The <italic toggle="yes">sps</italic> Genes Encode an Original Legionaminic Acid Pathway Required for Crust Assembly in <named-content content-type="genus-species">Bacillus subtilis</named-content>

ABSTRACT The crust is the outermost spore layer of most Bacillus strains devoid of an exosporium. This outermost layer, composed of both proteins and carbohydrates, plays a major role in the adhesion and spreading of spores into the environment. Recent studies have identified several crust proteins...

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Autores principales:	Thomas Dubois, Frederic Krzewinski, Nao Yamakawa, Christelle Lemy, Audrey Hamiot, Loïc Brunet, Anne-Sophie Lacoste, Yuryi Knirel, Yann Guerardel, Christine Faille
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Bacillus subtilis bacterial adhesion crust legionaminic acid nonulosonic acid spores Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2bd350a309584094b4aca6b2f0a81b7f
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spelling	oai:doaj.org-article:2bd350a309584094b4aca6b2f0a81b7f2021-11-15T15:56:43ZThe <italic toggle="yes">sps</italic> Genes Encode an Original Legionaminic Acid Pathway Required for Crust Assembly in <named-content content-type="genus-species">Bacillus subtilis</named-content>10.1128/mBio.01153-202150-7511https://doaj.org/article/2bd350a309584094b4aca6b2f0a81b7f2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01153-20https://doaj.org/toc/2150-7511ABSTRACT The crust is the outermost spore layer of most Bacillus strains devoid of an exosporium. This outermost layer, composed of both proteins and carbohydrates, plays a major role in the adhesion and spreading of spores into the environment. Recent studies have identified several crust proteins and have provided insights about their organization at the spore surface. However, although carbohydrates are known to participate in adhesion, little is known about their composition, structure, and localization. In this study, we showed that the spore surface of Bacillus subtilis is covered with legionaminic acid (Leg), a nine-carbon backbone nonulosonic acid known to decorate the flagellin of the human pathogens Helicobacter pylori and Campylobacter jejuni. We demonstrated that the spsC, spsD, spsE, spsG, and spsM genes of Bacillus subtilis are required for Leg biosynthesis during sporulation, while the spsF gene is required for Leg transfer from the mother cell to the surface of the forespore. We also characterized the activity of SpsM and highlighted an original Leg biosynthesis pathway in B. subtilis. Finally, we demonstrated that Leg is required for the assembly of the crust around the spores, and we showed that in the absence of Leg, spores were more adherent to stainless steel probably because of their reduced hydrophilicity and charge. IMPORTANCE Bacillus species are a major economic and food safety concern of the food industry because of their food spoilage-causing capability and persistence. Their persistence is mainly due to their ability to form highly resistant spores adhering to the surfaces of industrial equipment. Spores of the Bacillus subtilis group are surrounded by the crust, a superficial layer which plays a key role in their adhesion properties. However, knowledge of the composition and structure of this layer remains incomplete. Here, for the first time, we identified a nonulosonic acid (Leg) at the surfaces of bacterial spores (B. subtilis). We uncovered a novel Leg biosynthesis pathway, and we demonstrated that Leg is required for proper crust assembly. This work contributes to the description of the structure and composition of Bacillus spores which has been under way for decades, and it provides keys to understanding the importance of carbohydrates in Bacillus adhesion and persistence in the food industry.Thomas DuboisFrederic KrzewinskiNao YamakawaChristelle LemyAudrey HamiotLoïc BrunetAnne-Sophie LacosteYuryi KnirelYann GuerardelChristine FailleAmerican Society for MicrobiologyarticleBacillus subtilisbacterial adhesioncrustlegionaminic acidnonulosonic acidsporesMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacillus subtilis bacterial adhesion crust legionaminic acid nonulosonic acid spores Microbiology QR1-502
