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Interaction of Bacterial Membrane Vesicles with Specific Species and Their Potential for Delivery to Target Cells

Membrane vesicles (MVs) are secreted from a wide range of microbial species and transfer their content to other cells. Although MVs play critical roles in bacterial communication, whether MVs selectively interact with bacterial cells in microbial communities is unclear. In this study, we investigate...

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Autores principales: Tashiro, Yosuke, Hasegawa, Yusuke, Shintani, Masaki, Takaki, Kotaro, Ohkuma, Moriya, Kimbara, Kazuhide, Futamata, Hiroyuki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5383704/
https://www.ncbi.nlm.nih.gov/pubmed/28439261
http://dx.doi.org/10.3389/fmicb.2017.00571
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author Tashiro, Yosuke
Hasegawa, Yusuke
Shintani, Masaki
Takaki, Kotaro
Ohkuma, Moriya
Kimbara, Kazuhide
Futamata, Hiroyuki
author_facet Tashiro, Yosuke
Hasegawa, Yusuke
Shintani, Masaki
Takaki, Kotaro
Ohkuma, Moriya
Kimbara, Kazuhide
Futamata, Hiroyuki
author_sort Tashiro, Yosuke
collection PubMed
description Membrane vesicles (MVs) are secreted from a wide range of microbial species and transfer their content to other cells. Although MVs play critical roles in bacterial communication, whether MVs selectively interact with bacterial cells in microbial communities is unclear. In this study, we investigated the specificity of the MV-cell interactions and evaluated the potential of MVs to target bacterial cells for delivery. MV association with bacterial cells was examined using a fluorescent membrane dye to label MVs. MVs derived from the enterobacterium Buttiauxella agrestis specifically interacted with cells of the parent strain but interacted less specifically with those of other genera tested in this study. Electron microscopic analyses showed that MVs were not only attached on B. agrestis cells but also fused to them. The interaction energy, which was characterized by hydrodynamic diameter and zeta potential based on the Derjaguin–Landau–Verwey–Overbeek (DLVO) theory, was significant low between MVs and cells in B. agrestis, compared to those between B. agrestis MVs and cells of other genera. Similar specific interaction was also occurred between B. agrestis MVs and cells of six other species belonging to Buttiauxella spp. B. agrestis harboring plasmid pBBR1MCS-1 secreted plasmid-containing MVs (p-MVs), and plasmid DNA in p-MVs was transferred to the same species. Moreover, antibiotic-associated MVs enabled effective killing of target species; the survival rate of B. agrestis was lower than those of Escherichia coli and Pseudomonas aeruginosa in the presence of gentamicin-associated MVs derived from B. agrestis. Altogether, we provide the evidence that MVs selectively interact with target bacterial cells and offer a new avenue for controlling specific bacterial species using bacterial MVs in microbial communities.
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spelling pubmed-53837042017-04-24 Interaction of Bacterial Membrane Vesicles with Specific Species and Their Potential for Delivery to Target Cells Tashiro, Yosuke Hasegawa, Yusuke Shintani, Masaki Takaki, Kotaro Ohkuma, Moriya Kimbara, Kazuhide Futamata, Hiroyuki Front Microbiol Microbiology Membrane vesicles (MVs) are secreted from a wide range of microbial species and transfer their content to other cells. Although MVs play critical roles in bacterial communication, whether MVs selectively interact with bacterial cells in microbial communities is unclear. In this study, we investigated the specificity of the MV-cell interactions and evaluated the potential of MVs to target bacterial cells for delivery. MV association with bacterial cells was examined using a fluorescent membrane dye to label MVs. MVs derived from the enterobacterium Buttiauxella agrestis specifically interacted with cells of the parent strain but interacted less specifically with those of other genera tested in this study. Electron microscopic analyses showed that MVs were not only attached on B. agrestis cells but also fused to them. The interaction energy, which was characterized by hydrodynamic diameter and zeta potential based on the Derjaguin–Landau–Verwey–Overbeek (DLVO) theory, was significant low between MVs and cells in B. agrestis, compared to those between B. agrestis MVs and cells of other genera. Similar specific interaction was also occurred between B. agrestis MVs and cells of six other species belonging to Buttiauxella spp. B. agrestis harboring plasmid pBBR1MCS-1 secreted plasmid-containing MVs (p-MVs), and plasmid DNA in p-MVs was transferred to the same species. Moreover, antibiotic-associated MVs enabled effective killing of target species; the survival rate of B. agrestis was lower than those of Escherichia coli and Pseudomonas aeruginosa in the presence of gentamicin-associated MVs derived from B. agrestis. Altogether, we provide the evidence that MVs selectively interact with target bacterial cells and offer a new avenue for controlling specific bacterial species using bacterial MVs in microbial communities. Frontiers Media S.A. 2017-04-07 /pmc/articles/PMC5383704/ /pubmed/28439261 http://dx.doi.org/10.3389/fmicb.2017.00571 Text en Copyright © 2017 Tashiro, Hasegawa, Shintani, Takaki, Ohkuma, Kimbara and Futamata. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Tashiro, Yosuke
Hasegawa, Yusuke
Shintani, Masaki
Takaki, Kotaro
Ohkuma, Moriya
Kimbara, Kazuhide
Futamata, Hiroyuki
Interaction of Bacterial Membrane Vesicles with Specific Species and Their Potential for Delivery to Target Cells
title Interaction of Bacterial Membrane Vesicles with Specific Species and Their Potential for Delivery to Target Cells
title_full Interaction of Bacterial Membrane Vesicles with Specific Species and Their Potential for Delivery to Target Cells
title_fullStr Interaction of Bacterial Membrane Vesicles with Specific Species and Their Potential for Delivery to Target Cells
title_full_unstemmed Interaction of Bacterial Membrane Vesicles with Specific Species and Their Potential for Delivery to Target Cells
title_short Interaction of Bacterial Membrane Vesicles with Specific Species and Their Potential for Delivery to Target Cells
title_sort interaction of bacterial membrane vesicles with specific species and their potential for delivery to target cells
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5383704/
https://www.ncbi.nlm.nih.gov/pubmed/28439261
http://dx.doi.org/10.3389/fmicb.2017.00571
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