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The small RNA ncS35 regulates growth in Burkholderia cenocepacia J2315

Sanne Kiekens (UGent) , Andrea Sass (UGent) , Filip Van Nieuwerburgh (UGent) , Dieter Deforce (UGent) and Tom Coenye (UGent)
(2018) MSPHERE. 3(1).
Author
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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, Delta ncS35, was constructed. Compared to planktonic growth in a rich medium, the expression of ncS35 was elevated when B. cenocepacia 12315 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 Delta ncS35. 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.
Keywords
Burkholderia cenocepacia, metabolism, small RNA, BURKHOLDERIA-CEPACIA COMPLEX, CYSTIC-FIBROSIS, BIOFILMS, BACTERIA, ROLES, SUSCEPTIBILITY, IDENTIFICATION, EPIDEMIOLOGY, PERSISTENCE, TOBRAMYCIN

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Citation

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MLA
Kiekens, Sanne, Andrea Sass, Filip Van Nieuwerburgh, et al. “The Small RNA ncS35 Regulates Growth in Burkholderia Cenocepacia J2315.” MSPHERE 3.1 (2018): n. pag. Print.
APA
Kiekens, S., Sass, A., Van Nieuwerburgh, F., Deforce, D., & Coenye, T. (2018). The small RNA ncS35 regulates growth in Burkholderia cenocepacia J2315. MSPHERE, 3(1).
Chicago author-date
Kiekens, Sanne, Andrea Sass, Filip Van Nieuwerburgh, Dieter Deforce, and Tom Coenye. 2018. “The Small RNA ncS35 Regulates Growth in Burkholderia Cenocepacia J2315.” Msphere 3 (1).
Chicago author-date (all authors)
Kiekens, Sanne, Andrea Sass, Filip Van Nieuwerburgh, Dieter Deforce, and Tom Coenye. 2018. “The Small RNA ncS35 Regulates Growth in Burkholderia Cenocepacia J2315.” Msphere 3 (1).
Vancouver
1.
Kiekens S, Sass A, Van Nieuwerburgh F, Deforce D, Coenye T. The small RNA ncS35 regulates growth in Burkholderia cenocepacia J2315. MSPHERE. 2018;3(1).
IEEE
[1]
S. Kiekens, A. Sass, F. Van Nieuwerburgh, D. Deforce, and T. Coenye, “The small RNA ncS35 regulates growth in Burkholderia cenocepacia J2315,” MSPHERE, vol. 3, no. 1, 2018.
@article{8551244,
  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, Delta ncS35, was constructed. Compared to planktonic growth in a rich medium, the expression of ncS35 was elevated when B. cenocepacia 12315 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 Delta ncS35. 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.},
  articleno    = {e00579-17},
  author       = {Kiekens, Sanne and Sass, Andrea and Van Nieuwerburgh, Filip and Deforce, Dieter and Coenye, Tom},
  issn         = {2379-5042},
  journal      = {MSPHERE},
  keywords     = {Burkholderia cenocepacia,metabolism,small RNA,BURKHOLDERIA-CEPACIA COMPLEX,CYSTIC-FIBROSIS,BIOFILMS,BACTERIA,ROLES,SUSCEPTIBILITY,IDENTIFICATION,EPIDEMIOLOGY,PERSISTENCE,TOBRAMYCIN},
  language     = {eng},
  number       = {1},
  pages        = {16},
  title        = {The small RNA ncS35 regulates growth in Burkholderia cenocepacia J2315},
  url          = {http://dx.doi.org/10.1128/msphere.00579-17},
  volume       = {3},
  year         = {2018},
}

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