Bacterial crystalline cellulose secretion via a supramolecular BcsHD scaffold

Author:

Abidi Wiem123ORCID,Decossas Marion12ORCID,Torres-Sánchez Lucía123ORCID,Puygrenier Lucie2,Létoffé Sylvie4,Ghigo Jean-Marc4ORCID,Krasteva Petya V.12ORCID

Affiliation:

1. Université de Bordeaux, CNRS, Bordeaux INP, CBMN, UMR 5248, Pessac, France.

2. ‘Structural Biology of Biofilms’ Group, European Institute of Chemistry and Biology (IECB), Pessac, France.

3. Doctoral School of Therapeutic Innovation ITFA, Université Paris-Saclay, Orsay, France.

4. Institut Pasteur, Université de Paris, UMR CNRS2001, ‘Genetics of Biofilms’ laboratory, 25-28 rue du Docteur Roux, 75015 Paris, France.

Abstract

Cellulose, the most abundant biopolymer on Earth, is not only the predominant constituent of plants but also a key extracellular polysaccharide in the biofilms of many bacterial species. Depending on the producers, chemical modifications, and three-dimensional assemblies, bacterial cellulose (BC) can present diverse degrees of crystallinity. Highly ordered, or crystalline, cellulose presents great economical relevance due to its ever-growing number of biotechnological applications. Even if some acetic acid bacteria have long been identified as BC superproducers, the molecular mechanisms determining the secretion of crystalline versus amorphous cellulose remain largely unknown. Here, we present structural and mechanistic insights into the role of the accessory subunits BcsH (CcpAx) and BcsD (CesD) that determine crystalline BC secretion in the Gluconacetobacter lineage. We show that oligomeric BcsH drives the assembly of BcsD into a supramolecular cytoskeletal scaffold that likely stabilizes the cellulose-extruding synthase nanoarrays through an unexpected inside-out mechanism for secretion system assembly.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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