Given the success of this Research Topic, we would like to launch a second edition of the topic <a href="https://www.frontiersin.org/research-topics/16245/antimicrobial-resistance-in-aquatic-environments">"Antimicrobial Resistance in Aquatic Environments"</a>

Technical University of Ambato

Agroscope (Switzerland)

Pontificia Universidad Católica de Valparaíso

University of Barcelona

Frontiers in Microbiology

Antimicrobials, Resistance and Chemotherapy

Antimicrobial Resistance in Aquatic Environments, Vol II

An integrated approach that encompasses all ecological compartments is urgently needed to understand the emergence, maintenance, and dissemination of multidrug-resistant bacteria and antimicrobial resistance genes (ARGs) (<a href="#B2">Hernando-Amado et al., 2019</a>). However, the role of aquatic environments in this process remains an open question for the scientific community. In light of this, we collaborated with Frontiers in Microbiology to launch a Research Topic “Antimicrobial resistance in aquatic environments” during 2020–2021. This topic aimed to deliver state-of-the-art knowledge and ideas on the role of aquatic environments in selecting, maintaining, and dispersing antimicrobial resistance (AMR) determinants. It included articles from Europe, Asia, America, and Africa that expanded our knowledge and raised new questions for the global scientific community (<a href="#B1">Calero-Cáceres et al., 2022</a>). Due to its success, we launched a second volume of the Research Topic in May 2022.This volume received 8 manuscript submissions, all of which underwent strict peer review. Of these, 5 were accepted for publication. The Research Topics covered a range of subjects, including the evaluation of anthropogenic pollution in water bodies, bioinformatic re-analysis of whole-genome sequences of Escherichia coli harboring mobile colistin resistance, a review article on cross-selection of antibiotic resistance in aquatic environments, and a meta-analysis of the prevalence of antibiotic-resistant bacteria (ARB) in marine bivalves. These studies employed modern methodologies such as high-throughput qPCR and whole-genome sequencing.Two articles in this volume evaluated the anthropogenic impact on water bodies in terms of antibiotic resistance determinants and biological tracers of pollution. The first study, conducted by <a href="https://doi.org/10.3389/fmicb.2022.1009297">Fernanda et al.</a> in China, assessed the diversity and abundance of ARGs and mobile genetic elements (MGEs) in Taihu Lake's inflow rivers. Results showed a significant correlation between water quality parameters and ARG abundance, as well as a strong positive correlation between ARGs and industrial, low-density residential, and cultivated land. These findings indicate that Taihu Lake's inflow rivers are polluted by multiple sources, including nutrients and high ARGs abundance.The second study was conducted by <a href="https://doi.org/10.3389/fmicb.2022.1029176">Nguyen et al.</a> at two sites along the Chattahoochee River in the United States to understand how within-day variation could impact monitoring data interpretation. Samples were collected and assayed for fecal indicator bacteria (FIB), human fecal-associated microbial source tracking (MST) markers, and clinically relevant ARGs. Mean levels of FIB and ARGs were similar across sites, while MST markers occurred at higher mean levels at the natural site. Human-associated MST markers positively correlated with ARGs at both sites. In addition to their relevance in their specific geographical areas, these results provide valuable insights for potentially standardizing tracers for ARGs dissemination in the environment.In their article, <a href="https://doi.org/10.3389/fmicb.2022.1032753">Calero-Cáceres et al.</a> discussed the importance of the One Health concept in addressing multidrug-resistant bacteria. They presented an analysis of whole-genome sequences of E. coli that harbor the mobile colistin resistance gene mcr-1 from various origins and geographical locations. The results revealed a wide array of ARGs, virulence genes, and plasmids in E. coli isolates that carry mcr-1 genes worldwide. These findings underscore the importance of analyzing environmental settings as part of surveillance programs to understand the origins and dissemination of mcr genes.This study of <a href="https://doi.org/10.3389/fmicb.2022.1040568">Albini et al.</a> aimed to describe the prevalence of AMR in bacterial isolates from bivalves using a systematic review of the literature. The meta-analysis revealed Aeromonas spp. as the genus with the highest prevalence of AMR (37%), followed by Vibrio spp. (34%), Salmonella spp. (18%), and E. coli (15%). Resistance to third/fourth/fifth generation cephalosporins and fluoroquinolones was recorded in ~10% of E. coli isolates. The study shows the presence of ARB, including bacteria resistant to the highest priority critically important antimicrobials in marine bivalves, posing a risk for consumers.The review of <a href="https://doi.org/10.3389/fmicb.2022.1050558">Basiry et al.</a> addressed the issue of increased use of disinfectants and antiseptics (DAs) due to the outbreak of the SARS-CoV-2 pandemic, resulting in higher concentrations of these compounds in wastewaters and water bodies. Their constant presence in water bodies may lead to development and acquisition of resistance against the DAs and may also promote antibiotic resistance (AR) due to cross- and co-selection of AR among bacteria that are exposed to the DAs. The review provides an overview of DAs structure and their mode of action against microorganisms. Relevant examples of treatment techniques to increase the DAs removal efficiency from wastewater are discussed. Research needs to determine the impact of DAs in wastewater treatment plants and the consequences of their presence to the spread of AR.In conclusion, these studies provide an excellent update on the role of aquatic ecosystems in the evolution and dissemination of AMR globally. The editors encourage the scientific community to take note of the results and challenges presented in this Research Topic.JO-P, EM, LR-R, and WC-C contributed to analyzing the reviewed articles and preparing the manuscript. All authors contributed to the article and approved the submitted version.WC-C expresses gratitude toward the Operative Unit of the Department of Food and Biotechnology Science and Engineering, of the Directorate of Research (Universidad T&#xe9;cnica de Ambato). LR-R is a lecturer of the Serra-H&#xfa;nter program (Generalitat de Catalunya). JO-P would like to thank to Millennium Science Initiative/Millennium Initiative for Collaborative Research on Bacterial Resistance, MICROB-R.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.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.

