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Directional RNA deep sequencing sheds new light on the transcriptional response of Anabaena sp strain PCC 7120 to combined-nitrogen deprivation

Britt L Flaherty, Filip Van Nieuwerburgh UGent, Steven R Head and James W Golden (2011) BMC GENOMICS. 12.
abstract
Background: Cyanobacteria are potential sources of renewable chemicals and biofuels and serve as model organisms for bacterial photosynthesis, nitrogen fixation, and responses to environmental changes. Anabaena (Nostoc) sp. strain PCC 7120 (hereafter Anabaena) is a multicellular filamentous cyanobacterium that can "fix" atmospheric nitrogen into ammonia when grown in the absence of a source of combined nitrogen. Because the nitrogenase enzyme is oxygen sensitive, Anabaena forms specialized cells called heterocysts that create a microoxic environment for nitrogen fixation. We have employed directional RNA-seq to map the Anabaena transcriptome during vegetative cell growth and in response to combined-nitrogen deprivation, which induces filaments to undergo heterocyst development. Our data provide an unprecedented view of transcriptional changes in Anabaena filaments during the induction of heterocyst development and transition to diazotrophic growth. Results: Using the Illumina short read platform and a directional RNA-seq protocol, we obtained deep sequencing data for RNA extracted from filaments at 0, 6, 12, and 21 hours after the removal of combined nitrogen. The RNA-seq data provided information on transcript abundance and boundaries for the entire transcriptome. From these data, we detected novel antisense transcripts within the UTRs (untranslated regions) and coding regions of key genes involved in heterocyst development, suggesting that antisense RNAs may be important regulators of the nitrogen response. In addition, many 5' UTRs were longer than anticipated, sometimes extending into upstream open reading frames (ORFs), and operons often showed complex structure and regulation. Finally, many genes that had not been previously identified as being involved in heterocyst development showed regulation, providing new candidates for future studies in this model organism. Conclusions: Directional RNA-seq data were obtained that provide comprehensive mapping of transcript boundaries and abundance for all transcribed RNAs in Anabaena filaments during the response to nitrogen deprivation. We have identified genes and noncoding RNAs that are transcriptionally regulated during heterocyst development. These data provide detailed information on the Anabaena transcriptome as filaments undergo heterocyst development and begin nitrogen fixation.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
GENE, NTCA, PCC-7120, CYANOBACTERIUM ANABAENA-7120, HETEROCYST DIFFERENTIATION, EXPRESSION, SEQ, REGULATOR, FIXATION, METABOLISM
journal title
BMC GENOMICS
BMC Genomics
volume
12
article_number
332
pages
10 pages
Web of Science type
Article
Web of Science id
000292930500001
JCR category
BIOTECHNOLOGY & APPLIED MICROBIOLOGY
JCR impact factor
4.073 (2011)
JCR rank
26/157 (2011)
JCR quartile
1 (2011)
ISSN
1471-2164
DOI
10.1186/1471-2164-12-332
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
1965696
handle
http://hdl.handle.net/1854/LU-1965696
date created
2011-12-13 10:35:01
date last changed
2011-12-13 14:57:28
@article{1965696,
  abstract     = {Background: Cyanobacteria are potential sources of renewable chemicals and biofuels and serve as model organisms for bacterial photosynthesis, nitrogen fixation, and responses to environmental changes. Anabaena (Nostoc) sp. strain PCC 7120 (hereafter Anabaena) is a multicellular filamentous cyanobacterium that can {\textacutedbl}fix{\textacutedbl} atmospheric nitrogen into ammonia when grown in the absence of a source of combined nitrogen. Because the nitrogenase enzyme is oxygen sensitive, Anabaena forms specialized cells called heterocysts that create a microoxic environment for nitrogen fixation. We have employed directional RNA-seq to map the Anabaena transcriptome during vegetative cell growth and in response to combined-nitrogen deprivation, which induces filaments to undergo heterocyst development. Our data provide an unprecedented view of transcriptional changes in Anabaena filaments during the induction of heterocyst development and transition to diazotrophic growth. 
Results: Using the Illumina short read platform and a directional RNA-seq protocol, we obtained deep sequencing data for RNA extracted from filaments at 0, 6, 12, and 21 hours after the removal of combined nitrogen. The RNA-seq data provided information on transcript abundance and boundaries for the entire transcriptome. From these data, we detected novel antisense transcripts within the UTRs (untranslated regions) and coding regions of key genes involved in heterocyst development, suggesting that antisense RNAs may be important regulators of the nitrogen response. In addition, many 5' UTRs were longer than anticipated, sometimes extending into upstream open reading frames (ORFs), and operons often showed complex structure and regulation. Finally, many genes that had not been previously identified as being involved in heterocyst development showed regulation, providing new candidates for future studies in this model organism. 
Conclusions: Directional RNA-seq data were obtained that provide comprehensive mapping of transcript boundaries and abundance for all transcribed RNAs in Anabaena filaments during the response to nitrogen deprivation. We have identified genes and noncoding RNAs that are transcriptionally regulated during heterocyst development. These data provide detailed information on the Anabaena transcriptome as filaments undergo heterocyst development and begin nitrogen fixation.},
  articleno    = {332},
  author       = {Flaherty, Britt L and Van Nieuwerburgh, Filip and Head, Steven R and Golden, James W},
  issn         = {1471-2164},
  journal      = {BMC GENOMICS},
  keyword      = {GENE,NTCA,PCC-7120,CYANOBACTERIUM ANABAENA-7120,HETEROCYST DIFFERENTIATION,EXPRESSION,SEQ,REGULATOR,FIXATION,METABOLISM},
  language     = {eng},
  pages        = {10},
  title        = {Directional RNA deep sequencing sheds new light on the transcriptional response of Anabaena sp strain PCC 7120 to combined-nitrogen deprivation},
  url          = {http://dx.doi.org/10.1186/1471-2164-12-332},
  volume       = {12},
  year         = {2011},
}

Chicago
Flaherty, Britt L, Filip Van Nieuwerburgh, Steven R Head, and James W Golden. 2011. “Directional RNA Deep Sequencing Sheds New Light on the Transcriptional Response of Anabaena Sp Strain PCC 7120 to Combined-nitrogen Deprivation.” Bmc Genomics 12.
APA
Flaherty, B. L., Van Nieuwerburgh, F., Head, S. R., & Golden, J. W. (2011). Directional RNA deep sequencing sheds new light on the transcriptional response of Anabaena sp strain PCC 7120 to combined-nitrogen deprivation. BMC GENOMICS, 12.
Vancouver
1.
Flaherty BL, Van Nieuwerburgh F, Head SR, Golden JW. Directional RNA deep sequencing sheds new light on the transcriptional response of Anabaena sp strain PCC 7120 to combined-nitrogen deprivation. BMC GENOMICS. 2011;12.
MLA
Flaherty, Britt L, Filip Van Nieuwerburgh, Steven R Head, et al. “Directional RNA Deep Sequencing Sheds New Light on the Transcriptional Response of Anabaena Sp Strain PCC 7120 to Combined-nitrogen Deprivation.” BMC GENOMICS 12 (2011): n. pag. Print.