Genomic and metabolic adaptations of biofilms to ecological windows of opportunity 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 Staercke, Martina Schön, Laura Nies, Ramona Marasco, Daniele Daffonchio, Leïla Ezzat, Paul Wilmes () and Tom J. Battin ()
Additional contact information
Susheel Bhanu Busi: University of Luxembourg
Massimo Bourquin: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Stilianos Fodelianakis: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Grégoire Michoud: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Tyler J. Kohler: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Hannes Peter: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Paraskevi Pramateftaki: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Michail Styllas: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Matteo Tolosano: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Vincent Staercke: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Martina Schön: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Laura Nies: University of Luxembourg
Ramona Marasco: King Abdullah University of Science and Technology (KAUST)
Daniele Daffonchio: King Abdullah University of Science and Technology (KAUST)
Leïla Ezzat: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Paul Wilmes: University of Luxembourg
Tom J. Battin: Ecole Polytechnique Fédérale de Lausanne (EPFL)

Nature Communications, 2022, vol. 13, issue 1, 1-15

Abstract: Abstract In glacier-fed streams, ecological windows of opportunity allow complex microbial biofilms to develop and transiently form the basis of the food web, thereby controlling key ecosystem processes. Using metagenome-assembled genomes, we unravel strategies that allow biofilms to seize this opportunity in an ecosystem otherwise characterized by harsh environmental conditions. We observe a diverse microbiome spanning the entire tree of life including a rich virome. Various co-existing energy acquisition pathways point to diverse niches and the exploitation of available resources, likely fostering the establishment of complex biofilms during windows of opportunity. The wide occurrence of rhodopsins, besides chlorophyll, highlights the role of solar energy capture in these biofilms while internal carbon and nutrient cycling between photoautotrophs and heterotrophs may help overcome constraints imposed by oligotrophy in these habitats. Mechanisms potentially protecting bacteria against low temperatures and high UV-radiation are also revealed and the selective pressure of this environment is further highlighted by a phylogenomic analysis differentiating important components of the glacier-fed stream microbiome from other ecosystems. Our findings reveal key genomic underpinnings of adaptive traits contributing to the success of complex biofilms to exploit environmental opportunities in glacier-fed streams, which are now rapidly changing owing to global warming.

Date: 2022
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DOI: 10.1038/s41467-022-29914-0

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