Zhi Wang
Yuyi Yang
Marcelo Pedrosa Gomes3
Surindra Suthar- 1Key Laboratory for Environment and Disaster Monitoring and Evaluation of Hubei, Innovation Academy for Precision Measurement Science and Technology, Chinese Academy of Sciences, Wuhan, China
- 2Key Laboratory of Aquatic Botany and Watershed Ecology Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China
- 3Laboratório de Fisiologia de Plantas Sob Estresse, Departamento de Botânica, Setor de Ciências Biológicas, Universidade Federal Do Paraná, Curitiba, Brazil
- 4School of Environment & Natural Resources, Doon University, Dehradun, India
Editorial on the Research Topic
Antibiotics and antibiotic resistance genes in waters: pollution, risks and control
Introduction
In 1928, British microbiologist Alexander Fleming discovered penicillin from Penicillium for the first time. Since then, human society has entered the golden age of antibiotics (Kümmerer, 2009; Zhang et al., 2015). Antibiotics play a great role in preventing and treating the disease, health maintenance, and life extension. However, it is also due to the extensive use and abuse of antibiotics that the continuous residue of antibiotics in the environment has been detected (Wang et al., 2017) resulting in their toxic effects on the ecosystem (Boxall et al., 2003; Sarmah et al., 2006). Moreover, long-term antibiotic exposure could induce the transfer, proliferation and diffusion of microbial antibiotic resistance genes (ARGs), and further, induce “super-resistant bacteria” in the environment or human body (Pruden et al., 2006; Martínez et al., 2015). Once these super-resistant bacteria invade humans, the corresponding diseases typically become incurable. According to the current development trend, it is predicted that “super-resistant bacteria” will cause about 10 million deaths worldwide every year by 2050 (de Kraker et al., 2016). Antibiotic resistance has been listed by the World Health Organization as one of the most urgent public health problems facing the world in the 21st century (WHO, 2014).
Antibiotics are poorly absorbed and metabolized by humans or animals. Studies revealed that up to 70% of antibiotics doses consumed are excreted through urine and faeces including primarily active substances or metabolites (e.g., Jutkina et al., 2018). Conventional sewage or sludge treatment facilities cannot remove antibiotics and resistance genes effectively, and a large number of antibiotics and ARGs eventually enter the natural environment (Berendonk et al., 2015; Cacace et al., 2019). Water is an important sink of antibiotic and resistance gene pollution. Antibiotics and ARGs have been widely detected in surface water, groundwater, and water supply systems (Ma et al., 2017; Wang et al., 2020; Zhang et al., 2022), which pose a great threat to both the ecosystem and human health. Due to the risk of antibiotics and resistance genes, the research on antibiotics and ARGs in the environment has become a hot issue during the past 20 years. Although several investigators have reported the distribution characteristics of antibiotics and ARGs in different environmental media, the understanding of pollution pathways, ecological and health risks, and the degradation and removal mechanisms of antibiotics and ARGs remain a challenge for the field of antibiotics and ARG research due to the complexity of the natural and artificial water systems.
Contents of This Research Topic
This topic mainly aims at the challenges in the current basic and technical research of antibiotics and ARGs in water systems. Finally, we selected 10 manuscripts for publishing after peer review. The main authors are from universities and scientific research institutes in China, America, India, Canada, Brazil, Japan, Ukraine, Switzerland, etc. Among ten published articles, one is a mini-review article, one is an opinion, and eight are original research articles. These published articles are all focused on the different aspects of antibiotics and/or antibiotic resistance genes in water.
Peng et al. introduced the method of analyzing antibiotic resistome in the environment by using metagenomic data and bioinformatics tools. They found that although SARG (Structured Antibiotic Resistance Gene database) is a good database, the application of two or more bioinformatics tools and databases could provide comprehensive information and an in-depth understanding of ARG transmission in the environment. In addition, Das et al. introduced HT-ARGfinder (horizontally transferred ARG finder), which is a pipeline for detecting and enumerating horizontally transferred ARGs in metagenomic data and can also estimate the directionality of transfer.
Gomes et al. investigated the pollution and risk assessment of 10 antibiotics in the river water of the Doce river watershed (Brazil). They found that the detection rate of acyclovir, amoxicillin, azithromycin, ciprofloxacin, enrofloxacin, fluoxetine, erythromycin, sulfadiazine and sulfamethoxazole was 100%; and the highest concentrations of ciprofloxacin and sulfamethoxazole was 4,854.6 ng/L and 9,640 ng/L, respectively. They found most of the investigated antibiotics were above concentrations that pose an ecotoxicological risk to aquatic biota. Guo et al. detected 12 target antibiotics in Dongting Lake in China and found that the antibiotic concentrations in the surface water and sediment were N.D. ∼ 943.49 ng/L and N.D. ∼ 177.43 ng/g, respectively. The risk assessment shows that ofloxacin, sulfamethoxazole, ciprofloxacin, enrofloxacin, roxithromycin and erythromycin have high ecological risks.