Editorial: Antimicrobial resistance in aquatic environments, volume II

The importance of the One Health concept in attempting to deal with the increasing levels of multidrug-resistant bacteria in both human and animal health is a challenge for the scientific community, policymakers, and the industry. The discovery of the plasmid-borne mobile colistin resistance (mcr) in 2015 poses a significant threat because of the ability of these plasmids to move between different bacterial species through horizontal gene transfer. In light of these findings, the World Health Organization (WHO) recommends that countries implement surveillance strategies to detect the presence of plasmid-mediated colistin-resistant microorganisms and take suitable measures to control and prevent their dissemination. Seven years later, ten different variants of the mcr gene (mcr-1 to mcr-10) have been detected worldwide in bacteria isolated from humans, animals, foods, the environment, and farms. However, the possible transmission mechanisms of the mcr gene among isolates from different geographical origins and sources are largely unknown. This article presents an analysis of whole-genome sequences of Escherichia coli that harbor mcr-1 gene from different origins (human, animal, food, or environment) and geographical location, to identify specific patterns related to virulence genes, plasmid content and antibiotic resistance genes, as well as their phylogeny and their distribution with their origin. In general, E. coli isolates that harbor mcr-1 showed a wide plethora of ARGs. Regarding the plasmid content, the highest concentration of plasmids was found in animal samples. In turn, Asia was the continent that led with the largest diversity and occurrence of these plasmids. Finally, about virulence genes, terC, gad, and traT represent the most frequent virulence genes detected. These findings highlight the relevance of analyzing the environmental settings as an integrative part of the surveillance programs to understand the origins and dissemination of antimicrobial resistance.

The importance of the One Health concept in attempting to deal with the increasing levels of multidrug-resistant bacteria in both human and animal health is a challenge for the scientific community, policymakers, and the industry. The discovery of the plasmid-borne mobile colistin resistance (mcr) in 2015 poses a significant threat because of the ability of these plasmids to move between different bacterial species through horizontal gene transfer. In light of these findings, the World Health Organization (WHO) recommends that countries implement surveillance strategies to detect the presence of plasmid-mediated colistin-resistant microorganisms and take suitable measures to control and prevent their dissemination. Seven years later, ten different variants of the mcr gene (mcr-1 to mcr-10) have been detected worldwide in bacteria isolated from humans, animals, foods, the environment, and farms. However, the possible transmission mechanisms of the mcr gene among isolates from different geographical origins and sources are largely unknown. This article presents an analysis of whole-genome sequences of Escherichia coli that harbor mcr-1 gene from different origins (human, animal, food, or environment) and geographical location, to identify specific patterns related to virulence genes, plasmid content and antibiotic resistance genes, as well as their phylogeny and their distribution with their origin. In general, E. coli isolates that harbor mcr-1 showed a wide plethora of ARGs. Regarding the plasmid content, the highest concentration of plasmids was found in animal samples. In turn, Asia was the continent that led with the largest diversity and occurrence of these plasmids. Finally, about virulence genes, terC, gad, and traT represent the most frequent virulence genes detected. These findings highlight the relevance of analyzing the environmental settings as an integrative part of the surveillance programs to understand the origins and dissemination of antimicrobial resistance.

