Mobilome-driven segregation of the resistome in biological wastewater treatment
- University of Luxembourg, Luxembourg
Abstract
Biological wastewater treatment plants (BWWTP) are considered to be hotspots of 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 fifteen 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 MGEs. 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, for which MGEs also contributed differentially to the dissemination of ARGs. Collectively our findings pave the way towards 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.
Data availability
The genomic FASTQ files used in this work (previously published) are publicly available at NCBI BioProject PRJNA230567. Metaproteomic data (previously published) are publicly available at the PRIDE database under accession number PXD013655.The open-source tools and algorithms used for the data analyses are reported in the Methods section, including relevant flags used for the various tools. Additionally, custom code for further analysis and generation of the figures can be found at: https://git-r3lab.uni.lu/laura.denies/lao_scripts
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Systems Biology of Lipid Accumulating OrganismsNCBI BioProject, PRJNA230567.
Article and author information
Author details
Susheel Bhanu Busi
Benoit Josef Kunath
Funding
Fonds National de la Recherche Luxembourg (CORE/BM/11333923)
- Paul Wilmes
European Research Council (ERC-CoG 863664)
- Paul Wilmes
Fonds National de la Recherche Luxembourg (PRIDE/11823097)
- Paul Wilmes
Fonds National de la Recherche Luxembourg (PRIDE/11823097)
- Laura de Nies
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (CRSII5_180241)
- Susheel Bhanu Busi
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- María Mercedes Zambrano, CorpoGen, Colombia
Version history
- Preprint posted: November 15, 2021 (view preprint)
- Received: June 19, 2022
- Accepted: September 15, 2022
- Accepted Manuscript published: September 16, 2022 (version 1)
- Version of Record published: November 8, 2022 (version 2)
Copyright
© 2022, de Nies et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Mobilome-driven segregation of the resistome in biological wastewater treatment
eLife 11:e81196.
https://doi.org/10.7554/eLife.81196
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