Duygan et al. systematically studied the biodegradation of 15 antibiotics such as ampicillin, chloramphenicol, erythromycin, penicillin and sulfamethoxazole under different sources of microorganisms and their effects on microbial communities. They found that growth linked biodegradation of antibiotics at low concentrations may be present among typical environmental microbes, but for a selected subset only, whereas for the majority of antibiotics negative effects prevail without any sign of productive growth.
The high concentration of antibiotics in wastewater can lead to the widespread of ARGs. Chen et al. studied the ARG distribution in cephalosporin production wastewater treatment plant (X-WWTP), subsequent municipal wastewater treatment plant (Y-WWTP) and receiving stream based on functional gene microarray technology. They found that the total abundance of ARGs in X-WWTP wastewater samples were significantly higher than that in Y-WWTP wastewater and stream samples, while the relative abundance of ARGs in river sediments did not change significantly with the distance from the Y-WWTP outlet. Kasuga et al. used a high-throughput quantitative polymerase chain reaction to characterize the profiles of ARGs and mobile gene elements (MGEs) in 24 urban rivers in Tokyo in Japan and their surrounding areas. They also found the effluent from the sewage treatment plant will affect the ARGs of the receiving river and int1could be used as a proxy for monitoring these ARGs and MGEs in urban rivers.
Yang et al. investigated the occurrence of ARGs and bacterial communities in the water and soil of the Ili River (in Xinjiang Province, China) using bacterial testing and metagenomic sequencing. They found fluoroquinolone, aminoglycoside, sulfonamide, and tetracycline resistanceenes were the most prevailing types in this river and pointed out that proteobacteria, bacteroidetes, and actinobacteria were the main potential hosts of ARGs. Guo et al. found sul1 and sul2 were the dominant ARGs in East Dongting Lake Basin; while in the sea ecosystem, Prekrasna et al. found that although the concentration of antibiotics in the Black Sea was below the detection limit, there were relatively high ARG pollution concentrations of vanB, blaSHV, blaCMY and mcr-1.
In addition, Singh et al. published an article on the pollution, risk and control of antibiotics and resistance genes in water. They emphasized the pollution sources and health effects of ARGs in water.
Future Prospects
Due to the extensive use and abuse of antibiotics, it is predictable that residues of antibiotics will be present in the environment for the foreseeable future, and that will contribute to the amplification and transmission of ARGs. In the past half-century, the increasing prevalence of microbial antibiotic resistance has far exceeded the discovery and invention of new antibiotics. Antibiotic resistance has become a global health risk problem. The water environment is the main storage and transmission reservoir of antibiotics and ARGs. The pollution potential of antibiotics and ARGs are bound to have impacts on the ecosystems and human health. Although research on antibiotics and ARGs is increasing in many conunties, major scientific gaps and questions persist, including: 1) The environmental behaviour and ecological effects of antibiotics in different environmental media. What concentration and how long exposure can bring irreversible risks to the ecological environment and biosphere? 2) What are the influencing factors or limiting factors of ARG transmission and diffusion, what is the specific mechanism, and whether the purpose of ARG control can be achieved by regulating these factors? 3) How to quantify the risk of ARGs to the ecosystem and human health? 4) Can regulatory standards of ARGs in the water environment be established? 5) How should antibiotics and ARG pollution be managed and controlled in the future, and how to suggest a balance between antibiotic use and control? All these issues warrent further research.
Finally, we sincerely thank the authors, editorial staff and reviewers who have made great efforts for this Research Topic.
Author Contributions
All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Acknowledgments
We appreciate all authors and reviewers who have contributed to this Research Topic. We are also grateful to the Key Project of Hubei Province Natural Science Foundation China (No. 2020CFA110), the Youth Innovation Promotion Association, Chinese of Academy of Sciences (No. 2018369) by ZW, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) for the research productivity grant awarded to MG.
