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Environmental Microbiology | Spotlight

Extracellular Vesicles Produced by Bifidobacterium longum Export Mucin-Binding Proteins

Keita Nishiyama, Takashi Takaki, Makoto Sugiyama, Itsuko Fukuda, Maho Aiso, Takao Mukai, Toshitaka Odamaki, Jin-zhong Xiao, Ro Osawa, Nobuhiko Okada
Danilo Ercolini, Editor
Keita Nishiyama
aDepartment of Microbiology, School of Pharmacy, Kitasato University, Tokyo, Japan
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  • ORCID record for Keita Nishiyama
Takashi Takaki
bSection of Electron Microscopy, Showa University, Tokyo, Japan
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Makoto Sugiyama
cLaboratory of Veterinary Anatomy, School of Veterinary Medicine, Kitasato University, Towada, Aomori, Japan
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Itsuko Fukuda
dResearch Center for Food Safety and Security, Graduate School of Agricultural Science, Kobe University, Kobe, Hyogo, Japan
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Maho Aiso
eDepartment of Animal Science, School of Veterinary Medicine, Kitasato University, Towada, Aomori, Japan
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Takao Mukai
eDepartment of Animal Science, School of Veterinary Medicine, Kitasato University, Towada, Aomori, Japan
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Toshitaka Odamaki
fNext Generation Science Institute, Morinaga Milk Industry Co., Ltd., Zama, Kanagawa, Japan
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Jin-zhong Xiao
fNext Generation Science Institute, Morinaga Milk Industry Co., Ltd., Zama, Kanagawa, Japan
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Ro Osawa
dResearch Center for Food Safety and Security, Graduate School of Agricultural Science, Kobe University, Kobe, Hyogo, Japan
gDepartment of Bioresource Science, Graduate School of Agricultural Science, Kobe University, Kobe, Hyogo, Japan
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Nobuhiko Okada
aDepartment of Microbiology, School of Pharmacy, Kitasato University, Tokyo, Japan
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Danilo Ercolini
University of Naples Federico II
Roles: Editor
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DOI: 10.1128/AEM.01464-20
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ABSTRACT

Extracellular proteins are important factors in host-microbe interactions; however, the specific factors that enable bifidobacterial adhesion and survival in the gastrointestinal (GI) tract are not fully characterized. Here, we discovered that Bifidobacterium longum NCC2705 cultured in bacterium-free supernatants of human fecal fermentation broth released a myriad of particles into the extracellular environment. The aim of this study was to characterize the physiological properties of these extracellular particles. The particles, approximately 50 to 80 nm in diameter, had high protein and double-stranded DNA contents, suggesting that they were extracellular vesicles (EVs). A proteomic analysis showed that the EVs primarily consisted of cytoplasmic proteins with crucial functions in essential cellular processes. We identified several mucin-binding proteins by performing a biomolecular interaction analysis of phosphoketolase, GroEL, elongation factor Tu (EF-Tu), phosphoglycerate kinase, transaldolase (Tal), and heat shock protein 20 (Hsp20). The recombinant GroEL and Tal proteins showed high binding affinities to mucin. Furthermore, the immobilization of these proteins on microbeads affected the permanence of the microbeads in the murine GI tract. These results suggest that bifidobacterial exposure conditions that mimic the intestine stimulate B. longum EV production. The resulting EVs exported several cytoplasmic proteins that may have promoted B. longum adhesion. This study improved our understanding of the Bifidobacterium colonization strategy in the intestinal microbiome.

IMPORTANCE Bifidobacterium is a natural inhabitant of the human gastrointestinal (GI) tract. Morphological observations revealed that extracellular appendages of bifidobacteria in complex microbial communities are important for understanding its adaptations to the GI tract environment. We identified dynamic extracellular vesicle (EV) production by Bifidobacterium longum in bacterium-free fecal fermentation broth that was strongly suggestive of differing bifidobacterial extracellular appendages in the GI tract. In addition, export of the adhesive moonlighting proteins mediated by EVs may promote bifidobacterial colonization. This study provides new insight into the roles of EVs in bifidobacterial colonization processes as these bacteria adapt to the GI environment.

FOOTNOTES

    • Received 26 June 2020.
    • Accepted 29 July 2020.
    • Accepted manuscript posted online 31 July 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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Extracellular Vesicles Produced by Bifidobacterium longum Export Mucin-Binding Proteins
Keita Nishiyama, Takashi Takaki, Makoto Sugiyama, Itsuko Fukuda, Maho Aiso, Takao Mukai, Toshitaka Odamaki, Jin-zhong Xiao, Ro Osawa, Nobuhiko Okada
Applied and Environmental Microbiology Sep 2020, 86 (19) e01464-20; DOI: 10.1128/AEM.01464-20

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Extracellular Vesicles Produced by Bifidobacterium longum Export Mucin-Binding Proteins
Keita Nishiyama, Takashi Takaki, Makoto Sugiyama, Itsuko Fukuda, Maho Aiso, Takao Mukai, Toshitaka Odamaki, Jin-zhong Xiao, Ro Osawa, Nobuhiko Okada
Applied and Environmental Microbiology Sep 2020, 86 (19) e01464-20; DOI: 10.1128/AEM.01464-20
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KEYWORDS

Bifidobacterium
adhesion
colonization
extracellular vesicle
fecal fermentation
symbiosis

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