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Genetics and Molecular Biology

Multilamellar and Multivesicular Outer Membrane Vesicles Produced by a Buttiauxella agrestis tolB Mutant

Kotaro Takaki, Yuhei O. Tahara, Nao Nakamichi, Yusuke Hasegawa, Masaki Shintani, Moriya Ohkuma, Makoto Miyata, Hiroyuki Futamata, Yosuke Tashiro
Maia Kivisaar, Editor
Kotaro Takaki
aDepartment of Engineering, Graduate School of Integrated Science and Technology, Shizuoka University, Hamamatsu, Japan
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Yuhei O. Tahara
bGraduate School of Science, Osaka City University, Osaka, Japan
cThe OCU Advanced Research Institute for Natural Science and Technology (OCARINA), Osaka City University, Osaka, Japan
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Nao Nakamichi
aDepartment of Engineering, Graduate School of Integrated Science and Technology, Shizuoka University, Hamamatsu, Japan
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Yusuke Hasegawa
aDepartment of Engineering, Graduate School of Integrated Science and Technology, Shizuoka University, Hamamatsu, Japan
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Masaki Shintani
aDepartment of Engineering, Graduate School of Integrated Science and Technology, Shizuoka University, Hamamatsu, Japan
dGraduate School of Science and Technology, Shizuoka University, Hamamatsu, Japan
eResearch Institute of Green Science and Technology, Shizuoka University, Shizuoka, Japan
fJapan Collection of Microorganisms, RIKEN BioResource Research Center, Tsukuba, Japan
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  • ORCID record for Masaki Shintani
Moriya Ohkuma
fJapan Collection of Microorganisms, RIKEN BioResource Research Center, Tsukuba, Japan
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Makoto Miyata
bGraduate School of Science, Osaka City University, Osaka, Japan
cThe OCU Advanced Research Institute for Natural Science and Technology (OCARINA), Osaka City University, Osaka, Japan
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Hiroyuki Futamata
aDepartment of Engineering, Graduate School of Integrated Science and Technology, Shizuoka University, Hamamatsu, Japan
dGraduate School of Science and Technology, Shizuoka University, Hamamatsu, Japan
eResearch Institute of Green Science and Technology, Shizuoka University, Shizuoka, Japan
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Yosuke Tashiro
aDepartment of Engineering, Graduate School of Integrated Science and Technology, Shizuoka University, Hamamatsu, Japan
dGraduate School of Science and Technology, Shizuoka University, Hamamatsu, Japan
gJST PRESTO, Kawaguchi, Japan
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Maia Kivisaar
University of Tartu
Roles: Editor
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DOI: 10.1128/AEM.01131-20
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ABSTRACT

Outer membrane vesicles (OMVs) are naturally released from Gram-negative bacteria and play important roles in various biological functions. Released vesicles are not uniform in shape, size, or characteristics, and little is known about this diversity of OMVs. Here, we show that deletion of tolB, which encodes a part of the Tol-Pal system, leads to the production of multiple types of vesicles and increases overall vesicle production in the high-vesicle-forming Buttiauxella agrestis type strain JCM 1090. The ΔtolB mutant produced small OMVs and multilamellar/multivesicular OMVs (M-OMVs) as well as vesicles with a striking similarity to the wild type. M-OMVs, previously undescribed, contained triple-lamellar membrane vesicles and multiple vesicle-incorporating vesicles. Ultracentrifugation enabled the separation and purification of each type of OMV released from the ΔtolB mutant, and visualization by quick-freeze deep-etch and replica electron microscopy indicated that M-OMVs are composed of several lamellar membranes. Visualization of intracellular compartments of ΔtolB mutant cells showed that vesicles were accumulated in the broad periplasm, which is probably due to the low linkage between the outer and inner membranes attributed to the Tol-Pal defect. The outer membrane was invaginating inward by wrapping a vesicle, and the precursor of M-OMVs existed in the cell. Thus, we demonstrated a novel type of bacterial OMV and showed that unconventional processes enable the B. agrestis ΔtolB mutant to form unique vesicles.

IMPORTANCE Membrane vesicle (MV) formation has been recognized as a common mechanism in prokaryotes, and MVs play critical roles in intercellular interaction. However, a broad range of MV types and their multiple production processes make it difficult to gain a comprehensive understanding of MVs. In this work, using vesicle separation and electron microscopic analyses, we demonstrated that diverse types of outer membrane vesicles (OMVs) were released from an engineered strain, Buttiauxella agrestis JCM 1090T ΔtolB mutant. We also discovered a previously undiscovered type of vesicle, multilamellar/multivesicular outer membrane vesicles (M-OMVs), which were released by this mutant using unconventional processes. These findings have facilitated considerable progress in understanding MV diversity and expanding the utility of MVs in biotechnological applications.

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Multilamellar and Multivesicular Outer Membrane Vesicles Produced by a Buttiauxella agrestis tolB Mutant
Kotaro Takaki, Yuhei O. Tahara, Nao Nakamichi, Yusuke Hasegawa, Masaki Shintani, Moriya Ohkuma, Makoto Miyata, Hiroyuki Futamata, Yosuke Tashiro
Applied and Environmental Microbiology Oct 2020, 86 (20) e01131-20; DOI: 10.1128/AEM.01131-20

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Multilamellar and Multivesicular Outer Membrane Vesicles Produced by a Buttiauxella agrestis tolB Mutant
Kotaro Takaki, Yuhei O. Tahara, Nao Nakamichi, Yusuke Hasegawa, Masaki Shintani, Moriya Ohkuma, Makoto Miyata, Hiroyuki Futamata, Yosuke Tashiro
Applied and Environmental Microbiology Oct 2020, 86 (20) e01131-20; DOI: 10.1128/AEM.01131-20
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KEYWORDS

membrane vesicles
OMV
quick-freeze deep-etch and replica electron microscopy
TolB

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