Key Laboratory of Emerging Infectious Diseases, School of Public Health, The University of Hong Kong, Pokfulam, 999077 Hong Kong, China.
⁶ Laboratory of Data Discovery for Health, Hong Kong Science & Technology Parks, New Territories, 99077 Hong Kong, China.
⁷ Department of Fisheries and Wildlife, Michigan State University, East Lansing, 48824 Michigan, United States.
⁸ Environmental Microbial Genomics, CNRS UMR 5005 Laboratoire Ampère, École Centrale de Lyon, Université Claude Bernard Lyon1, Université de Lyon, 69130 Écully, France.
⁹ Department of Biology, Maynooth University, Maynooth, R51 Co. Kildare, Ireland.
¹⁰ Faculty of Environmental Sciences, Technische Universität Dresden, Institute for Hydrobiology, 01217 Dresden, Germany.
¹¹ Wellcome Trust, NW1 2BE London, U.K.
¹² Department of Civil Engineering and Applied Mechanics, McGill University, 817 Sherbrooke St. West, Montreal, H3A 0C3 Quebec, Canada.
¹³ Michael G. DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, L8N 3Z5 Ontario, Canada.
¹⁴ Unit for Environmental Sciences and Management (UESM)-Microbiology, North-West University, 2531 Potchefstroom, South Africa.
¹⁵ Medical Microbiology Department, Paulo de Góes Microbiology Institute of the Federal University of Rio de Janeiro, 21941-902 Rio de Janeiro, Brazil.
¹⁶ Department of Biochemical Engineering & Biotechnology, Indian Institute of Technology Delhi, Hauz Khas, 110016 New Delhi, India.
¹⁷ Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, 9210 Aalborg, Denmark.
¹⁸ School of Chemistry and Molecular Biosciences, Australian Centre for Ecogenomics, The University of Queensland, Brisbane, 4072 Queensland, Australia.
¹⁹ Faculty of Science and Engineering, Southern Cross University, Bilinga, 4225 Queensland, Australia.
²⁰ Molecular Ecology Group (MEG), Water Research Institute, National Research Council of Italy (CNR-IRSA), 28922 Verbania, Italy.
²¹ Department of Civil and Environmental Engineering and Nireas International Water Research Center, University of Cyprus, P.O. Box 20537, 1678 Nicosia, Cyprus.
²² Eawag: Swiss Federal Institute of Aquatic Science and Technology, 6047 Kastanienbaum, Switzerland.
²³ Centre for Zoonoses and Environmental Microbiology-Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), 3721 Bilthoven, The Netherlands.
²⁴ Department of Biotechnology, Delft University of Technology, 2628 Delft, the Netherlands.
²⁵ Department of Systems Biotechnology and Center for Antibiotic Resistome, Chung-Ang University, 17546 Anseong, Republic of Korea.
²⁶ The Charles Edward Via, Jr., Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, 24060 Virginia, United States.
²⁷ Julius Kühn Institute (JKI) Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, 38104 Braunschweig, Germany.
²⁸ Department of Soil Chemistry, Plant Nutrition and Microbiology, Institute of Soil, Water and Environmental Sciences, The Volcani Institute, Agricultural Research Organization, 7528809 Rishon LeZion, Israel.
²⁹ State Key Laboratory of Environmental Aquatic Chemistry, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, 100085 Beijing, China.
³⁰ Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 361021 Xiamen, China.
³¹ Department of Environmental and Resource Engineering, Technical University of Denmark, 2800 Lyngby, Denmark.
³² School of Engineering, Newcastle University, NE1 7RU Newcastle Upon Tyne, U.K.
³³ School of Natural Sciences and ARC Centre of Excellence in Synthetic Biology, Macquarie University, Sydney, 2109 New South Wales, Australia.
³⁴ University of Exeter Medical School, Environment and Sustainability Institute, University of Exeter, TR10 9FE Cornwall, U.K.
³⁵ Universidade Católica Portuguesa, CBQF-Centro de Biotecnologia e Química Fina-Laboratório Associado, Escola Superior de Biotecnologia, 4169-005 Porto, Portugal.
³⁶ Department of Biotechnology, Delft University of Technology, van der Maasweg 9, 2629 HZ Delft, the Netherlands.
³⁷ Department of Civil and Environmental Engineering, Rice University, Houston, 77005 Texas, United States.
³⁸ Center for Advanced Biotechnology and Medicine, Rutgers University, Piscataway, 08854 New Jersey, United States.
³⁹ Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, 48824 Michigan, United States.
⁴⁰ London Research and Development Centre (LRDC), Agriculture and Agri-Food Canada, London, N5V 4T3 Ontario, Canada.

PMID: 37310875
DOI: 10.1021/acs.est.3c00159

Toward a Universal Unit for Quantification of Antibiotic Resistance Genes in Environmental Samples

Xiaole Yin et al. Environ Sci Technol. 2023.

. 2023 Jul 4;57(26):9713-9721.

doi: 10.1021/acs.est.3c00159. Epub 2023 Jun 13.

