Layered Structure and Complex Mechanochemistry Underlie Strength and Versatility in a Bacterial Adhesive

ABSTRACT While designing synthetic adhesives that perform in aqueous environments has proven challenging, microorganisms commonly produce bioadhesives that efficiently attach to a variety of substrates, including wet surfaces. The aquatic bacterium Caulobacter crescentus uses a discrete polysacchari...

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Auteurs principaux:	Mercedes Hernando-Pérez, Sima Setayeshgar, Yifeng Hou, Roger Temam, Yves V. Brun, Bogdan Dragnea, Cécile Berne
Format:	article
Langue:	EN
Publié:	American Society for Microbiology 2018
Sujets:	atomic force microscopy bacterial adhesion bioadhesive Caulobacter crescentus holdfast Microbiology QR1-502
Accès en ligne:	https://doaj.org/article/a5248ecc11a645ebb6e86f8525517de6
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spelling	oai:doaj.org-article:a5248ecc11a645ebb6e86f8525517de62021-11-15T15:53:26ZLayered Structure and Complex Mechanochemistry Underlie Strength and Versatility in a Bacterial Adhesive10.1128/mBio.02359-172150-7511https://doaj.org/article/a5248ecc11a645ebb6e86f8525517de62018-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02359-17https://doaj.org/toc/2150-7511ABSTRACT While designing synthetic adhesives that perform in aqueous environments has proven challenging, microorganisms commonly produce bioadhesives that efficiently attach to a variety of substrates, including wet surfaces. The aquatic bacterium Caulobacter crescentus uses a discrete polysaccharide complex, the holdfast, to strongly attach to surfaces and resist flow. The holdfast is extremely versatile and has impressive adhesive strength. Here, we used atomic force microscopy in conjunction with superresolution microscopy and enzymatic assays to unravel the complex structure of the holdfast and to characterize its chemical constituents and their role in adhesion. Our data support a model whereby the holdfast is a heterogeneous material organized as two layers: a stiffer nanoscopic core layer wrapped into a sparse, far-reaching, flexible brush layer. Moreover, we found that the elastic response of the holdfast evolves after surface contact from initially heterogeneous to more homogeneous. From a composition point of view, besides N-acetyl-d-glucosamine (NAG), the only component that had been identified to date, our data show that the holdfast contains peptides and DNA. We hypothesize that, while polypeptides are the most important components for adhesive force, the presence of DNA mainly impacts the brush layer and the strength of initial adhesion, with NAG playing a primarily structural role within the core. The unanticipated complexity of both the structure and composition of the holdfast likely underlies its versatility as a wet adhesive and its distinctive strength. Continued improvements in understanding of the mechanochemistry of this bioadhesive could provide new insights into how bacteria attach to surfaces and could inform the development of new adhesives. IMPORTANCE There is an urgent need for strong, biocompatible bioadhesives that perform underwater. To strongly adhere to surfaces and resist flow underwater, the bacterium Caulobacter crescentus produces an adhesive called the holdfast, the mechanochemistry of which remains undefined. We show that the holdfast is a layered structure with a stiff core layer and a polymeric brush layer and consists of polysaccharides, polypeptides, and DNA. The DNA appears to play a role in the structure of the brush layer and initial adhesion, the peptides in adhesive strength, and the polysaccharides in the structure of the core. The complex, multilayer organization and diverse chemistry described here underlie the distinctive adhesive properties of the holdfast and will provide important insights into the mechanisms of bacterial adhesion and bioadhesive applications.Mercedes Hernando-PérezSima SetayeshgarYifeng HouRoger TemamYves V. BrunBogdan DragneaCécile BerneAmerican Society for Microbiologyarticleatomic force microscopybacterial adhesionbioadhesiveCaulobacter crescentusholdfastMicrobiologyQR1-502ENmBio, Vol 9, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	atomic force microscopy bacterial adhesion bioadhesive Caulobacter crescentus holdfast Microbiology QR1-502
spellingShingle	atomic force microscopy bacterial adhesion bioadhesive Caulobacter crescentus holdfast Microbiology QR1-502 Mercedes Hernando-Pérez Sima Setayeshgar Yifeng Hou Roger Temam Yves V. Brun Bogdan Dragnea Cécile Berne Layered Structure and Complex Mechanochemistry Underlie Strength and Versatility in a Bacterial Adhesive
