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.

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.

Metrics

  • 1,438
    views
  • 342
    downloads
  • 6
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Microbiology and Infectious Disease
    Michi Miura, Naho Kiuchi ... Mineki Saito
    Research Article

    Influenza A virus transcribes viral mRNAs from the eight segmented viral genome when it infects. The kinetics of viral transcription, nuclear export of viral transcripts, and their potential variation between the eight segments are poorly characterised. Here, we introduce a statistical framework for estimating the nuclear export rate of each segment from a snapshot of in situ mRNA localisation. This exploits the cell-to-cell variation at a single time point observed by an imaging-based in situ transcriptome assay. Using our model, we revealed the variation in the mRNA nuclear export rate of the eight viral segments. Notably, the two influenza viral antigens hemagglutinin and neuraminidase were the slowest segments in the nuclear export, suggesting the possibility that influenza A virus uses the nuclear retention of viral transcripts to delay the expression of antigenic molecules. Our framework presented in this study can be widely used for investigating the nuclear retention of nascent transcripts produced in a transcription burst.

    1. Microbiology and Infectious Disease
    Yuqian Wang, Guibin Wang ... Xiangmin Lin
    Research Article

    Protein NƐ-lysine acetylation (Kac) modifications play crucial roles in diverse physiological and pathological functions in cells. In prokaryotic cells, there are only two types of lysine deacetylases (KDACs) that are Zn2+- or NAD+-dependent. In this study, we reported a protein, AhCobQ, in Aeromonas hydrophila ATCC 7966 that presents NAD+- and Zn2+-independent KDAC activity. Furthermore, its KDAC activity is located in an unidentified domain (from 195 to 245 aa). Interestingly, AhCobQ has no homology with current known KDACs, and no homologous protein was found in eukaryotic cells. A protein substrate analysis showed that AhCobQ has specific protein substrates in common with other known KDACs, indicating that these KDACs can dynamically co-regulate the states of Kac proteins. Microbiological methods employed in this study affirmed AhCobQ’s positive regulation of isocitrate dehydrogenase (ICD) enzymatic activity at the K388 site, implicating AhCobQ in the modulation of bacterial enzymatic activities. In summary, our findings present compelling evidence that AhCobQ represents a distinctive type of KDAC with significant roles in bacterial biological functions.