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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. (2020) Structure of the bacterial cellulose ribbon and its assembly-guiding cytoskeleton by electron cryotomography. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20200417-145045074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 prevents dehydration and mechanical disruption of the biofilm. Bacteria in the Gluconacetobacter genus 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 G. hansenii and G. 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 microns 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, that we name the cortical belt, adjacent to the inner membrane and underlying the sites where cellulose is seen emerging from the cell. We find 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:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
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:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. Posted April 17, 2020. This work was supported by NIH grant R35-GM122588 to GJJ, 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 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. The authors 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
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. bioRxiv 2020.04.16.045534; doi: https://doi.org/10.1101/2020.04.16.045534
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:23 Apr 2020 18:44

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