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Genomic and metabolic adaptations of biofilms to ecological windows of opportunities in glacier-fed streams

View ORCID ProfileSusheel Bhanu Busi, View ORCID ProfileMassimo Bourquin, View ORCID ProfileStilianos Fodelianakis, Grégoire Michoud, View ORCID ProfileTyler J. Kohler, View ORCID ProfileHannes Peter, View ORCID ProfileParaskevi Pramateftaki, Michail Styllas, Matteo Tolosano, Vincent De Staercke, Martina Schön, Laura de Nies, View ORCID ProfileRamona Marasco, View ORCID ProfileDaniele Daffonchio, View ORCID ProfileLeïla Ezzat, View ORCID ProfilePaul Wilmes, View ORCID ProfileTom J. Battin
doi: https://doi.org/10.1101/2021.10.07.463499
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
Massimo Bourquin
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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  • ORCID record for Massimo Bourquin
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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Tyler J. Kohler
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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Paraskevi Pramateftaki
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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Laura de Nies
1Systems Ecology Group, Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg
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Ramona Marasco
3Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia
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Daniele Daffonchio
3Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia
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Leïla Ezzat
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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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: tom.battin@epfl.ch paul.wilmes@uni.lu
Tom J. Battin
2Stream Biofilm & Ecosystem Research Lab, ENAC, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
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  • For correspondence: tom.battin@epfl.ch paul.wilmes@uni.lu
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Abstract

Microorganisms dominate life in cryospheric ecosystems. In glacier-fed streams (GFSs), ecological windows of opportunities allow complex microbial biofilms to develop and transiently form the basis of the food web, thereby controlling key ecosystem processes. Here, using high-resolution metagenomics, we unravel strategies that allow biofilms to seize this opportunity in an ecosystem otherwise characterized by harsh environmental conditions. We found a diverse microbiome spanning the entire tree of life and including a rich virome. Various and co-existing energy acquisition pathways point to diverse niches and the simultaneous exploitation of available resources, likely fostering the establishment of complex biofilms in GFSs during windows of opportunity. The wide occurrence of rhodopsins across metagenome-assembled genomes (MAGs), besides chlorophyll, highlights the role of solar energy capture in these biofilms. Concomitantly, internal carbon and nutrient cycling between photoautotrophs and heterotrophs may help overcome constraints imposed by the high oligotrophy in GFSs. MAGs also revealed mechanisms potentially protecting bacteria against low temperatures and high UV-radiation. The selective pressure of the GFS environment is further highlighted by the phylogenomic analysis, differentiating the representatives of the genus Polaromonas, an important component of the GFS microbiome, from those found in other ecosystems. Our findings reveal key genomic underpinnings of adaptive traits that contribute to the success of complex biofilms to exploit environmental opportunities in GFSs, now rapidly changing owing to global warming.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://doi.org/10.5281/zenodo.5545722

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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 4.0 International license.
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Genomic and metabolic adaptations of biofilms to ecological windows of opportunities in glacier-fed streams
Susheel Bhanu Busi, Massimo Bourquin, Stilianos Fodelianakis, Grégoire Michoud, Tyler J. Kohler, Hannes Peter, Paraskevi Pramateftaki, Michail Styllas, Matteo Tolosano, Vincent De Staercke, Martina Schön, Laura de Nies, Ramona Marasco, Daniele Daffonchio, Leïla Ezzat, Paul Wilmes, Tom J. Battin
bioRxiv 2021.10.07.463499; doi: https://doi.org/10.1101/2021.10.07.463499
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Genomic and metabolic adaptations of biofilms to ecological windows of opportunities in glacier-fed streams
Susheel Bhanu Busi, Massimo Bourquin, Stilianos Fodelianakis, Grégoire Michoud, Tyler J. Kohler, Hannes Peter, Paraskevi Pramateftaki, Michail Styllas, Matteo Tolosano, Vincent De Staercke, Martina Schön, Laura de Nies, Ramona Marasco, Daniele Daffonchio, Leïla Ezzat, Paul Wilmes, Tom J. Battin
bioRxiv 2021.10.07.463499; doi: https://doi.org/10.1101/2021.10.07.463499

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