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Author Spotlight: Understanding and Detecting Environmental Antimicrobial Resistance by Combining Culture-Based Techniques and Genomics
Published on: July 19, 2024
Mobilome-driven segregation of the resistome in biological wastewater treatment
Laura de Nies1, Susheel Bhanu Busi1, Benoit Josef Kunath1
1Systems Ecology Group, Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg.
Abstract:
Biological wastewater treatment plants (BWWTP) are considered to be hotspots for the evolution and subsequent spread of antimicrobial resistance (AMR). Mobile genetic elements (MGEs) promote the mobilization and dissemination of antimicrobial resistance genes (ARGs) and are thereby critical mediators of AMR within the BWWTP microbial community. At present, it is unclear whether specific AMR categories are differentially disseminated via bacteriophages (phages) or plasmids. To understand the segregation of AMR in relation to MGEs, we analyzed meta-omic (metagenomic, metatranscriptomic and metaproteomic) data systematically collected over 1.5 years from a BWWTP. Our results showed a core group of 15 AMR categories which were found across all timepoints. Some of these AMR categories were disseminated exclusively (bacitracin) or primarily (aminoglycoside, MLS and sulfonamide) via plasmids or phages (fosfomycin and peptide), whereas others were disseminated equally by both. Combined and timepoint-specific analyses of gene, transcript and protein abundances further demonstrated that aminoglycoside, bacitracin and sulfonamide resistance genes were expressed more by plasmids, in contrast to fosfomycin and peptide AMR expression by phages, thereby validating our genomic findings. In the analyzed communities, the dominant taxon Candidatus Microthrix parvicella was a major contributor to several AMR categories whereby its plasmids primarily mediated aminoglycoside resistance. Importantly, we also found AMR associated with ESKAPEE pathogens within the BWWTP, and here MGEs also contributed differentially to the dissemination of the corresponding ARGs. Collectively our findings pave the way toward understanding the segmentation of AMR within MGEs, thereby shedding new light on resistome populations and their mediators, essential elements that are of immediate relevance to human health.
Insights
Biological wastewater treatment plants spread antimicrobial resistance (AMR) via mobile genetic elements like phages and plasmids. This study reveals specific AMR types are predominantly spread by either phages or plasmids, impacting human health.
Area of Science:
- Environmental microbiology
- Molecular biology
- Public health
Background:
- Biological wastewater treatment plants (BWWTPs) are significant reservoirs for antimicrobial resistance (AMR) evolution and dissemination.
- Mobile genetic elements (MGEs), including plasmids and bacteriophages (phages), are key drivers of antimicrobial resistance gene (ARG) spread within microbial communities.
- The differential roles of phages and plasmids in disseminating specific AMR categories remain poorly understood.
Purpose of the Study:
- To investigate the segregation of AMR categories in relation to MGEs (phages and plasmids) within a BWWTP.
- To determine if specific AMR types are preferentially disseminated by phages or plasmids.
- To understand the contribution of MGEs to AMR in dominant bacterial taxa and pathogens.
Main Methods:
- Systematic analysis of meta-omic data (metagenomics, metatranscriptomics, metaproteomics) collected over 1.5 years from a BWWTP.
- Identification and quantification of AMR categories and their associated MGEs.
- Analysis of gene, transcript, and protein abundances to infer ARG expression and dissemination mechanisms.
Main Results:
- A core set of 15 AMR categories were consistently detected throughout the study period.
- Specific AMR categories showed distinct dissemination patterns: bacitracin (exclusively plasmids), aminoglycoside, MLS, and sulfonamide (primarily plasmids), and fosfomycin and peptide (primarily phages).
- Candidatus Microthrix parvicella was a major AMR contributor, with its plasmids mediating aminoglycoside resistance. AMR associated with ESKAPEE pathogens was also observed, with differential MGE contributions.
Conclusions:
- AMR dissemination in BWWTPs is significantly mediated by MGEs, with distinct preferences for phages or plasmids for specific resistance types.
- Understanding these MGE-plasmid/phage-AMR associations provides crucial insights into resistome dynamics and public health.
- This research highlights the need to consider MGE-mediated AMR spread in wastewater treatment for effective public health strategies.
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