The Small RNA ncS35 Regulates Growth in <named-content content-type="genus-species">Burkholderia cenocepacia</named-content> J2315

ABSTRACT Burkholderia cenocepacia J2315 is a member of the B. cepacia complex. It has a large genome with three replicons and one plasmid; 7,261 genes code for annotated proteins, while 113 code for functional RNAs. Small regulatory RNAs of B. cenocepacia have not yet been functionally characterized...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Sanne Kiekens, Andrea Sass, Filip Van Nieuwerburgh, Dieter Deforce, Tom Coenye
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2018
Materias:
Acceso en línea:https://doaj.org/article/921fa85e9a234d9f90ebb4affb450020
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:921fa85e9a234d9f90ebb4affb450020
record_format dspace
spelling oai:doaj.org-article:921fa85e9a234d9f90ebb4affb4500202021-11-15T15:22:02ZThe Small RNA ncS35 Regulates Growth in <named-content content-type="genus-species">Burkholderia cenocepacia</named-content> J231510.1128/mSphere.00579-172379-5042https://doaj.org/article/921fa85e9a234d9f90ebb4affb4500202018-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00579-17https://doaj.org/toc/2379-5042ABSTRACT Burkholderia cenocepacia J2315 is a member of the B. cepacia complex. It has a large genome with three replicons and one plasmid; 7,261 genes code for annotated proteins, while 113 code for functional RNAs. Small regulatory RNAs of B. cenocepacia have not yet been functionally characterized. We investigated a small regulatory RNA, designated ncS35, that was discovered by differential RNA sequencing. Its expression under various conditions was quantified, and a deletion mutant, ΔncS35, was constructed. Compared to planktonic growth in a rich medium, the expression of ncS35 was elevated when B. cenocepacia J2315 was grown in biofilms and in minimal medium. Cells of the deletion mutant showed increased aggregation, higher metabolic activity, a higher growth rate, and an increased susceptibility to tobramycin. A transcriptomic analysis revealed upregulation of the phenylacetic acid and tryptophan degradation pathways in ΔncS35. Computational target prediction indicated that ncS35 likely interacts with the first gene of the tryptophan degradation pathway. Overall, we demonstrated that small RNA ncS35 is a noncoding RNA with an attenuating effect on the metabolic rate and growth. It is possible that slower growth protects B. cenocepacia J2315 against stressors acting on fast-dividing cells and enhances survival under unfavorable conditions. IMPORTANCE Small RNAs play an important role in the survival of bacteria in diverse environments. We explored the physiological role of ncS35, a small RNA expressed in B. cenocepacia J2315, an opportunistic pathogen in cystic fibrosis patients. In cystic fibrosis patients, infections can lead to “cepacia syndrome,” a rapidly progressing and often fatal pneumonia. Infections with Burkholderia spp. are difficult to threat with antibiotics because of their high intrinsic resistance and ability to form biofilms. We show that ncS35 attenuates the growth and reduces the metabolic rate of B. cenocepacia and influences biofilm structure. This demonstrates that as-yet-uncharacterized small RNAs with regulatory function can influence physiological traits of B. cenocepacia that are relevant for infection.Sanne KiekensAndrea SassFilip Van NieuwerburghDieter DeforceTom CoenyeAmerican Society for MicrobiologyarticleBurkholderia cenocepaciametabolismsmall RNAMicrobiologyQR1-502ENmSphere, Vol 3, Iss 1 (2018)
institution DOAJ
collection DOAJ
language EN
topic Burkholderia cenocepacia
metabolism
small RNA
Microbiology
QR1-502
spellingShingle Burkholderia cenocepacia
metabolism
small RNA
Microbiology
QR1-502
Sanne Kiekens
Andrea Sass
Filip Van Nieuwerburgh
Dieter Deforce
Tom Coenye
The Small RNA ncS35 Regulates Growth in <named-content content-type="genus-species">Burkholderia cenocepacia</named-content> J2315
