A Small Non-Coding RNA Modulates Expression of Pilus-1 Type in <i>Streptococcus pneumoniae</i>

<i>Streptococcus pneumoniae</i> is a major cause of morbidity and mortality worldwide, and about 30% of the pneumococcal clinical isolates show type I pili-like structures. These long proteinaceous polymers extending from the bacterial surface are encoded by pilus islet 1 and play major...

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Main Authors: Paloma Acebo, Cristina Herranz, Lucas Bernal Espenberger, Alicia Gómez-Sanz, María Carmen Terrón, Daniel Luque, Mónica Amblar
Format: Article
Language:English
Published: MDPI AG 2021-09-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/9/9/1883
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author Paloma Acebo
Cristina Herranz
Lucas Bernal Espenberger
Alicia Gómez-Sanz
María Carmen Terrón
Daniel Luque
Mónica Amblar
author_facet Paloma Acebo
Cristina Herranz
Lucas Bernal Espenberger
Alicia Gómez-Sanz
María Carmen Terrón
Daniel Luque
Mónica Amblar
author_sort Paloma Acebo
collection DOAJ
description <i>Streptococcus pneumoniae</i> is a major cause of morbidity and mortality worldwide, and about 30% of the pneumococcal clinical isolates show type I pili-like structures. These long proteinaceous polymers extending from the bacterial surface are encoded by pilus islet 1 and play major roles in adhesion and host colonization. Pili expression is bistable and is controlled by the transcriptional activator RlrA. In this work, we demonstrate that the previously identified small noncoding RNA <i>srn135</i> also participates in pilus regulation. Our findings show that <i>srn135</i> is generated upon processing of the 5′-UTR region of <i>rrgA</i> messenger and its deletion prevents the synthesis of RrgA, the main pili adhesin. Moreover, overexpression of <i>srn135</i> increases the expression of all pili genes and rises the percentage of piliated bacteria within a clonal population. This regulation is mediated by the stabilization of <i>rlrA</i> mRNA since higher levels of <i>srn135</i> increase its half-life to 165%. Our findings suggest that <i>srn135</i> has a dual role in pilus expression acting both in <i>cis-</i> (on the RrgA levels) and in <i>trans-</i> (modulating the levels of RlrA) and contributes to the delicate balance between pili expressing and non-expressing bacteria.
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spelling doaj.art-3b52a4ba7314418aa6750e6943e94e0c2023-11-22T14:18:33ZengMDPI AGMicroorganisms2076-26072021-09-0199188310.3390/microorganisms9091883A Small Non-Coding RNA Modulates Expression of Pilus-1 Type in <i>Streptococcus pneumoniae</i>Paloma Acebo0Cristina Herranz1Lucas Bernal Espenberger2Alicia Gómez-Sanz3María Carmen Terrón4Daniel Luque5Mónica Amblar6Unidad de Patología Molecular del Neumococo, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, 28220 Madrid, SpainUnidad de Patología Molecular del Neumococo, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, 28220 Madrid, SpainUnidad de Patología Molecular del Neumococo, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, 28220 Madrid, SpainUnidad de Patología Molecular del Neumococo, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, 28220 Madrid, SpainUnidad de Microscopia Electrónica y Confocal, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, 28220 Madrid, SpainUnidad de Microscopia Electrónica y Confocal, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, 28220 Madrid, SpainUnidad de Patología Molecular del Neumococo, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, 28220 Madrid, Spain<i>Streptococcus pneumoniae</i> is a major cause of morbidity and mortality worldwide, and about 30% of the pneumococcal clinical isolates show type I pili-like structures. These long proteinaceous polymers extending from the bacterial surface are encoded by pilus islet 1 and play major roles in adhesion and host colonization. Pili expression is bistable and is controlled by the transcriptional activator RlrA. In this work, we demonstrate that the previously identified small noncoding RNA <i>srn135</i> also participates in pilus regulation. Our findings show that <i>srn135</i> is generated upon processing of the 5′-UTR region of <i>rrgA</i> messenger and its deletion prevents the synthesis of RrgA, the main pili adhesin. Moreover, overexpression of <i>srn135</i> increases the expression of all pili genes and rises the percentage of piliated bacteria within a clonal population. This regulation is mediated by the stabilization of <i>rlrA</i> mRNA since higher levels of <i>srn135</i> increase its half-life to 165%. Our findings suggest that <i>srn135</i> has a dual role in pilus expression acting both in <i>cis-</i> (on the RrgA levels) and in <i>trans-</i> (modulating the levels of RlrA) and contributes to the delicate balance between pili expressing and non-expressing bacteria.https://www.mdpi.com/2076-2607/9/9/1883<i>S. pneumoniae</i>Pilus-1 typePI-1sRNAregulatory RNA
spellingShingle Paloma Acebo
Cristina Herranz
Lucas Bernal Espenberger
Alicia Gómez-Sanz
María Carmen Terrón
Daniel Luque
Mónica Amblar
A Small Non-Coding RNA Modulates Expression of Pilus-1 Type in <i>Streptococcus pneumoniae</i>
Microorganisms
<i>S. pneumoniae</i>
Pilus-1 type
PI-1
sRNA
regulatory RNA
title A Small Non-Coding RNA Modulates Expression of Pilus-1 Type in <i>Streptococcus pneumoniae</i>
title_full A Small Non-Coding RNA Modulates Expression of Pilus-1 Type in <i>Streptococcus pneumoniae</i>
title_fullStr A Small Non-Coding RNA Modulates Expression of Pilus-1 Type in <i>Streptococcus pneumoniae</i>
title_full_unstemmed A Small Non-Coding RNA Modulates Expression of Pilus-1 Type in <i>Streptococcus pneumoniae</i>
title_short A Small Non-Coding RNA Modulates Expression of Pilus-1 Type in <i>Streptococcus pneumoniae</i>
title_sort small non coding rna modulates expression of pilus 1 type in i streptococcus pneumoniae i
topic <i>S. pneumoniae</i>
Pilus-1 type
PI-1
sRNA
regulatory RNA
url https://www.mdpi.com/2076-2607/9/9/1883
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