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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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2020-08-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.01153-20 |
| _version_ | 1818856653356793856 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-19T08:27:55Z |
| format | Article |
| id | doaj.art-2bd350a309584094b4aca6b2f0a81b7f |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-19T08:27:55Z |
| publishDate | 2020-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-2bd350a309584094b4aca6b2f0a81b7f2022-12-21T20:29:15ZengAmerican Society for MicrobiologymBio2150-75112020-08-0111410.1128/mBio.01153-20The <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>Thomas Dubois0Frederic Krzewinski1Nao Yamakawa2Christelle Lemy3Audrey Hamiot4Loïc Brunet5Anne-Sophie Lacoste6Yuryi Knirel7Yann Guerardel8Christine Faille9University Lille, CNRS, INRAE, Centrale Lille, UMR 8207—UMET—Unité Matériaux et Transformations, Lille, FranceUniversity Lille, CNRS, UMR 8576—UGSF—Unité de Glycobiologie Structurale et Fonctionnelle, Lille, FranceUniversity Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, US 41—UMS 2014—PLBS, Lille, FranceUniversity Lille, CNRS, INRAE, Centrale Lille, UMR 8207—UMET—Unité Matériaux et Transformations, Lille, FranceUniversity Lille, CNRS, INRAE, Centrale Lille, UMR 8207—UMET—Unité Matériaux et Transformations, Lille, FranceUniversity Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, US 41—UMS 2014—PLBS, Lille, FranceUniversity Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, US 41—UMS 2014—PLBS, Lille, FranceN.D. Zelinsky Institute of Organic Chemistry, Russian Academy of Sciences, Moscow, RussiaUniversity Lille, CNRS, UMR 8576—UGSF—Unité de Glycobiologie Structurale et Fonctionnelle, Lille, FranceUniversity Lille, CNRS, INRAE, Centrale Lille, UMR 8207—UMET—Unité Matériaux et Transformations, Lille, FranceABSTRACT 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.https://journals.asm.org/doi/10.1128/mBio.01153-20Bacillus subtilisbacterial adhesioncrustlegionaminic acidnonulosonic acidspores |
| spellingShingle | 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> mBio Bacillus subtilis bacterial adhesion crust legionaminic acid nonulosonic acid spores |
| 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_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_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_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 |
| topic | Bacillus subtilis bacterial adhesion crust legionaminic acid nonulosonic acid spores |
| url | https://journals.asm.org/doi/10.1128/mBio.01153-20 |
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