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Acinetobacter type VI secretion system comprises a non-canonical membrane complex
A. baumannii can rapidly acquire new resistance mechanisms and persist on abiotic surface, enabling the colonization of asymptomatic human host. In Acinetobacter the type VI secretion system (T6SS) is involved in twitching, surface motility and is used for interbacterial competition allowing the bac...
Autores principales: | , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10564176/ https://www.ncbi.nlm.nih.gov/pubmed/37769028 http://dx.doi.org/10.1371/journal.ppat.1011687 |
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author | Kandolo, Ona Cherrak, Yassine Filella-Merce, Isaac Le Guenno, Hugo Kosta, Artemis Espinosa, Leon Santucci, Pierre Verthuy, Christophe Lebrun, Régine Nilges, Michael Pellarin, Riccardo Durand, Eric |
author_facet | Kandolo, Ona Cherrak, Yassine Filella-Merce, Isaac Le Guenno, Hugo Kosta, Artemis Espinosa, Leon Santucci, Pierre Verthuy, Christophe Lebrun, Régine Nilges, Michael Pellarin, Riccardo Durand, Eric |
author_sort | Kandolo, Ona |
collection | PubMed |
description | A. baumannii can rapidly acquire new resistance mechanisms and persist on abiotic surface, enabling the colonization of asymptomatic human host. In Acinetobacter the type VI secretion system (T6SS) is involved in twitching, surface motility and is used for interbacterial competition allowing the bacteria to uptake DNA. A. baumannii possesses a T6SS that has been well studied for its regulation and specific activity, but little is known concerning its assembly and architecture. The T6SS nanomachine is built from three architectural sub-complexes. Unlike the baseplate (BP) and the tail-tube complex (TTC), which are inherited from bacteriophages, the membrane complex (MC) originates from bacteria. The MC is the most external part of the T6SS and, as such, is subjected to evolution and adaptation. One unanswered question on the MC is how such a gigantesque molecular edifice is inserted and crosses the bacterial cell envelope. The A. baumannii MC lacks an essential component, the TssJ lipoprotein, which anchors the MC to the outer membrane. In this work, we studied how A. baumannii compensates the absence of a TssJ. We have characterized for the first time the A. baumannii’s specific T6SS MC, its unique characteristic, its membrane localization, and assembly dynamics. We also defined its composition, demonstrating that its biogenesis employs three Acinetobacter-specific envelope-associated proteins that define an intricate network leading to the assembly of a five-proteins membrane super-complex. Our data suggest that A. baumannii has divided the function of TssJ by (1) co-opting a new protein TsmK that stabilizes the MC and by (2) evolving a new domain in TssM for homo-oligomerization, a prerequisite to build the T6SS channel. We believe that the atypical species-specific features we report in this study will have profound implication in our understanding of the assembly and evolutionary diversity of different T6SSs, that warrants future investigation. |
format | Online Article Text |
id | pubmed-10564176 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-105641762023-10-11 Acinetobacter type VI secretion system comprises a non-canonical membrane complex Kandolo, Ona Cherrak, Yassine Filella-Merce, Isaac Le Guenno, Hugo Kosta, Artemis Espinosa, Leon Santucci, Pierre Verthuy, Christophe Lebrun, Régine Nilges, Michael Pellarin, Riccardo Durand, Eric PLoS Pathog Research Article A. baumannii can rapidly acquire new resistance mechanisms and persist on abiotic surface, enabling the colonization of asymptomatic human host. In Acinetobacter the type VI secretion system (T6SS) is involved in twitching, surface motility and is used for interbacterial competition allowing the bacteria to uptake DNA. A. baumannii possesses a T6SS that has been well studied for its regulation and specific activity, but little is known concerning its assembly and architecture. The T6SS nanomachine is built from three architectural sub-complexes. Unlike the baseplate (BP) and the tail-tube complex (TTC), which are inherited from bacteriophages, the membrane complex (MC) originates from bacteria. The MC is the most external part of the T6SS and, as such, is subjected to evolution and adaptation. One unanswered question on the MC is how such a gigantesque molecular edifice is inserted and crosses the bacterial cell envelope. The A. baumannii MC lacks an essential component, the TssJ lipoprotein, which anchors the MC to the outer membrane. In this work, we studied how A. baumannii compensates the absence of a TssJ. We have characterized for the first time the A. baumannii’s specific T6SS MC, its unique characteristic, its membrane localization, and assembly dynamics. We also defined its composition, demonstrating that its biogenesis employs three Acinetobacter-specific envelope-associated proteins that define an intricate network leading to the assembly of a five-proteins membrane super-complex. Our data suggest that A. baumannii has divided the function of TssJ by (1) co-opting a new protein TsmK that stabilizes the MC and by (2) evolving a new domain in TssM for homo-oligomerization, a prerequisite to build the T6SS channel. We believe that the atypical species-specific features we report in this study will have profound implication in our understanding of the assembly and evolutionary diversity of different T6SSs, that warrants future investigation. Public Library of Science 2023-09-28 /pmc/articles/PMC10564176/ /pubmed/37769028 http://dx.doi.org/10.1371/journal.ppat.1011687 Text en © 2023 Kandolo et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Kandolo, Ona Cherrak, Yassine Filella-Merce, Isaac Le Guenno, Hugo Kosta, Artemis Espinosa, Leon Santucci, Pierre Verthuy, Christophe Lebrun, Régine Nilges, Michael Pellarin, Riccardo Durand, Eric Acinetobacter type VI secretion system comprises a non-canonical membrane complex |
title | Acinetobacter type VI secretion system comprises a non-canonical membrane complex |
title_full | Acinetobacter type VI secretion system comprises a non-canonical membrane complex |
title_fullStr | Acinetobacter type VI secretion system comprises a non-canonical membrane complex |
title_full_unstemmed | Acinetobacter type VI secretion system comprises a non-canonical membrane complex |
title_short | Acinetobacter type VI secretion system comprises a non-canonical membrane complex |
title_sort | acinetobacter type vi secretion system comprises a non-canonical membrane complex |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10564176/ https://www.ncbi.nlm.nih.gov/pubmed/37769028 http://dx.doi.org/10.1371/journal.ppat.1011687 |
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