Genomic insights of mcr-1 harboring Escherichia coli by geographical region and a One-Health perspective

The outbreak of the SARS-CoV-2 pandemic led to increased use of disinfectants and antiseptics (DAs), resulting in higher concentrations of these compounds in wastewaters, wastewater treatment plant (WWTP) effluents and receiving water bodies. Their constant presence in water bodies may lead to development and acquisition of resistance against the DAs. In addition, they may also promote antibiotic resistance (AR) due to cross- and co-selection of AR among bacteria that are exposed to the DAs, which is a highly important issue with regards to human and environmental health. This review addresses this issue and provides an overview of DAs structure together with their modes of action against microorganisms. Relevant examples of the most effective treatment techniques to increase the DAs removal efficiency from wastewater are discussed. Moreover, insight on the resistance mechanisms to DAs and the mechanism of DAs enhancement of cross- and co-selection of ARs are presented. Furthermore, this review discusses the impact of DAs on resistance against antibiotics, the occurrence of DAs in aquatic systems, and DA removal mechanisms in WWTPs, which in principle serve as the final barrier before releasing these compounds into the receiving environment. By recognition of important research gaps, research needs to determine the impact of the majority of DAs in WWTPs and the consequences of their presence and spread of antibiotic resistance were identified.

The outbreak of the SARS-CoV-2 pandemic led to increased use of disinfectants and antiseptics (DAs), resulting in higher concentrations of these compounds in wastewaters, wastewater treatment plant (WWTP) effluents and receiving water bodies. Their constant presence in water bodies may lead to development and acquisition of resistance against the DAs. In addition, they may also promote antibiotic resistance (AR) due to cross- and co-selection of AR among bacteria that are exposed to the DAs, which is a highly important issue with regards to human and environmental health. This review addresses this issue and provides an overview of DAs structure together with their modes of action against microorganisms. Relevant examples of the most effective treatment techniques to increase the DAs removal efficiency from wastewater are discussed. Moreover, insight on the resistance mechanisms to DAs and the mechanism of DAs enhancement of cross- and co-selection of ARs are presented. Furthermore, this review discusses the impact of DAs on resistance against antibiotics, the occurrence of DAs in aquatic systems, and DA removal mechanisms in WWTPs, which in principle serve as the final barrier before releasing these compounds into the receiving environment. By recognition of important research gaps, research needs to determine the impact of the majority of DAs in WWTPs and the consequences of their presence and spread of antibiotic resistance were identified.

The effect of disinfectants and antiseptics on co- and cross-selection of resistance to antibiotics in aquatic environments and wastewater treatment plants

Bivalves are filter-feeding animals able to accumulate contaminants and microorganisms, either of marine or terrestrial origin. The aim of this study was to describe the prevalence of antimicrobial resistance (AMR) in bacterial isolates from bivalves using a systematic review of the literature. Comprehensive searches of MEDLINE, EMBASE, and Web of Science were carried out, based upon a registered protocol (PROSPERO), and following the preferred Reporting Items for Systematic reviews and Meta-Analysis (PRISMA) guidelines. The methodological quality of the included studies was assessed using a modified Hoy checklist. Meta-analyses of prevalence were carried out using random-effects models. In total, 103 articles were selected from 1,280 records and were included in the final analysis. The studies were from Asia (n = 54), Europe (n = 27), South and North America (n = 10 and n = 6, respectively), Africa (n = 2), Oceania (n = 1), and multicentre and intercontinental (n = 3). The meta-analysis of multiple antibiotic resistance (MAR) index revealed Aeromonas spp. as the genus with the highest prevalence of AMR (37%), followed by Vibrio spp. (34%), Salmonella spp. (18%), and Escherichia coli (15%). Resistance to third/fourth/fifth generation cephalosporins and fluoroquinolones, two highest priority, critically important antimicrobials (HPCIA), was recorded in approximately 10% of E. coli isolates. Resistance to carbapenems was very low (<2%) in Salmonella spp. and in E. coli, but was found in 5% of Vibrio spp. and in more than a third of Aeromonas spp. isolates. In aquatic bacteria, resistance to carbapenems was higher in Asian than in European isolates. Our study shows the presence of antibiotic resistant bacteria (ARB), including bacteria resistant to HPCIA, in marine bivalves, posing a risk for consumers.