References
Berendonk, T. U., Manaia, C. M., Merlin, C., Fatta-Kassinos, D., Cytryn, E., Walsh, F., et al. (2015). Tackling Antibiotic Resistance: the Environmental Framework. Nat. Rev. Microbiol. 13, 310–317. doi:10.1038/nrmicro3439
Boxall, A. B. A., Kolpin, D. W., Halling-Sørensen, B., and Tolls, J. (2003). Peer Reviewed: Are Veterinary Medicines Causing Environmental Risks? Environ. Sci. Technol. 37, 286A–294A. doi:10.1021/es032519b
Cacace, D., Fatta-Kassinos, D., Manaia, C. M., Cytryn, E., Kreuzinger, N., Rizzo, L., et al. (2019). Antibiotic Resistance Genes in Treated Wastewater and in the Receiving Water Bodies: A Pan-European Survey of Urban Settings. Water Res. 162, 320–330. doi:10.1016/j.watres.2019.06.039
de Kraker, M. E. A., Stewardson, A. J., and Harbarth, S. (2016). Will 10 Million People Die a Year Due to Antimicrobial Resistance by 2050? PLoS Med. 13, e1002184. doi:10.1371/journal.pmed.1002184
Jutkina, J., Marathe, N. P., Flach, C.-F., and Larsson, D. G. J. (2018). Antibiotics and Common Antibacterial Biocides Stimulate Horizontal Transfer of Resistance at Low Concentrations. Sci. Total Environ. 616-617, 172–178. doi:10.1016/j.scitotenv.2017.10.312
Kümmerer, K. (2009). Antibiotics in the Aquatic Environment - A Review - Part I. Chemosphere 75, 417–434. doi:10.1016/j.chemosphere.2008.11.086
Ma, L., Li, B., Jiang, X.-T., Wang, Y.-L., Xia, Y., Li, A.-D., et al. (2017). Catalogue of Antibiotic Resistome and Host-Tracking in Drinking Water Deciphered by a Large Scale Survey. Microbiome 5, 154. doi:10.1186/s40168-017-0369-0
Martínez, J. L., Coque, T. M., and Baquero, F. (2015). What Is a Resistance Gene? Ranking Risk in Resistomes. Nat. Rev. Microbiol. 13, 116–123. doi:10.1038/nrmicro3399
Pruden, A., Pei, R., Storteboom, H., and Carlson, K. H. (2006). Antibiotic Resistance Genes as Emerging Contaminants: Studies in Northern Colorado. Environ. Sci. Technol. 40, 7445–7450. doi:10.1021/es060413l
Sarmah, A. K., Meyer, M. T., and Boxall, A. B. A. (2006). A Global Perspective on the Use, Sales, Exposure Pathways, Occurrence, Fate and Effects of Veterinary Antibiotics (VAs) in the Environment. Chemosphere 65, 725–759. doi:10.1016/j.chemosphere.2006.03.026
Wang, Z., Du, Y., Yang, C., Liu, X., Zhang, J., Li, E., et al. (2017). Occurrence and Ecological Hazard Assessment of Selected Antibiotics in the Surface Waters in and Around Lake Honghu, China. Sci. Total Environ. 609, 1423–1432. doi:10.1016/j.scitotenv.2017.08.009
Wang, Z., Han, M., Li, E., Liu, X., Wei, H., Yang, C., et al. (2020). Distribution of Antibiotic Resistance Genes in an Agriculturally Disturbed Lake in China: Their Links with Microbial Communities, Antibiotics, and Water Quality. J. Hazard. Mater. 393, 122426. doi:10.1016/j.jhazmat.2020.122426
WHO (2014). Antimicrobial Resistance: Global Report on Surveillance. Geneva, Switzerland: World Health Organization.
Zhang, L., Ji, L., Liu, X., Zhu, X., Ning, K., and Wang, Z. (2022). Linkage and Driving Mechanisms of Antibiotic Resistome in Surface and Ground Water: Their Responses to Land Use and Seasonal Variation. Water Res. 215, 118279. doi:10.1016/j.watres.2022.118279
Zhang, Q.-Q., Ying, G.-G., Pan, C.-G., Liu, Y.-S., and Zhao, J.-L. (2015). Comprehensive Evaluation of Antibiotics Emission and Fate in the River Basins of China: Source Analysis, Multimedia Modeling, and Linkage to Bacterial Resistance. Environ. Sci. Technol. 49, 6772–6782. doi:10.1021/acs.est.5b00729
Keywords: antibiotics, antibiotic resistance genes, environment, risks, one-health
Citation: Wang Z, Yang Y, Gomes MP and Suthar S (2022) Editorial: Antibiotics and Antibiotic Resistance Genes in Waters: Pollution, Risks, and Control. Front. Environ. Sci. 10:967118. doi: 10.3389/fenvs.2022.967118
Received: 12 June 2022; Accepted: 14 June 2022;
Published: 30 June 2022.
Edited and reviewed by:
Oladele Ogunseitan, University of California, United StatesCopyright © 2022 Wang, Yang, Gomes and Suthar. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Zhi Wang, endhbmdAYXBtLmFjLmNu