description ABSTRACT Burkholderia cenocepacia J2315 is a member of the B. cepacia complex. It has a large genome with three replicons and one plasmid; 7,261 genes code for annotated proteins, while 113 code for functional RNAs. Small regulatory RNAs of B. cenocepacia have not yet been functionally characterized. We investigated a small regulatory RNA, designated ncS35, that was discovered by differential RNA sequencing. Its expression under various conditions was quantified, and a deletion mutant, ΔncS35, was constructed. Compared to planktonic growth in a rich medium, the expression of ncS35 was elevated when B. cenocepacia J2315 was grown in biofilms and in minimal medium. Cells of the deletion mutant showed increased aggregation, higher metabolic activity, a higher growth rate, and an increased susceptibility to tobramycin. A transcriptomic analysis revealed upregulation of the phenylacetic acid and tryptophan degradation pathways in ΔncS35. Computational target prediction indicated that ncS35 likely interacts with the first gene of the tryptophan degradation pathway. Overall, we demonstrated that small RNA ncS35 is a noncoding RNA with an attenuating effect on the metabolic rate and growth. It is possible that slower growth protects B. cenocepacia J2315 against stressors acting on fast-dividing cells and enhances survival under unfavorable conditions. IMPORTANCE Small RNAs play an important role in the survival of bacteria in diverse environments. We explored the physiological role of ncS35, a small RNA expressed in B. cenocepacia J2315, an opportunistic pathogen in cystic fibrosis patients. In cystic fibrosis patients, infections can lead to “cepacia syndrome,” a rapidly progressing and often fatal pneumonia. Infections with Burkholderia spp. are difficult to threat with antibiotics because of their high intrinsic resistance and ability to form biofilms. We show that ncS35 attenuates the growth and reduces the metabolic rate of B. cenocepacia and influences biofilm structure. This demonstrates that as-yet-uncharacterized small RNAs with regulatory function can influence physiological traits of B. cenocepacia that are relevant for infection.
format article
author Sanne Kiekens
Andrea Sass
Filip Van Nieuwerburgh
Dieter Deforce
Tom Coenye
author_facet Sanne Kiekens
Andrea Sass
Filip Van Nieuwerburgh
Dieter Deforce
Tom Coenye
author_sort Sanne Kiekens
title The Small RNA ncS35 Regulates Growth in <named-content content-type="genus-species">Burkholderia cenocepacia</named-content> J2315
title_short The Small RNA ncS35 Regulates Growth in <named-content content-type="genus-species">Burkholderia cenocepacia</named-content> J2315
title_full The Small RNA ncS35 Regulates Growth in <named-content content-type="genus-species">Burkholderia cenocepacia</named-content> J2315
title_fullStr The Small RNA ncS35 Regulates Growth in <named-content content-type="genus-species">Burkholderia cenocepacia</named-content> J2315
title_full_unstemmed The Small RNA ncS35 Regulates Growth in <named-content content-type="genus-species">Burkholderia cenocepacia</named-content> J2315
title_sort small rna ncs35 regulates growth in <named-content content-type="genus-species">burkholderia cenocepacia</named-content> j2315
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/921fa85e9a234d9f90ebb4affb450020
work_keys_str_mv AT sannekiekens thesmallrnancs35regulatesgrowthinnamedcontentcontenttypegenusspeciesburkholderiacenocepacianamedcontentj2315
AT andreasass thesmallrnancs35regulatesgrowthinnamedcontentcontenttypegenusspeciesburkholderiacenocepacianamedcontentj2315
AT filipvannieuwerburgh thesmallrnancs35regulatesgrowthinnamedcontentcontenttypegenusspeciesburkholderiacenocepacianamedcontentj2315
AT dieterdeforce thesmallrnancs35regulatesgrowthinnamedcontentcontenttypegenusspeciesburkholderiacenocepacianamedcontentj2315
AT tomcoenye thesmallrnancs35regulatesgrowthinnamedcontentcontenttypegenusspeciesburkholderiacenocepacianamedcontentj2315
AT sannekiekens smallrnancs35regulatesgrowthinnamedcontentcontenttypegenusspeciesburkholderiacenocepacianamedcontentj2315
AT andreasass smallrnancs35regulatesgrowthinnamedcontentcontenttypegenusspeciesburkholderiacenocepacianamedcontentj2315
AT filipvannieuwerburgh smallrnancs35regulatesgrowthinnamedcontentcontenttypegenusspeciesburkholderiacenocepacianamedcontentj2315
AT dieterdeforce smallrnancs35regulatesgrowthinnamedcontentcontenttypegenusspeciesburkholderiacenocepacianamedcontentj2315
AT tomcoenye smallrnancs35regulatesgrowthinnamedcontentcontenttypegenusspeciesburkholderiacenocepacianamedcontentj2315
_version_ 1718428084482342912