Bivalves are filter-feeding animals able to accumulate contaminants and microorganisms, either of marine or terrestrial origin. The aim of this study was to describe the prevalence of antimicrobial resistance (AMR) in bacterial isolates from bivalves using a systematic review of the literature. Comprehensive searches of MEDLINE, EMBASE, and Web of Science were carried out, based upon a registered protocol (PROSPERO), and following the preferred Reporting Items for Systematic reviews and Meta-Analysis (PRISMA) guidelines. The methodological quality of the included studies was assessed using a modified Hoy checklist. Meta-analyses of prevalence were carried out using random-effects models. In total, 103 articles were selected from 1,280 records and were included in the final analysis. The studies were from Asia (n = 54), Europe (n = 27), South and North America (n = 10 and n = 6, respectively), Africa (n = 2), Oceania (n = 1), and multicentre and intercontinental (n = 3). The meta-analysis of multiple antibiotic resistance (MAR) index revealed Aeromonas spp. as the genus with the highest prevalence of AMR (37%), followed by Vibrio spp. (34%), Salmonella spp. (18%), and Escherichia coli (15%). Resistance to third/fourth/fifth generation cephalosporins and fluoroquinolones, two highest priority, critically important antimicrobials (HPCIA), was recorded in approximately 10% of E. coli isolates. Resistance to carbapenems was very low (&lt;2%) in Salmonella spp. and in E. coli, but was found in 5% of Vibrio spp. and in more than a third of Aeromonas spp. isolates. In aquatic bacteria, resistance to carbapenems was higher in Asian than in European isolates. Our study shows the presence of antibiotic resistant bacteria (ARB), including bacteria resistant to HPCIA, in marine bivalves, posing a risk for consumers.

A systematic review and meta-analysis on antimicrobial resistance in marine bivalves

Water bodies that serve as sources of drinking or recreational water are routinely monitored for fecal indicator bacteria (FIB) by state and local agencies. Exceedances of monitoring thresholds set by those agencies signal likely elevated human health risk from exposure, but FIB give little information about the potential source of contamination. To improve our understanding of how within-day variation could impact monitoring data interpretation, we conducted a study at two sites along the Chattahoochee River that varied in their recreational usage and adjacent land-use (natural versus urban), collecting samples every 30 min over one 24-h period. We assayed for three types of microbial indicators: FIB (total coliforms and Escherichia coli); human fecal-associated microbial source tracking (MST) markers (crAssphage and HF183/BacR287); and a suite of clinically relevant antibiotic resistance genes (ARGs; blaCTX-M, blaCMY, MCR, KPC, VIM, NDM) and a gene associated with antibiotic resistance (intl1). Mean levels of FIB and clinically relevant ARGs (blaCMY and KPC) were similar across sites, while MST markers and intI1 occurred at higher mean levels at the natural site. The human-associated MST markers positively correlated with antibiotic resistant-associated genes at both sites, but no consistent associations were detected between culturable FIB and any molecular markers. For all microbial indicators, generalized additive mixed models were used to examine diurnal variability and whether this variability was associated with environmental factors (water temperature, turbidity, pH, and sunlight). We found that FIB peaked during morning and early afternoon hours and were not associated with environmental factors. With the exception of HF183/BacR287 at the urban site, molecular MST markers and intI1 exhibited diurnal variability, and water temperature, pH, and turbidity were significantly associated with this variability. For blaCMY and KPC, diurnal variability was present but was not correlated with environmental factors. These results suggest that differences in land use (natural or urban) both adjacent and upstream may impact overall levels of microbial contamination. Monitoring agencies should consider matching sample collection times with peak levels of target microbial indicators, which would be in the morning or early afternoon for the fecal associated indicators. Measuring multiple microbial indicators can lead to clearer interpretations of human health risk associated with exposure to contaminated water.