description	ABSTRACT While designing synthetic adhesives that perform in aqueous environments has proven challenging, microorganisms commonly produce bioadhesives that efficiently attach to a variety of substrates, including wet surfaces. The aquatic bacterium Caulobacter crescentus uses a discrete polysaccharide complex, the holdfast, to strongly attach to surfaces and resist flow. The holdfast is extremely versatile and has impressive adhesive strength. Here, we used atomic force microscopy in conjunction with superresolution microscopy and enzymatic assays to unravel the complex structure of the holdfast and to characterize its chemical constituents and their role in adhesion. Our data support a model whereby the holdfast is a heterogeneous material organized as two layers: a stiffer nanoscopic core layer wrapped into a sparse, far-reaching, flexible brush layer. Moreover, we found that the elastic response of the holdfast evolves after surface contact from initially heterogeneous to more homogeneous. From a composition point of view, besides N-acetyl-d-glucosamine (NAG), the only component that had been identified to date, our data show that the holdfast contains peptides and DNA. We hypothesize that, while polypeptides are the most important components for adhesive force, the presence of DNA mainly impacts the brush layer and the strength of initial adhesion, with NAG playing a primarily structural role within the core. The unanticipated complexity of both the structure and composition of the holdfast likely underlies its versatility as a wet adhesive and its distinctive strength. Continued improvements in understanding of the mechanochemistry of this bioadhesive could provide new insights into how bacteria attach to surfaces and could inform the development of new adhesives. IMPORTANCE There is an urgent need for strong, biocompatible bioadhesives that perform underwater. To strongly adhere to surfaces and resist flow underwater, the bacterium Caulobacter crescentus produces an adhesive called the holdfast, the mechanochemistry of which remains undefined. We show that the holdfast is a layered structure with a stiff core layer and a polymeric brush layer and consists of polysaccharides, polypeptides, and DNA. The DNA appears to play a role in the structure of the brush layer and initial adhesion, the peptides in adhesive strength, and the polysaccharides in the structure of the core. The complex, multilayer organization and diverse chemistry described here underlie the distinctive adhesive properties of the holdfast and will provide important insights into the mechanisms of bacterial adhesion and bioadhesive applications.
format	article
author	Mercedes Hernando-Pérez Sima Setayeshgar Yifeng Hou Roger Temam Yves V. Brun Bogdan Dragnea Cécile Berne
author_facet	Mercedes Hernando-Pérez Sima Setayeshgar Yifeng Hou Roger Temam Yves V. Brun Bogdan Dragnea Cécile Berne
author_sort	Mercedes Hernando-Pérez
title	Layered Structure and Complex Mechanochemistry Underlie Strength and Versatility in a Bacterial Adhesive
title_short	Layered Structure and Complex Mechanochemistry Underlie Strength and Versatility in a Bacterial Adhesive
title_full	Layered Structure and Complex Mechanochemistry Underlie Strength and Versatility in a Bacterial Adhesive
title_fullStr	Layered Structure and Complex Mechanochemistry Underlie Strength and Versatility in a Bacterial Adhesive
title_full_unstemmed	Layered Structure and Complex Mechanochemistry Underlie Strength and Versatility in a Bacterial Adhesive
title_sort	layered structure and complex mechanochemistry underlie strength and versatility in a bacterial adhesive
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/a5248ecc11a645ebb6e86f8525517de6
work_keys_str_mv	AT mercedeshernandoperez layeredstructureandcomplexmechanochemistryunderliestrengthandversatilityinabacterialadhesive AT simasetayeshgar layeredstructureandcomplexmechanochemistryunderliestrengthandversatilityinabacterialadhesive AT yifenghou layeredstructureandcomplexmechanochemistryunderliestrengthandversatilityinabacterialadhesive AT rogertemam layeredstructureandcomplexmechanochemistryunderliestrengthandversatilityinabacterialadhesive AT yvesvbrun layeredstructureandcomplexmechanochemistryunderliestrengthandversatilityinabacterialadhesive AT bogdandragnea layeredstructureandcomplexmechanochemistryunderliestrengthandversatilityinabacterialadhesive AT cecileberne layeredstructureandcomplexmechanochemistryunderliestrengthandversatilityinabacterialadhesive
_version_	1718427293852893184

Layered Structure and Complex Mechanochemistry Underlie Strength and Versatility in a Bacterial Adhesive

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