Cargando…

T6SS secretes an LPS-binding effector to recruit OMVs for exploitative competition and horizontal gene transfer

Outer membrane vesicles (OMVs) can function as nanoscale vectors that mediate bacterial interactions in microbial communities. How bacteria recognize and recruit OMVs inter-specifically remains largely unknown, thus limiting our understanding of the complex physiological and ecological roles of OMVs...

Descripción completa

Detalles Bibliográficos
Autores principales: Li, Changfu, Zhu, Lingfang, Wang, Dandan, Wei, Zhiyan, Hao, Xinwei, Wang, Zhuo, Li, Tengfei, Zhang, Lei, Lu, Zhiqiang, Long, Mingxiu, Wang, Yao, Wei, Gehong, Shen, Xihui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8776902/
https://www.ncbi.nlm.nih.gov/pubmed/34433898
http://dx.doi.org/10.1038/s41396-021-01093-8
_version_ 1784636939705516032
author Li, Changfu
Zhu, Lingfang
Wang, Dandan
Wei, Zhiyan
Hao, Xinwei
Wang, Zhuo
Li, Tengfei
Zhang, Lei
Lu, Zhiqiang
Long, Mingxiu
Wang, Yao
Wei, Gehong
Shen, Xihui
author_facet Li, Changfu
Zhu, Lingfang
Wang, Dandan
Wei, Zhiyan
Hao, Xinwei
Wang, Zhuo
Li, Tengfei
Zhang, Lei
Lu, Zhiqiang
Long, Mingxiu
Wang, Yao
Wei, Gehong
Shen, Xihui
author_sort Li, Changfu
collection PubMed
description Outer membrane vesicles (OMVs) can function as nanoscale vectors that mediate bacterial interactions in microbial communities. How bacteria recognize and recruit OMVs inter-specifically remains largely unknown, thus limiting our understanding of the complex physiological and ecological roles of OMVs. Here, we report a ligand-receptor interaction-based OMV recruitment mechanism, consisting of a type VI secretion system (T6SS)-secreted lipopolysaccharide (LPS)-binding effector TeoL and the outer membrane receptors CubA and CstR. We demonstrated that Cupriavidus necator T6SS1 secretes TeoL to preferentially associate with OMVs in the extracellular milieu through interactions with LPS, one of the most abundant components of OMVs. TeoL associated with OMVs can further bind outer membrane receptors CubA and CstR, which tethers OMVs to the recipient cells and allows cargo to be delivered. The LPS-mediated mechanism enables bacterial cells to recruit OMVs derived from different species, and confers advantages to bacterial cells in iron acquisition, interbacterial competition, and horizontal gene transfer (HGT). Moreover, our findings provide multiple new perspectives on T6SS functionality in the context of bacterial competition and HGT, through the recruitment of OMVs.
format Online
Article
Text
id pubmed-8776902
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-87769022022-02-04 T6SS secretes an LPS-binding effector to recruit OMVs for exploitative competition and horizontal gene transfer Li, Changfu Zhu, Lingfang Wang, Dandan Wei, Zhiyan Hao, Xinwei Wang, Zhuo Li, Tengfei Zhang, Lei Lu, Zhiqiang Long, Mingxiu Wang, Yao Wei, Gehong Shen, Xihui ISME J Article Outer membrane vesicles (OMVs) can function as nanoscale vectors that mediate bacterial interactions in microbial communities. How bacteria recognize and recruit OMVs inter-specifically remains largely unknown, thus limiting our understanding of the complex physiological and ecological roles of OMVs. Here, we report a ligand-receptor interaction-based OMV recruitment mechanism, consisting of a type VI secretion system (T6SS)-secreted lipopolysaccharide (LPS)-binding effector TeoL and the outer membrane receptors CubA and CstR. We demonstrated that Cupriavidus necator T6SS1 secretes TeoL to preferentially associate with OMVs in the extracellular milieu through interactions with LPS, one of the most abundant components of OMVs. TeoL associated with OMVs can further bind outer membrane receptors CubA and CstR, which tethers OMVs to the recipient cells and allows cargo to be delivered. The LPS-mediated mechanism enables bacterial cells to recruit OMVs derived from different species, and confers advantages to bacterial cells in iron acquisition, interbacterial competition, and horizontal gene transfer (HGT). Moreover, our findings provide multiple new perspectives on T6SS functionality in the context of bacterial competition and HGT, through the recruitment of OMVs. Nature Publishing Group UK 2021-08-25 2022-02 /pmc/articles/PMC8776902/ /pubmed/34433898 http://dx.doi.org/10.1038/s41396-021-01093-8 Text en © The Author(s) 2021 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Li, Changfu
Zhu, Lingfang
Wang, Dandan
Wei, Zhiyan
Hao, Xinwei
Wang, Zhuo
Li, Tengfei
Zhang, Lei
Lu, Zhiqiang
Long, Mingxiu
Wang, Yao
Wei, Gehong
Shen, Xihui
T6SS secretes an LPS-binding effector to recruit OMVs for exploitative competition and horizontal gene transfer
title T6SS secretes an LPS-binding effector to recruit OMVs for exploitative competition and horizontal gene transfer
title_full T6SS secretes an LPS-binding effector to recruit OMVs for exploitative competition and horizontal gene transfer
title_fullStr T6SS secretes an LPS-binding effector to recruit OMVs for exploitative competition and horizontal gene transfer
title_full_unstemmed T6SS secretes an LPS-binding effector to recruit OMVs for exploitative competition and horizontal gene transfer
title_short T6SS secretes an LPS-binding effector to recruit OMVs for exploitative competition and horizontal gene transfer
title_sort t6ss secretes an lps-binding effector to recruit omvs for exploitative competition and horizontal gene transfer
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8776902/
https://www.ncbi.nlm.nih.gov/pubmed/34433898
http://dx.doi.org/10.1038/s41396-021-01093-8
work_keys_str_mv AT lichangfu t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT zhulingfang t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT wangdandan t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT weizhiyan t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT haoxinwei t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT wangzhuo t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT litengfei t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT zhanglei t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT luzhiqiang t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT longmingxiu t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT wangyao t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT weigehong t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer
AT shenxihui t6sssecretesanlpsbindingeffectortorecruitomvsforexploitativecompetitionandhorizontalgenetransfer