Cargando…

Controllable secretion of multilayer vesicles driven by microbial polymer accumulation

Membrane vesicles (MVs) are formed in various microorganisms triggered by physiological and environmental phenomena. In this study, we have discovered that the biogenesis of MV took place in the recombinant cell of Escherichia coli BW25113 strain that intracellularly accumulates microbial polyester,...

Descripción completa

Detalles Bibliográficos
Autores principales: Koh, Sangho, Sato, Michio, Yamashina, Kota, Usukura, Yuki, Toyofuku, Masanori, Nomura, Nobuhiko, Taguchi, Seiichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8888611/
https://www.ncbi.nlm.nih.gov/pubmed/35233015
http://dx.doi.org/10.1038/s41598-022-07218-z
_version_ 1784661197424951296
author Koh, Sangho
Sato, Michio
Yamashina, Kota
Usukura, Yuki
Toyofuku, Masanori
Nomura, Nobuhiko
Taguchi, Seiichi
author_facet Koh, Sangho
Sato, Michio
Yamashina, Kota
Usukura, Yuki
Toyofuku, Masanori
Nomura, Nobuhiko
Taguchi, Seiichi
author_sort Koh, Sangho
collection PubMed
description Membrane vesicles (MVs) are formed in various microorganisms triggered by physiological and environmental phenomena. In this study, we have discovered that the biogenesis of MV took place in the recombinant cell of Escherichia coli BW25113 strain that intracellularly accumulates microbial polyester, polyhydroxybutyrate (PHB). This discovery was achieved as a trigger of foam formation during the microbial PHB fermentation. The purified MVs were existed as a mixture of outer MVs and outer/inner MVs, revealed by transmission electron microscopy. It should be noted that there was a good correlation between MV formation and PHB production level that can be finely controlled by varying glucose concentrations, suggesting the causal relationship in both supramolecules artificially produced in the microbial platform. Notably, the controllable secretion of MV was governed spatiotemporally through the morphological change of the E. coli cells caused by the PHB intracellular accumulation. Based on a hypothesis of PHB internal-pressure dependent envelope-disorder induced MV biogenesis, here we propose a new Polymer Intracellular Accumulation-triggered system for MV Production (designated “PIA-MVP”) with presenting a mechanistic model for MV biogenesis. The PIA-MVP is a promising microbial platform that will provides us with a significance for further study focusing on biopolymer capsulation and cross-membrane transportation for different application purposes.
format Online
Article
Text
id pubmed-8888611
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-88886112022-03-03 Controllable secretion of multilayer vesicles driven by microbial polymer accumulation Koh, Sangho Sato, Michio Yamashina, Kota Usukura, Yuki Toyofuku, Masanori Nomura, Nobuhiko Taguchi, Seiichi Sci Rep Article Membrane vesicles (MVs) are formed in various microorganisms triggered by physiological and environmental phenomena. In this study, we have discovered that the biogenesis of MV took place in the recombinant cell of Escherichia coli BW25113 strain that intracellularly accumulates microbial polyester, polyhydroxybutyrate (PHB). This discovery was achieved as a trigger of foam formation during the microbial PHB fermentation. The purified MVs were existed as a mixture of outer MVs and outer/inner MVs, revealed by transmission electron microscopy. It should be noted that there was a good correlation between MV formation and PHB production level that can be finely controlled by varying glucose concentrations, suggesting the causal relationship in both supramolecules artificially produced in the microbial platform. Notably, the controllable secretion of MV was governed spatiotemporally through the morphological change of the E. coli cells caused by the PHB intracellular accumulation. Based on a hypothesis of PHB internal-pressure dependent envelope-disorder induced MV biogenesis, here we propose a new Polymer Intracellular Accumulation-triggered system for MV Production (designated “PIA-MVP”) with presenting a mechanistic model for MV biogenesis. The PIA-MVP is a promising microbial platform that will provides us with a significance for further study focusing on biopolymer capsulation and cross-membrane transportation for different application purposes. Nature Publishing Group UK 2022-03-01 /pmc/articles/PMC8888611/ /pubmed/35233015 http://dx.doi.org/10.1038/s41598-022-07218-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Koh, Sangho
Sato, Michio
Yamashina, Kota
Usukura, Yuki
Toyofuku, Masanori
Nomura, Nobuhiko
Taguchi, Seiichi
Controllable secretion of multilayer vesicles driven by microbial polymer accumulation
title Controllable secretion of multilayer vesicles driven by microbial polymer accumulation
title_full Controllable secretion of multilayer vesicles driven by microbial polymer accumulation
title_fullStr Controllable secretion of multilayer vesicles driven by microbial polymer accumulation
title_full_unstemmed Controllable secretion of multilayer vesicles driven by microbial polymer accumulation
title_short Controllable secretion of multilayer vesicles driven by microbial polymer accumulation
title_sort controllable secretion of multilayer vesicles driven by microbial polymer accumulation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8888611/
https://www.ncbi.nlm.nih.gov/pubmed/35233015
http://dx.doi.org/10.1038/s41598-022-07218-z
work_keys_str_mv AT kohsangho controllablesecretionofmultilayervesiclesdrivenbymicrobialpolymeraccumulation
AT satomichio controllablesecretionofmultilayervesiclesdrivenbymicrobialpolymeraccumulation
AT yamashinakota controllablesecretionofmultilayervesiclesdrivenbymicrobialpolymeraccumulation
AT usukurayuki controllablesecretionofmultilayervesiclesdrivenbymicrobialpolymeraccumulation
AT toyofukumasanori controllablesecretionofmultilayervesiclesdrivenbymicrobialpolymeraccumulation
AT nomuranobuhiko controllablesecretionofmultilayervesiclesdrivenbymicrobialpolymeraccumulation
AT taguchiseiichi controllablesecretionofmultilayervesiclesdrivenbymicrobialpolymeraccumulation