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Functional analysis of an unusual type IV pilus in the Gram‐positive Streptococcus sanguinis
Type IV pili (Tfp), which have been studied extensively in a few Gram‐negative species, are the paradigm of a group of widespread and functionally versatile nano‐machines. Here, we performed the most detailed molecular characterisation of Tfp in a Gram‐positive bacterium. We demonstrate that the nat...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4832360/ https://www.ncbi.nlm.nih.gov/pubmed/26435398 http://dx.doi.org/10.1111/mmi.13237 |
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author | Gurung, Ishwori Spielman, Ingrid Davies, Mark R. Lala, Rajan Gaustad, Peter Biais, Nicolas Pelicic, Vladimir |
author_facet | Gurung, Ishwori Spielman, Ingrid Davies, Mark R. Lala, Rajan Gaustad, Peter Biais, Nicolas Pelicic, Vladimir |
author_sort | Gurung, Ishwori |
collection | PubMed |
description | Type IV pili (Tfp), which have been studied extensively in a few Gram‐negative species, are the paradigm of a group of widespread and functionally versatile nano‐machines. Here, we performed the most detailed molecular characterisation of Tfp in a Gram‐positive bacterium. We demonstrate that the naturally competent S treptococcus sanguinis produces retractable Tfp, which like their Gram‐negative counterparts can generate hundreds of piconewton of tensile force and promote intense surface‐associated motility. Tfp power ‘train‐like’ directional motion parallel to the long axis of chains of cells, leading to spreading zones around bacteria grown on plates. However, S . sanguinis Tfp are not involved in DNA uptake, which is mediated by a related but distinct nano‐machine, and are unusual because they are composed of two pilins in comparable amounts, rather than one as normally seen. Whole genome sequencing identified a locus encoding all the genes involved in Tfp biology in S . sanguinis. A systematic mutational analysis revealed that Tfp biogenesis in S . sanguinis relies on a more basic machinery (only 10 components) than in Gram‐negative species and that a small subset of four proteins dispensable for pilus biogenesis are essential for motility. Intriguingly, one of the piliated mutants that does not exhibit spreading retains microscopic motility but moves sideways, which suggests that the corresponding protein controls motion directionality. Besides establishing S . sanguinis as a useful new model for studying Tfp biology, these findings have important implications for our understanding of these widespread filamentous nano‐machines. |
format | Online Article Text |
id | pubmed-4832360 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
spelling | pubmed-48323602016-04-20 Functional analysis of an unusual type IV pilus in the Gram‐positive Streptococcus sanguinis Gurung, Ishwori Spielman, Ingrid Davies, Mark R. Lala, Rajan Gaustad, Peter Biais, Nicolas Pelicic, Vladimir Mol Microbiol Research Articles Type IV pili (Tfp), which have been studied extensively in a few Gram‐negative species, are the paradigm of a group of widespread and functionally versatile nano‐machines. Here, we performed the most detailed molecular characterisation of Tfp in a Gram‐positive bacterium. We demonstrate that the naturally competent S treptococcus sanguinis produces retractable Tfp, which like their Gram‐negative counterparts can generate hundreds of piconewton of tensile force and promote intense surface‐associated motility. Tfp power ‘train‐like’ directional motion parallel to the long axis of chains of cells, leading to spreading zones around bacteria grown on plates. However, S . sanguinis Tfp are not involved in DNA uptake, which is mediated by a related but distinct nano‐machine, and are unusual because they are composed of two pilins in comparable amounts, rather than one as normally seen. Whole genome sequencing identified a locus encoding all the genes involved in Tfp biology in S . sanguinis. A systematic mutational analysis revealed that Tfp biogenesis in S . sanguinis relies on a more basic machinery (only 10 components) than in Gram‐negative species and that a small subset of four proteins dispensable for pilus biogenesis are essential for motility. Intriguingly, one of the piliated mutants that does not exhibit spreading retains microscopic motility but moves sideways, which suggests that the corresponding protein controls motion directionality. Besides establishing S . sanguinis as a useful new model for studying Tfp biology, these findings have important implications for our understanding of these widespread filamentous nano‐machines. John Wiley and Sons Inc. 2015-10-27 2016-01 /pmc/articles/PMC4832360/ /pubmed/26435398 http://dx.doi.org/10.1111/mmi.13237 Text en © 2015 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Articles Gurung, Ishwori Spielman, Ingrid Davies, Mark R. Lala, Rajan Gaustad, Peter Biais, Nicolas Pelicic, Vladimir Functional analysis of an unusual type IV pilus in the Gram‐positive Streptococcus sanguinis |
title | Functional analysis of an unusual type IV pilus in the Gram‐positive Streptococcus sanguinis
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title_full | Functional analysis of an unusual type IV pilus in the Gram‐positive Streptococcus sanguinis
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title_fullStr | Functional analysis of an unusual type IV pilus in the Gram‐positive Streptococcus sanguinis
|
title_full_unstemmed | Functional analysis of an unusual type IV pilus in the Gram‐positive Streptococcus sanguinis
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title_short | Functional analysis of an unusual type IV pilus in the Gram‐positive Streptococcus sanguinis
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title_sort | functional analysis of an unusual type iv pilus in the gram‐positive streptococcus sanguinis |
topic | Research Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4832360/ https://www.ncbi.nlm.nih.gov/pubmed/26435398 http://dx.doi.org/10.1111/mmi.13237 |
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