Nanoscale resolution of microbial fiber degradation in action

  1. Meltem Tatli
  2. Sarah Moraïs
  3. Omar E Tovar-Herrera
  4. Yannick J Bomble
  5. Edward A Bayer
  6. Ohad Medalia  Is a corresponding author
  7. Itzhak Mizrahi  Is a corresponding author
  1. University of Zurich, Switzerland
  2. Ben-Gurion University of the Negev, Israel
  3. National Renewable Energy Laboratory, United States
  4. Weizmann Institute of Science, Israel
  5. University of Zürich, Switzerland

Abstract

The lives of microbes unfold at the micron scale, and their molecular machineries operate at the nanoscale. Their study at these resolutions is key towards achieving a better understanding of their ecology. We focus on cellulose degradation of the canonical Clostridium thermocellum system to comprehend how microbes build and use their cellulosomal machinery at these nanometer scales. Degradation of cellulose, the most abundant organic polymer on Earth, is instrumental to the global carbon cycle. We reveal that bacterial cells form 'cellulosome capsules' driven by catalytic product-dependent dynamics, which can increase the rate of hydrolysis. Biosynthesis of this energetically costly machinery and cell growth are decoupled at the single-cell level, hinting at a division-of-labor strategy through phenotypic heterogeneity. This novel observation highlights intra-population interactions as key to understanding rates of fiber degradation.

Data availability

Structural data that support the findings of this study has been deposited in the Electron Microscopy Data Bank https://www.ebi.ac.uk/emdb/ (accession code EMD-11986). Representative data set can be found in EMPIAR under the accession number EMPIAR-10593.

The following data sets were generated

Article and author information

Author details

  1. Meltem Tatli

    Department of Biochemistry, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Sarah Moraïs

    Faculty of Natural Sciences, Ben-Gurion University of the Negev, Beer Sheva, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Omar E Tovar-Herrera

    Faculty of Natural Sciences, Ben-Gurion University of the Negev, Beer Sheva, Israel
    Competing interests
    The authors declare that no competing interests exist.
  4. Yannick J Bomble

    National Renewable Energy Laboratory, Golden, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7624-8000
  5. Edward A Bayer

    Department of Biomolecular Sciences, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  6. Ohad Medalia

    Department of Biochemistry, University of Zürich, Zurich, Switzerland
    For correspondence
    omedalia@bioc.uzh.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0994-2937
  7. Itzhak Mizrahi

    Faculty of Natural Sciences, Ben-Gurion University of the Negev, Beer Sheva, Israel
    For correspondence
    imizrahi@bgu.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6636-8818

Funding

Deutsche Forschungsgemeinschaft (2476/2 -1)

  • Ohad Medalia
  • Itzhak Mizrahi

HORIZON EUROPE European Research Council (64084)

  • Itzhak Mizrahi

Swiss national foundation (31003A_179418)

  • Ohad Medalia

Center for Bioenergy Innovation

  • Yannick J Bomble

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Steven Smith

Version history

  1. Preprint posted: February 16, 2021 (view preprint)
  2. Received: December 21, 2021
  3. Accepted: May 30, 2022
  4. Accepted Manuscript published: May 31, 2022 (version 1)
  5. Version of Record published: June 13, 2022 (version 2)
  6. Version of Record updated: June 21, 2022 (version 3)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Meltem Tatli
  2. Sarah Moraïs
  3. Omar E Tovar-Herrera
  4. Yannick J Bomble
  5. Edward A Bayer
  6. Ohad Medalia
  7. Itzhak Mizrahi
(2022)
Nanoscale resolution of microbial fiber degradation in action
eLife 11:e76523.
https://doi.org/10.7554/eLife.76523

Share this article

https://doi.org/10.7554/eLife.76523

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