Nanoscale resolution of microbial fiber degradation in action

Abstract
Data availability
Article and author information
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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

1. Tatli M
2. Morais S
3. Tovar-Herrera OE
4. Bomble YJ
5. Bayer EA
6. Medalia O
7. Mizrahi I
(2021) Cryo-EM structure of exoglucanase Cel48S
Electron Microscopy Data Bank, EMD-11986.

https://www.ebi.ac.uk/emdb/EMD-11986
1. Tatli M
2. Moraïs S
3. Tovar-Herrera OE
4. Bomble Y
5. Bayer EA
6. Medalia O
7. Mizrahi I
(2022) Nanoscale view of the Clostridium thermocellum cellulosome during cellulose degradation reveals an ecological strategy leading to phenotypic heterogeneity
EMPIAR, EMPIAR-10593.

https://www.ebi.ac.uk/empiar/EMPIAR-10593/

Article and author information

Author details

Meltem Tatli

Department of Biochemistry, University of Zurich, Zurich, Switzerland

Competing interests
The authors declare that no competing interests exist.
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.
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.
Yannick J Bomble

National Renewable Energy Laboratory, Golden, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7624-8000
Edward A Bayer

Department of Biomolecular Sciences, Weizmann Institute of Science, Rehovot, Israel

Competing interests
The authors declare that no competing interests exist.
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.

"This ORCID iD identifies the author of this article:" 0000-0003-0994-2937
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.

"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.