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Antibiotic Resistome from the One-Health Perspective: Understanding and Controlling Antimicrobial Resistance Transmission Dae-Wi Kim1 and Chang-Jun Cha2

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Antibiotic Resistome from the One-Health Perspective: Understanding and Controlling Antimicrobial Resistance Transmission Dae-Wi Kim1 and Chang-Jun Cha2 Kim and Cha Experimental & Molecular Medicine (2021) 53:301–309 https://doi.org/10.1038/s12276-021-00569-z Experimental & Molecular Medicine REVIEW ARTICLE Open Access Antibiotic resistome from the One-Health perspective: understanding and controlling antimicrobial resistance transmission Dae-Wi Kim1 and Chang-Jun Cha2 Abstract The concept of the antibiotic resistome was introduced just over a decade ago, and since then, active resistome studies have been conducted. In the present study, we describe the previously established concept of the resistome, which encompasses all types of antibiotic resistance genes (ARGs), and the important findings from each One-Health sector considering this concept, thereby emphasizing the significance of the One-Health approach in understanding ARG transmission. Cutting-edge research methodologies are essential for deciphering the complex resistome structure in the microbiomes of humans, animals, and the environment. Based on the recent achievements of resistome studies in multiple One-Health sectors, future directions for resistome research have been suggested to improve the understanding and control of ARG transmission: (1) ranking the critical ARGs and their hosts; (2) understanding ARG transmission at the interfaces of One-Health sectors; (3) identifying selective pressures affecting the emergence, transmission, and evolution of ARGs; and (4) elucidating the mechanisms that allow an organism to overcome taxonomic barriers in ARG transmission. 1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; Introduction genes originated from antibiotic-producing actinomy- Since the discovery of the first antibiotic penicillin1, cetes6. Consequently, after this discovery, ARGs were antibiotics have been considered essential drugs for intensively studied in only clinical pathogens for >30 years treating bacterial infections; however, unlike with other until the resistome concept was proposed7; this concept medicines, antibiotic drug resistance has become a great has provided exceptional insights into the origin and concern owing to its continuous emergence and rapid dissemination of ARGs. This review aims to describe the dissemination among pathogens, as reported in recent concept of the antibiotic resistome; summarize the cases, posing substantial clinical threats2,3. Since the use information from the last decade regarding approaches of early-date antibiotics, such as penicillin and salvarsan, under the concept; and provide a comprehensive under- emergence and dissemination of resistance have been standing of the origin, emergence, dissemination, and observed after introducing antibiotics into clinical set- evolution of ARGs. In particular, resistome studies from tings4,5; this resistance is considered to be mainly medi- the One-Health (Human–Animal–Environment) per- ated by antibiotic resistance genes (ARGs). In 1973, spective will be essential for deciphering the complex environmental ARGs were characterized to be genetically resistome structure and determining prioritized factors to similar to clinical ARGs, suggesting that these clinical aid in the mitigation of ARG transmission to the clinic. Concept of the antibiotic resistome Correspondence: Chang-Jun Cha ([email protected]) The term “antibiotic resistome” was first coined in 2006 1 Division of Life Sciences, Jeonbuk National University, Jeonju 54896, Republic by Gerry Wright’s group, who defined the soil resistome of Korea 2Department of Systems Biotechnology and Center for Antibiotic Resistome, as “resistance determinants present in the soil”, thereby Chung-Ang University, Anseong 17546, Republic of Korea © The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a linktotheCreativeCommons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Official journal of the Korean Society for Biochemistry and Molecular Biology Kim and Cha Experimental & Molecular Medicine (2021) 53:301–309 302 demonstrating that multidrug resistance in a population environment18; (v) anthropogenic activities shape the of environmental bacteria was more prevalent than pre- environmental resistome19; (vi) mobile genetic elements viously assumed7. Later, the resistome was defined as “a are responsible for ARG transmission20; and (vii) ARGs collection of all the ARGs and their precursors in flow among humans, animals, and the environment21. pathogenic and nonpathogenic bacteria”8. Its constituents These discoveries have provided the base for recent were precisely described as “all ARGs, including those approaches aimed at improving the understanding of circulating in pathogenic bacteria, antibiotic producers, AMR in the human, animal, and environmental sectors, and benign nonpathogenic bacteria”9. Considering the namely, the “One-Health” approach. origin of ARGs, the resistome has been suggested to include protoresistance genes as a deep reservoir of ARG Antibiotic resistome in One-Health sectors precursors, as well as clinical, environmental, and intrinsic The One-Health concept resistance genes10. After a large number of studies on the As mentioned above, ARGs circulate among the resistome were published, the definition was further microbiomes of humans, animals, and the environment, refined by designating types of resistance, such as which form the different sectors of the One-Health con- acquired resistance (vertically or horizontally transferred, cept. One-Health is defined as the “collaborative effort of taxa-nonspecific), intrinsic resistance (only vertically multiple disciplines–working locally, nationally, and transmitted, taxa-specific), silent/cryptic resistance (phe- globally–to attain optimal health for people, animals, and notypically sensitive, functional but not expressed), and the environment through policy, research, education, and protoresistance (phenotypically sensitive, little/no activity practice”22,23. Initially, zoonoses were recognized as major until mutated)11. In summary, the antibiotic resistome issues in both humans and animals. In 2008, the impor- encompasses all types of ARGs (acquired and intrinsic tance of “ecosystems” was particularly emphasized in the resistance genes), their precursors, and some potential One-Health concept; this was documented by consulta- resistance mechanisms within microbial communities tion from several organizations including the Food and that require evolution or alterations in the expression Agriculture Organization (FAO), World Organization for context to confer resistance (Fig. 1). Animal Health (OIE), and World Health Organization Since 2006, critical information about antimicrobial (WHO) (http://www.fao.org/3/aj137e/aj137e00.htm). In resistance (AMR) has been revealed based on the resis- general, infectious diseases, including zoonoses, are the tome concept. Old speculations were confirmed, and main concerns and targets of the One-Health approach. critical new findings were suggested as follows: (i) AMR is AMR, which is directly related to such diseases, was – ancient and ubiquitous in various microbiomes12 14; (ii) considered one of the three One-Health priorities during the antibiotic resistome is complex and diverse15,16; (iii) the tripartite (FAO-OIE-WHO) meeting in 201124. Con- the environmental resistome is the origin and a reservoir sidering ARG flow among the One-Health sectors, it has of ARGs13,15,17; (iv) the resistome is generally determined been recognized as one of the main issues in the One- by the microbial community structure in the natural Health approach25,26. The One-Health concept has focused on interconnections and interdependencies among sectors at local sites; however, recently, consider- Microbiome ing global health, the comprehension of communication Environmental microbiome fi Animal microbiome among local ecosystems and the identi cation of factors Human microbiome that stimulate the global AMR crisis has also gained immense attention27. In the present study, we review the Pathogenic Commensal Environmental bacteria bacteria bacteria achievements in each sector and evaluate the factors that need to be prioritized to mitigate ARG transmission to the clinic. Strain-level Microbiome-level Resistome Environmental resistome Since the resistome concept originated in the soil Intrinsic ARG environment, the environmental resistome has been Proto Expression Silent 7 Evoluon extensively deciphered . ARGs, as ancient and ubiquitous ARG context ARG components of bacteria, exist in all ecological niches that Acquired ARG harbor various microbial communities13,28. From the viewpoint of microbial ecology, the environment can be classified into natural and built environments, and the Fig. 1 Concept of the antibiotic resistome from the One-Health perspective. former can be divided into aquatic and terrestrial envir- onments. The aquatic environment includes marine Official journal of the
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