Iron-regulated small RNA expression as Neisseria gonorrhoeae FA 1090 transitions into stationary phase growth

Abstract Background For most pathogens, iron (Fe) homeostasis is crucial for maintenance within the host and the ability to cause disease. The primary transcriptional regulator that controls intracellular Fe levels is the Fur (ferric uptake regulator) protein, which exerts its action on transcriptio...

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Main Authors: Lydgia A. Jackson, Michael Day, Jennie Allen, Edgar Scott, David W. Dyer
Format: Article
Language:English
Published: BMC 2017-04-01
Series:BMC Genomics
Subjects:
Fur
Online Access:http://link.springer.com/article/10.1186/s12864-017-3684-8
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spelling doaj-ce6579dec7704fc7a64314756b8b610c2020-11-24T21:57:44ZengBMCBMC Genomics1471-21642017-04-0118111310.1186/s12864-017-3684-8Iron-regulated small RNA expression as Neisseria gonorrhoeae FA 1090 transitions into stationary phase growthLydgia A. Jackson0Michael Day1Jennie Allen2Edgar Scott3David W. Dyer4Department of Microbiology and Immunology, University of Oklahoma Health SciencesDepartment of Microbiology and Immunology, University of Oklahoma Health SciencesDepartment of Microbiology and Immunology, University of Oklahoma Health SciencesDepartment of Microbiology and Immunology, University of Oklahoma Health SciencesDepartment of Microbiology and Immunology, University of Oklahoma Health SciencesAbstract Background For most pathogens, iron (Fe) homeostasis is crucial for maintenance within the host and the ability to cause disease. The primary transcriptional regulator that controls intracellular Fe levels is the Fur (ferric uptake regulator) protein, which exerts its action on transcription by binding to a promoter-proximal sequence termed the Fur box. Fur-regulated transcriptional responses are often fine-tuned at the post-transcriptional level through the action of small regulatory RNAs (sRNAs). Consequently, identifying sRNAs contributing to the control of Fe homeostasis is important for understanding the Fur-controlled bacterial Fe-response network. Results In this study, we sequenced size-selected directional libraries representing sRNA samples from Neisseria gonorrhoeae strain FA 1090, and examined the Fe- and temporal regulation of these sRNAs. RNA-seq data for all time points identified a pool of at least 340 potential sRNAs. Differential analysis demonstrated that expression appeared to be regulated by Fe availability for at least fifteen of these sRNAs. Fourteen sRNAs were induced in high Fe conditions, consisting of both cis and trans sRNAs, some of which are predicted to control expression of a known virulence factor, and one SAM riboswitch. An additional putative cis-acting sRNA was repressed by Fe availability. In the pathogenic Neisseria species, one sRNA that contributes to Fe-regulated post-transcriptional control is the Fur-repressible sRNA NrrF. The expression of five Fe-induced sRNAs appeared to be at least partially controlled by NrrF, while the remainder was expressed independently of NrrF. The expression of the 14 Fe-induced sRNAs also exhibited temporal control, as their expression levels increased dramatically as the bacteria entered stationary phase. Conclusions Here we report the temporal expression of Fe-regulated sRNAs in N. gonorrhoeae FA 1090 with several appearing to be controlled by the Fe-repressible sRNA NrrF. Temporal regulation of these sRNAs suggests a regulatory role in controlling functions necessary for survival, and may be important for phenotypes often associated with altered growth rates, such as biofilm formation or intracellular survival. Future functional studies will be needed to understand how these regulatory sRNAs contribute to gonococcal biology and pathogenesis.http://link.springer.com/article/10.1186/s12864-017-3684-8RNA-seqSmall RNAIronFurNeisseria gonorrhoeaeNrrF
collection DOAJ
language English
format Article
sources DOAJ
author Lydgia A. Jackson
Michael Day
Jennie Allen
Edgar Scott
David W. Dyer
spellingShingle Lydgia A. Jackson
Michael Day
Jennie Allen
Edgar Scott
David W. Dyer
Iron-regulated small RNA expression as Neisseria gonorrhoeae FA 1090 transitions into stationary phase growth
BMC Genomics
RNA-seq
Small RNA
Iron
Fur
Neisseria gonorrhoeae
NrrF
author_facet Lydgia A. Jackson
Michael Day
Jennie Allen
Edgar Scott
David W. Dyer
author_sort Lydgia A. Jackson
title Iron-regulated small RNA expression as Neisseria gonorrhoeae FA 1090 transitions into stationary phase growth
title_short Iron-regulated small RNA expression as Neisseria gonorrhoeae FA 1090 transitions into stationary phase growth
title_full Iron-regulated small RNA expression as Neisseria gonorrhoeae FA 1090 transitions into stationary phase growth
title_fullStr Iron-regulated small RNA expression as Neisseria gonorrhoeae FA 1090 transitions into stationary phase growth
title_full_unstemmed Iron-regulated small RNA expression as Neisseria gonorrhoeae FA 1090 transitions into stationary phase growth
title_sort iron-regulated small rna expression as neisseria gonorrhoeae fa 1090 transitions into stationary phase growth
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2017-04-01
description Abstract Background For most pathogens, iron (Fe) homeostasis is crucial for maintenance within the host and the ability to cause disease. The primary transcriptional regulator that controls intracellular Fe levels is the Fur (ferric uptake regulator) protein, which exerts its action on transcription by binding to a promoter-proximal sequence termed the Fur box. Fur-regulated transcriptional responses are often fine-tuned at the post-transcriptional level through the action of small regulatory RNAs (sRNAs). Consequently, identifying sRNAs contributing to the control of Fe homeostasis is important for understanding the Fur-controlled bacterial Fe-response network. Results In this study, we sequenced size-selected directional libraries representing sRNA samples from Neisseria gonorrhoeae strain FA 1090, and examined the Fe- and temporal regulation of these sRNAs. RNA-seq data for all time points identified a pool of at least 340 potential sRNAs. Differential analysis demonstrated that expression appeared to be regulated by Fe availability for at least fifteen of these sRNAs. Fourteen sRNAs were induced in high Fe conditions, consisting of both cis and trans sRNAs, some of which are predicted to control expression of a known virulence factor, and one SAM riboswitch. An additional putative cis-acting sRNA was repressed by Fe availability. In the pathogenic Neisseria species, one sRNA that contributes to Fe-regulated post-transcriptional control is the Fur-repressible sRNA NrrF. The expression of five Fe-induced sRNAs appeared to be at least partially controlled by NrrF, while the remainder was expressed independently of NrrF. The expression of the 14 Fe-induced sRNAs also exhibited temporal control, as their expression levels increased dramatically as the bacteria entered stationary phase. Conclusions Here we report the temporal expression of Fe-regulated sRNAs in N. gonorrhoeae FA 1090 with several appearing to be controlled by the Fe-repressible sRNA NrrF. Temporal regulation of these sRNAs suggests a regulatory role in controlling functions necessary for survival, and may be important for phenotypes often associated with altered growth rates, such as biofilm formation or intracellular survival. Future functional studies will be needed to understand how these regulatory sRNAs contribute to gonococcal biology and pathogenesis.
topic RNA-seq
Small RNA
Iron
Fur
Neisseria gonorrhoeae
NrrF
url http://link.springer.com/article/10.1186/s12864-017-3684-8
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