spellingShingle	Bacillus subtilis bacterial adhesion crust legionaminic acid nonulosonic acid spores Microbiology QR1-502 Thomas Dubois Frederic Krzewinski Nao Yamakawa Christelle Lemy Audrey Hamiot Loïc Brunet Anne-Sophie Lacoste Yuryi Knirel Yann Guerardel Christine Faille The <italic toggle="yes">sps</italic> Genes Encode an Original Legionaminic Acid Pathway Required for Crust Assembly in <named-content content-type="genus-species">Bacillus subtilis</named-content>
description	ABSTRACT The crust is the outermost spore layer of most Bacillus strains devoid of an exosporium. This outermost layer, composed of both proteins and carbohydrates, plays a major role in the adhesion and spreading of spores into the environment. Recent studies have identified several crust proteins and have provided insights about their organization at the spore surface. However, although carbohydrates are known to participate in adhesion, little is known about their composition, structure, and localization. In this study, we showed that the spore surface of Bacillus subtilis is covered with legionaminic acid (Leg), a nine-carbon backbone nonulosonic acid known to decorate the flagellin of the human pathogens Helicobacter pylori and Campylobacter jejuni. We demonstrated that the spsC, spsD, spsE, spsG, and spsM genes of Bacillus subtilis are required for Leg biosynthesis during sporulation, while the spsF gene is required for Leg transfer from the mother cell to the surface of the forespore. We also characterized the activity of SpsM and highlighted an original Leg biosynthesis pathway in B. subtilis. Finally, we demonstrated that Leg is required for the assembly of the crust around the spores, and we showed that in the absence of Leg, spores were more adherent to stainless steel probably because of their reduced hydrophilicity and charge. IMPORTANCE Bacillus species are a major economic and food safety concern of the food industry because of their food spoilage-causing capability and persistence. Their persistence is mainly due to their ability to form highly resistant spores adhering to the surfaces of industrial equipment. Spores of the Bacillus subtilis group are surrounded by the crust, a superficial layer which plays a key role in their adhesion properties. However, knowledge of the composition and structure of this layer remains incomplete. Here, for the first time, we identified a nonulosonic acid (Leg) at the surfaces of bacterial spores (B. subtilis). We uncovered a novel Leg biosynthesis pathway, and we demonstrated that Leg is required for proper crust assembly. This work contributes to the description of the structure and composition of Bacillus spores which has been under way for decades, and it provides keys to understanding the importance of carbohydrates in Bacillus adhesion and persistence in the food industry.
format	article
author	Thomas Dubois Frederic Krzewinski Nao Yamakawa Christelle Lemy Audrey Hamiot Loïc Brunet Anne-Sophie Lacoste Yuryi Knirel Yann Guerardel Christine Faille
author_facet	Thomas Dubois Frederic Krzewinski Nao Yamakawa Christelle Lemy Audrey Hamiot Loïc Brunet Anne-Sophie Lacoste Yuryi Knirel Yann Guerardel Christine Faille
author_sort	Thomas Dubois
title	The <italic toggle="yes">sps</italic> Genes Encode an Original Legionaminic Acid Pathway Required for Crust Assembly in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_short	The <italic toggle="yes">sps</italic> Genes Encode an Original Legionaminic Acid Pathway Required for Crust Assembly in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_full	The <italic toggle="yes">sps</italic> Genes Encode an Original Legionaminic Acid Pathway Required for Crust Assembly in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_fullStr	The <italic toggle="yes">sps</italic> Genes Encode an Original Legionaminic Acid Pathway Required for Crust Assembly in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_full_unstemmed	The <italic toggle="yes">sps</italic> Genes Encode an Original Legionaminic Acid Pathway Required for Crust Assembly in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_sort	<italic toggle="yes">sps</italic> genes encode an original legionaminic acid pathway required for crust assembly in <named-content content-type="genus-species">bacillus subtilis</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/2bd350a309584094b4aca6b2f0a81b7f
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The <italic toggle="yes">sps</italic> Genes Encode an Original Legionaminic Acid Pathway Required for Crust Assembly in <named-content content-type="genus-species">Bacillus subtilis</named-content>

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