Water bodies that serve as sources of drinking or recreational water are routinely monitored for fecal indicator bacteria (FIB) by state and local agencies. Exceedances of monitoring thresholds set by those agencies signal likely elevated human health risk from exposure, but FIB give little information about the potential source of contamination. To improve our understanding of how within-day variation could impact monitoring data interpretation, we conducted a study at two sites along the Chattahoochee River that varied in their recreational usage and adjacent land-use (natural versus urban), collecting samples every 30 min over one 24-h period. We assayed for three types of microbial indicators: FIB (total coliforms and Escherichia coli); human fecal-associated microbial source tracking (MST) markers (crAssphage and HF183/BacR287); and a suite of clinically relevant antibiotic resistance genes (ARGs; blaCTX-M, blaCMY, MCR, KPC, VIM, NDM) and a gene associated with antibiotic resistance (intl1). Mean levels of FIB and clinically relevant ARGs (blaCMY and KPC) were similar across sites, while MST markers and intI1 occurred at higher mean levels at the natural site. The human-associated MST markers positively correlated with antibiotic resistant-associated genes at both sites, but no consistent associations were detected between culturable FIB and any molecular markers. For all microbial indicators, generalized additive mixed models were used to examine diurnal variability and whether this variability was associated with environmental factors (water temperature, turbidity, pH, and sunlight). We found that FIB peaked during morning and early afternoon hours and were not associated with environmental factors. With the exception of HF183/BacR287 at the urban site, molecular MST markers and intI1 exhibited diurnal variability, and water temperature, pH, and turbidity were significantly associated with this variability. For blaCMY and KPC, diurnal variability was present but was not correlated with environmental factors. These results suggest that differences in land use (natural or urban) both adjacent and upstream may impact overall levels of microbial contamination. Monitoring agencies should consider matching sample collection times with peak levels of target microbial indicators, which would be in the morning or early afternoon for the fecal associated indicators. Measuring multiple microbial indicators can lead to clearer interpretations of human health risk associated with exposure to contaminated water.

Fecal indicators and antibiotic resistance genes exhibit diurnal trends in the Chattahoochee River: Implications for water quality monitoring

Taihu Lake is the third largest freshwater lake in China and an important source for drinking water, flood protection, aquaculture, agriculture, and other activities. This lake is connected to many principal and small rivers with inflow from west and outflow on the eastern side of the lake and these inflow rivers are believed to significantly contribute to the water pollution of the lake. This study was aimed at assessing the diversity and abundance of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs), and their relationship with water quality parameters and land use patterns. Water samples were collected from 10 major inflow rivers and the source water protection area of the Taihu Lake in spring and summer 2019. High-throughput profiling was used to detect and quantify 384 ARGs and MGEs and in addition, 11 water quality parameters were analyzed. The results showed that the number of ARGs/MGEs detected in each inflow river ranged from 105 to 185 in spring and 107 to 180 in summer. The aminoglycoside resistance genes were the most dominant types ARGs detected followed by beta-lactam resistance, multidrug resistance, macrolide-lincosamide-streptogramin B (MLSB) resistance genes, which contributed to 65% of the ARGs. The water quality parameters showed significant correlation with absolute abundance of ARGs. Furthermore, significant correlation between ARGs and MGEs were also observed which demonstrates potential gene transfer among organisms through horizontal gene transfer via MGEs. ARGs showed strong positive correlation with cultivated and industrial lands whereas, negative correlation was observed with river, lake, forest, land for green buffer, and land for port and harbor. The overall results indicate that the inflow rivers of Taihu Lake are polluted by various sources including multiple nutrients and high abundance of ARGs, which needs attention for better management of the inflow rivers of this lake.

Taihu Lake is the third largest freshwater lake in China and an important source for drinking water, flood protection, aquaculture, agriculture, and other activities. This lake is connected to many principal and small rivers with inflow from west and outflow on the eastern side of the lake and these inflow rivers are believed to significantly contribute to the water pollution of the lake. This study was aimed at assessing the diversity and abundance of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs), and their relationship with water quality parameters and land use patterns. Water samples were collected from 10 major inflow rivers and the source water protection area of the Taihu Lake in spring and summer 2019. High-throughput profiling was used to detect and quantify 384 ARGs and MGEs and in addition, 11 water quality parameters were analyzed. The results showed that the number of ARGs/MGEs detected in each inflow river ranged from 105 to 185 in spring and 107 to 180 in summer. The aminoglycoside resistance genes were the most dominant types ARGs detected followed by beta-lactam resistance, multidrug resistance, macrolide-lincosamide-streptogramin B (MLSB) resistance genes, which contributed to 65% of the ARGs. The water quality parameters showed significant correlation with absolute abundance of ARGs. Furthermore, significant correlation between ARGs and MGEs were also observed which demonstrates potential gene transfer among organisms through horizontal gene transfer via MGEs. ARGs showed strong positive correlation with cultivated and industrial lands whereas, negative correlation was observed with river, lake, forest, land for green buffer, and land for port and harbor. The overall results indicate that the inflow rivers of Taihu Lake are polluted by various sources including multiple nutrients and high abundance of ARGs, which needs attention for better management of the inflow rivers of this lake.