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

Author

Listed:
  • 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
    University of Luxembourg)

  • Tom J. Battin

    (Ecole Polytechnique Fédérale de Lausanne (EPFL))

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.

Suggested Citation

  • Susheel Bhanu Busi & Massimo Bourquin & Stilianos Fodelianakis & Grégoire Michoud & Tyler J. Kohler & Hannes Peter & Paraskevi Pramateftaki & Michail Styllas & Matteo Tolosano & Vincent Staercke & Mar, 2022. "Genomic and metabolic adaptations of biofilms to ecological windows of opportunity in glacier-fed streams," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29914-0
    DOI: 10.1038/s41467-022-29914-0
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    1. Robert L. Sinsabaugh & Brian H. Hill & Jennifer J. Follstad Shah, 2009. "Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment," Nature, Nature, vol. 462(7274), pages 795-798, December.
    2. Christopher M. Bellas & Declan C. Schroeder & Arwyn Edwards & Gary Barker & Alexandre M. Anesio, 2020. "Flexible genes establish widespread bacteriophage pan-genomes in cryoconite hole ecosystems," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    3. S. A. Amin & L. R. Hmelo & H. M. van Tol & B. P. Durham & L. T. Carlson & K. R. Heal & R. L. Morales & C. T. Berthiaume & M. S. Parker & B. Djunaedi & A. E. Ingalls & M. R. Parsek & M. A. Moran & E. V, 2015. "Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria," Nature, Nature, vol. 522(7554), pages 98-101, June.
    4. Matthias Huss & Regine Hock, 2018. "Global-scale hydrological response to future glacier mass loss," Nature Climate Change, Nature, vol. 8(2), pages 135-140, February.
    5. Tom J. Battin & Louis A. Kaplan & J. Denis Newbold & Claude M. E. Hansen, 2003. "Contributions of microbial biofilms to ecosystem processes in stream mesocosms," Nature, Nature, vol. 426(6965), pages 439-442, November.
    6. Yang Liu & Kira S. Makarova & Wen-Cong Huang & Yuri I. Wolf & Anastasia N. Nikolskaya & Xinxu Zhang & Mingwei Cai & Cui-Jing Zhang & Wei Xu & Zhuhua Luo & Lei Cheng & Eugene V. Koonin & Meng Li, 2021. "Expanded diversity of Asgard archaea and their relationships with eukaryotes," Nature, Nature, vol. 593(7860), pages 553-557, May.
    7. Zachary D Kurtz & Christian L Müller & Emily R Miraldi & Dan R Littman & Martin J Blaser & Richard A Bonneau, 2015. "Sparse and Compositionally Robust Inference of Microbial Ecological Networks," PLOS Computational Biology, Public Library of Science, vol. 11(5), pages 1-25, May.
    8. Martin T. Croft & Andrew D. Lawrence & Evelyne Raux-Deery & Martin J. Warren & Alison G. Smith, 2005. "Algae acquire vitamin B12 through a symbiotic relationship with bacteria," Nature, Nature, vol. 438(7064), pages 90-93, November.
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