Authors

Affiliations

¹ Environmental Microbiome Engineering and Biotechnology Laboratory, Center for Environmental Engineering Research, Department of Civil Engineering, The University of Hong Kong, Pokfulam, 99077 Hong Kong, China.
² Microbiome Research Centre, St George and Sutherland Clinical School, University of New South Wales, 2052 Sydney, Australia.
³ School of Marine Sciences, Sun Yat-sen University, 519082 Zhuhai, China.
⁴ State Environmental Protection Key Laboratory of Microorganism Application and Risk Control, Tsinghua Shenzhen International Graduate School, Tsinghua University, F518055 Shenzhen, China.
⁵ State Key Laboratory of Emerging Infectious Diseases, School of Public Health, The University of Hong Kong, Pokfulam, 999077 Hong Kong, China.
⁶ Laboratory of Data Discovery for Health, Hong Kong Science & Technology Parks, New Territories, 99077 Hong Kong, China.
⁷ Department of Fisheries and Wildlife, Michigan State University, East Lansing, 48824 Michigan, United States.
⁸ Environmental Microbial Genomics, CNRS UMR 5005 Laboratoire Ampère, École Centrale de Lyon, Université Claude Bernard Lyon1, Université de Lyon, 69130 Écully, France.
⁹ Department of Biology, Maynooth University, Maynooth, R51 Co. Kildare, Ireland.
¹⁰ Faculty of Environmental Sciences, Technische Universität Dresden, Institute for Hydrobiology, 01217 Dresden, Germany.
¹¹ Wellcome Trust, NW1 2BE London, U.K.
¹² Department of Civil Engineering and Applied Mechanics, McGill University, 817 Sherbrooke St. West, Montreal, H3A 0C3 Quebec, Canada.
¹³ Michael G. DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, L8N 3Z5 Ontario, Canada.
¹⁴ Unit for Environmental Sciences and Management (UESM)-Microbiology, North-West University, 2531 Potchefstroom, South Africa.
¹⁵ Medical Microbiology Department, Paulo de Góes Microbiology Institute of the Federal University of Rio de Janeiro, 21941-902 Rio de Janeiro, Brazil.
¹⁶ Department of Biochemical Engineering & Biotechnology, Indian Institute of Technology Delhi, Hauz Khas, 110016 New Delhi, India.
¹⁷ Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, 9210 Aalborg, Denmark.
¹⁸ School of Chemistry and Molecular Biosciences, Australian Centre for Ecogenomics, The University of Queensland, Brisbane, 4072 Queensland, Australia.
¹⁹ Faculty of Science and Engineering, Southern Cross University, Bilinga, 4225 Queensland, Australia.
²⁰ Molecular Ecology Group (MEG), Water Research Institute, National Research Council of Italy (CNR-IRSA), 28922 Verbania, Italy.
²¹ Department of Civil and Environmental Engineering and Nireas International Water Research Center, University of Cyprus, P.O. Box 20537, 1678 Nicosia, Cyprus.
²² Eawag: Swiss Federal Institute of Aquatic Science and Technology, 6047 Kastanienbaum, Switzerland.
²³ Centre for Zoonoses and Environmental Microbiology-Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), 3721 Bilthoven, The Netherlands.
²⁴ Department of Biotechnology, Delft University of Technology, 2628 Delft, the Netherlands.
²⁵ Department of Systems Biotechnology and Center for Antibiotic Resistome, Chung-Ang University, 17546 Anseong, Republic of Korea.
²⁶ The Charles Edward Via, Jr., Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, 24060 Virginia, United States.
²⁷ Julius Kühn Institute (JKI) Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, 38104 Braunschweig, Germany.
²⁸ Department of Soil Chemistry, Plant Nutrition and Microbiology, Institute of Soil, Water and Environmental Sciences, The Volcani Institute, Agricultural Research Organization, 7528809 Rishon LeZion, Israel.
²⁹ State Key Laboratory of Environmental Aquatic Chemistry, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, 100085 Beijing, China.
³⁰ Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 361021 Xiamen, China.
³¹ Department of Environmental and Resource Engineering, Technical University of Denmark, 2800 Lyngby, Denmark.
³² School of Engineering, Newcastle University, NE1 7RU Newcastle Upon Tyne, U.K.
³³ School of Natural Sciences and ARC Centre of Excellence in Synthetic Biology, Macquarie University, Sydney, 2109 New South Wales, Australia.
³⁴ University of Exeter Medical School, Environment and Sustainability Institute, University of Exeter, TR10 9FE Cornwall, U.K.
³⁵ Universidade Católica Portuguesa, CBQF-Centro de Biotecnologia e Química Fina-Laboratório Associado, Escola Superior de Biotecnologia, 4169-005 Porto, Portugal.
³⁶ Department of Biotechnology, Delft University of Technology, van der Maasweg 9, 2629 HZ Delft, the Netherlands.
³⁷ Department of Civil and Environmental Engineering, Rice University, Houston, 77005 Texas, United States.
³⁸ Center for Advanced Biotechnology and Medicine, Rutgers University, Piscataway, 08854 New Jersey, United States.
³⁹ Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, 48824 Michigan, United States.
⁴⁰ London Research and Development Centre (LRDC), Agriculture and Agri-Food Canada, London, N5V 4T3 Ontario, Canada.

PMID: 37310875
DOI: 10.1021/acs.est.3c00159

Abstract

Surveillance of antibiotic resistance genes (ARGs) has been increasingly conducted in environmental sectors to complement the surveys in human and animal sectors under the "One-Health" framework. However, there are substantial challenges in comparing and synthesizing the results of multiple studies that employ different test methods and approaches in bioinformatic analysis. In this article, we consider the commonly used quantification units (ARG copy per cell, ARG copy per genome, ARG density, ARG copy per 16S rRNA gene, RPKM, coverage, PPM, etc.) for profiling ARGs and suggest a universal unit (ARG copy per cell) for reporting such biological measurements of samples and improving the comparability of different surveillance efforts.

Keywords: ARG copy per cell; long-read sequencing; metagenomics; one-health; standardization.

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Toward a Universal Unit for Quantification of Antibiotic Resistance Genes in Environmental Samples

Affiliations

Toward a Universal Unit for Quantification of Antibiotic Resistance Genes in Environmental Samples

Authors

Affiliations

Abstract

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Grants and funding

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Medical