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Structure of the Bacterial Cellulose Ribbon and Its Assembly-Guiding Cytoskeleton by Electron Cryotomography

Nicolas, William J. and Ghosal, Debnath and Tocheva, Elitza I. and Meyerowitz, Elliot M. and Jensen, Grant J. (2021) Structure of the Bacterial Cellulose Ribbon and Its Assembly-Guiding Cytoskeleton by Electron Cryotomography. Journal of Bacteriology, 203 (3). Art. No. e00371-20. ISSN 0021-9193. PMCID PMC7811197. https://resolver.caltech.edu/CaltechAUTHORS:20200417-145045074

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Abstract

Cellulose is a widespread component of bacterial biofilms, where its properties of exceptional water retention, high tensile strength, and stiffness prevent dehydration and mechanical disruption of the biofilm. Bacteria in the genus Gluconacetobacter secrete crystalline cellulose, with a structure very similar to that found in plant cell walls. How this higher-order structure is produced is poorly understood. We used cryo-electron tomography and focused-ion-beam milling of native bacterial biofilms to image cellulose-synthesizing Gluconacetobacter hansenii and Gluconacetobacter xylinus bacteria in a frozen-hydrated, near-native state. We confirm previous results suggesting that cellulose crystallization occurs serially following its secretion along one side of the cell, leading to a cellulose ribbon that can reach several micrometers in length and combine with ribbons from other cells to form a robust biofilm matrix. We were able to take direct measurements in a near-native state of the cellulose sheets. Our results also reveal a novel cytoskeletal structure, which we have named the cortical belt, adjacent to the inner membrane and underlying the sites where cellulose is seen emerging from the cell. We found that this structure is not present in other cellulose-synthesizing bacterial species, Agrobacterium tumefaciens and Escherichia coli 1094, which do not produce organized cellulose ribbons. We therefore propose that the cortical belt holds the cellulose synthase complexes in a line to form higher-order cellulose structures, such as sheets and ribbons.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1128/JB.00371-20DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc7811197/PubMed CentralArticle
https://doi.org/10.1101/2020.04.16.045534DOIDiscussion Paper
ORCID:
AuthorORCID
Nicolas, William J.0000-0001-5970-8626
Ghosal, Debnath0000-0002-2227-0330
Tocheva, Elitza I.0000-0002-4869-8319
Meyerowitz, Elliot M.0000-0003-4798-5153
Jensen, Grant J.0000-0003-1556-4864
Additional Information:© 2020 Nicolas et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Received 29 June 2020; Accepted 26 October 2020; Accepted manuscript posted online 16 November 2020; Published 11 January 2021. This work was supported by NIH grant R35-GM122588 to G.J.J., the Howard Hughes Medical Institute (HHMI), and the Center for Environmental Microbial Interactions (CEMI) pilot grant program. Cryo-electron microscopy was performed in the Beckman Institute Resource Center for Transmission Electron Microscopy at Caltech. We thank Jean Marc Ghigo for kindly providing us the E. coli 1094 strain. Special acknowledgments go to Catherine Oikonomou for all the help and scientific advice given during this study and also to Candace Haigler for sharing her thoughts and her precious experience on the not so common Gluconacetobacter spp. We declare that there are no conflicts of interest.
Group:Caltech Center for Environmental Microbial Interactions (CEMI)
Funders:
Funding AgencyGrant Number
NIHR35-GM122588
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
Subject Keywords:cellulose, Gluconacetobacter, electron cryotomography
Issue or Number:3
PubMed Central ID:PMC7811197
Record Number:CaltechAUTHORS:20200417-145045074
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200417-145045074
Official Citation:Structure of the Bacterial Cellulose Ribbon and Its Assembly-Guiding Cytoskeleton by Electron Cryotomography. William J. Nicolas, Debnath Ghosal, Elitza I. Tocheva, Elliot M. Meyerowitz, Grant J. Jensen. Journal of Bacteriology Jan 2021, 203 (3) e00371-20; DOI: 10.1128/JB.00371-20
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:102640
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:17 Apr 2020 22:08
Last Modified:03 Mar 2021 21:42

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