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Glacier-fed stream biofilms harbour diverse resistomes and biosynthetic gene clusters

View ORCID ProfileSusheel Bhanu Busi, Laura de Nies, Paraskevi Pramateftaki, Massimo Bourquin, Leïla Ezzat, Tyler J. Kohler, Stilianos Fodelianakis, Grégoire Michoud, Hannes Peter, Michail Styllas, Matteo Tolosano, Vincent De Staercke, Martina Schön, Valentina Galata, Paul Wilmes, Tom Battin
doi: https://doi.org/10.1101/2021.11.18.469141
Susheel Bhanu Busi
1Systems Ecology Group, Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg
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  • ORCID record for Susheel Bhanu Busi
  • For correspondence: paul.wilmes@uni.lu susheel.busi@uni.lu
Laura de Nies
1Systems Ecology Group, Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg
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Paraskevi Pramateftaki
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Massimo Bourquin
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Leïla Ezzat
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Tyler J. Kohler
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Stilianos Fodelianakis
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Grégoire Michoud
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Hannes Peter
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Michail Styllas
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Matteo Tolosano
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Vincent De Staercke
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Martina Schön
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Valentina Galata
1Systems Ecology Group, Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg
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Paul Wilmes
1Systems Ecology Group, Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg
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  • For correspondence: paul.wilmes@uni.lu susheel.busi@uni.lu
Tom Battin
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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Abstract

Background Antimicrobial resistance (AMR) is a universal phenomenon whose origins lay in natural ecological interactions such as competition within niches, within and between micro- to higher-order organisms. However, the ecological and evolutionary processes shaping AMR need to be better understood in view of better antimicrobial stewardship. Resolving antibiotic biosynthetic pathways, including biosynthetic gene clusters (BGCs), and corresponding antimicrobial resistance genes (ARGs) may therefore help in understanding the inherent mechanisms. However, to study these phenomena, it is crucial to examine the origins of AMR in pristine environments with limited anthropogenic influences. In this context, epilithic biofilms residing in glacier-fed streams (GFSs) are an excellent model system to study diverse, intra- and inter-domain, ecological crosstalk.

Results We assessed the resistomes of epilithic biofilms from GFSs across the Southern Alps (New Zealand) and the Caucasus (Russia) and observed that both bacteria and eukaryotes encoded twenty-nine distinct AMR categories. Of these, beta-lactam, aminoglycoside, and multidrug resistance were both abundant and taxonomically distributed in most of the bacterial and eukaryotic phyla. AMR-encoding phyla included Bacteroidota and Proteobacteria among the bacteria, alongside Ochrophyta (algae) among the eukaryotes. Additionally, BGCs involved in the production of antibacterial compounds were identified across all phyla in the epilithic biofilms. Furthermore, we found that several bacterial genera (Flavobacterium, Polaromonas, etc.) including representatives of the superphylum Patescibacteria encode both ARGs and BGCs within close proximity of each other, thereby demonstrating their capacity to simultaneously influence and compete within the microbial community.

Conclusions Our findings highlight the presence and abundance of AMR in epilithic biofilms within GFSs. Additionally, we identify their role in the complex intra- and inter-domain competition and the underlying mechanisms influencing microbial survival in GFS epilithic biofilms. We demonstrate that eukaryotes may serve as AMR reservoirs owing to their potential for encoding ARGs. We also find that the taxonomic affiliation of the AMR and the BGCs are congruent. Importantly, our findings allow for understanding how naturally occurring BGCs and AMR contribute to the epilithic biofilms mode of life in GFSs. Importantly, these observations may be generalizable and potentially extended to other environments which may be more or less impacted by human activity.

Competing Interest Statement

The authors have declared no competing interest.

  • List of Abbreviations

    AMR
    Antimicrobial resistance
    ARGs
    Antimicrobial resistance gene(s)
    BGC
    Biosynthetic gene clusters
    CA
    Caucasus
    CPR
    Candidate Phyla radiation
    GFSs
    Glacier-fed stream(s)
    GL
    Glacier
    IRS-RS
    isoleucyl-tRNA synthetase - high resistance
    IMP
    Integrate Meta-Omics Pipeline
    KEGG
    Kyoto Encyclopedia of Genes and Genomes
    MAGs
    Metagenome-assembled genome(s)
    NRPS
    Non-ribosomal peptide synthetases
    PKS
    Polyketide synthases (type I and type II)
    RiPPs
    Post-translationally modified peptide(s)
    SA
    Southern Alps
  • Copyright 
    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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    Posted November 19, 2021.
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    Glacier-fed stream biofilms harbour diverse resistomes and biosynthetic gene clusters
    Susheel Bhanu Busi, Laura de Nies, Paraskevi Pramateftaki, Massimo Bourquin, Leïla Ezzat, Tyler J. Kohler, Stilianos Fodelianakis, Grégoire Michoud, Hannes Peter, Michail Styllas, Matteo Tolosano, Vincent De Staercke, Martina Schön, Valentina Galata, Paul Wilmes, Tom Battin
    bioRxiv 2021.11.18.469141; doi: https://doi.org/10.1101/2021.11.18.469141
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    Glacier-fed stream biofilms harbour diverse resistomes and biosynthetic gene clusters
    Susheel Bhanu Busi, Laura de Nies, Paraskevi Pramateftaki, Massimo Bourquin, Leïla Ezzat, Tyler J. Kohler, Stilianos Fodelianakis, Grégoire Michoud, Hannes Peter, Michail Styllas, Matteo Tolosano, Vincent De Staercke, Martina Schön, Valentina Galata, Paul Wilmes, Tom Battin
    bioRxiv 2021.11.18.469141; doi: https://doi.org/10.1101/2021.11.18.469141

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