Time-series sewage metagenomics distinguishes seasonal, human-derived and environmental microbial communities potentially allowing source-attributed surveillance

Sewage metagenomics has risen to prominence in urban population surveillance of pathogens and antimicrobial resistance (AMR). Unknown species with similarity to known genomes cause database bias in reference-based metagenomics. To improve surveillance, we seek to recover sewage genomes and develop a quantification and correlation workflow for these genomes and AMR over time. We use longitudinal sewage sampling in seven treatment plants from five major European cities to explore the utility of catch-all sequencing of these population-level samples. Using metagenomic assembly methods, we recover 2332 metagenome-assembled genomes (MAGs) from prokaryotic species, 1334 of which were previously undescribed. These genomes account for ~69% of sequenced DNA and provide insight into sewage microbial dynamics. Rotterdam (Netherlands) and Copenhagen (Denmark) show strong seasonal microbial community shifts, while Bologna, Rome, (Italy) and Budapest (Hungary) have occasional blooms of Pseudomonas-dominated communities, accounting for up to ~95% of sample DNA. Seasonal shifts and blooms present challenges for effective sewage surveillance. We find that bacteria of known shared origin, like human gut microbiota, form communities, suggesting the potential for source-attributing novel species and their ARGs through network community analysis. This could significantly improve AMR tracking in urban environments.

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Publication Details

Journal
Nature Communications
Published
2024-08-30
DOI
https://doi.org/10.1038/s41467-024-51957-8
Citations
39
Primary Topic
Genomics and Phylogenetic Studies
Type
article
Field-Weighted Citation Impact
9.12

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article

Time-series sewage metagenomics distinguishes seasonal, human-derived and environmental microbial communities potentially allowing source-attributed surveillance

Patrick Munk, Christian Brinch, Dávid Visontai, Saria Otani et al.
39 citations
Nature Communications
Genomics and Phylogenetic Studies
9.12
article

Time-series sewage metagenomics distinguishes seasonal, human-derived and environmental microbial communities potentially allowing source-attributed surveillance

Patrick Munk, Christian Brinch, Dávid Visontai, Saria Otani, Marion Koopmans, Péter Pollner, Patricia Alba, Frank M. Aarestrup, Olli Vapalahti, Daniel Remondini, József Stéger, Antonio Battisti, Frédérique Pasquali, Tarja Sironen, Alessandra Merlotti, István Csabai, Miranda de Graaf, Alessandro Fuschi, Krisztián Bànyai, Alessandra De Cesare, Ágnes Becsei, Ilja Weinstein, Fulvia Troja, Chiara Oliveri, Magdolna Makó, Ravi Kant, Claudia M. E. Schapendonk
article en
39 citations

Abstract

Sewage metagenomics has risen to prominence in urban population surveillance of pathogens and antimicrobial resistance (AMR). Unknown species with similarity to known genomes cause database bias in reference-based metagenomics. To improve surveillance, we seek to recover sewage genomes and develop a quantification and correlation workflow for these genomes and AMR over time. We use longitudinal sewage sampling in seven treatment plants from five major European cities to explore the utility of catch-all sequencing of these population-level samples. Using metagenomic assembly methods, we recover 2332 metagenome-assembled genomes (MAGs) from prokaryotic species, 1334 of which were previously undescribed. These genomes account for ~69% of sequenced DNA and provide insight into sewage microbial dynamics. Rotterdam (Netherlands) and Copenhagen (Denmark) show strong seasonal microbial community shifts, while Bologna, Rome, (Italy) and Budapest (Hungary) have occasional blooms of Pseudomonas-dominated communities, accounting for up to ~95% of sample DNA. Seasonal shifts and blooms present challenges for effective sewage surveillance. We find that bacteria of known shared origin, like human gut microbiota, form communities, suggesting the potential for source-attributing novel species and their ARGs through network community analysis. This could significantly improve AMR tracking in urban environments.

Nature CommunicationsVol. 15(1)
Semmelweis University (HU), Eötvös Loránd University (HU), University of Helsinki (FI), Erasmus MC (NL), HUN-REN Veterinary Medical Research Institute (HU), University of Veterinary Medicine (HU), Istituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana (IT), Gdańsk Medical University (PL), Erasmus University Rotterdam (NL), University of Bologna (IT), Technical University of Denmark (DK)
Novo Nordisk, Novo Nordisk Fonden, Horizon 2020 Framework Programme
Clean water and sanitation
Openalex Percentile: Top 1%
Genomics and Phylogenetic Studies
9.12
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