Genetic and genomic analysis of RNases in model cyanobacteria
Abstract
Cyanobacteria are diverse photosynthetic microbes with the ability to convert CO2 into useful products. However, metabolic engineering of cyanobacteria remains challenging because of the limited resources for modifying the expression of endogenous and exogenous biochemical pathways. Fine-tuned control of protein production will be critical to optimize the biological conversion of CO2 into desirable molecules. Messenger RNA (mRNA) are labile intermediates that play critical roles in determining the translation rate and steady state protein concentrations in the cell. The majority of studies on mRNA turnover have focused on the model heterotrophic bacteria Escherichia coli and Bacillus subtilis. These studies have elucidated many RNA modifying and processing enzymes and have highlighted the differences between these Gram-negative and Gram-positive bacteria, respectively. In contrast, much less is known about mRNA turnover in cyanobacteria. We generated a compendium of the major ribonucleases (RNases) and provide an in-depth analysis of RNase III-like enzymes in commonly studied and diverse cyanobacteria. Furthermore, using targeted gene deletion, we genetically dissected the RNases in Synechococcus sp. PCC 7002, one of the fastest growing and industrially attractive cyanobacterial strains. We found that all three cyanobacterial homologs of RNase III and a member of the RNase II/R family are not essential undermore »
- Authors:
-
- Univ. of Wisconsin-Madison, Madison, WI (United States)
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1466792
- Grant/Contract Number:
- SC0010329
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Photosynthesis Research
- Additional Journal Information:
- Journal Volume: 126; Journal Issue: 1; Journal ID: ISSN 0166-8595
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; mRNA; RNA; Ribonuclease; photosynthesis; cyanobacteria; synthetic biology; biofuels; comparative genomics
Citation Formats
Cameron, Jeffrey C., Gordon, Gina C., and Pfleger, Brian F. Genetic and genomic analysis of RNases in model cyanobacteria. United States: N. p., 2015.
Web. doi:10.1007/s11120-015-0076-2.
Cameron, Jeffrey C., Gordon, Gina C., & Pfleger, Brian F. Genetic and genomic analysis of RNases in model cyanobacteria. United States. https://doi.org/10.1007/s11120-015-0076-2
Cameron, Jeffrey C., Gordon, Gina C., and Pfleger, Brian F. Sat .
"Genetic and genomic analysis of RNases in model cyanobacteria". United States. https://doi.org/10.1007/s11120-015-0076-2. https://www.osti.gov/servlets/purl/1466792.
@article{osti_1466792,
title = {Genetic and genomic analysis of RNases in model cyanobacteria},
author = {Cameron, Jeffrey C. and Gordon, Gina C. and Pfleger, Brian F.},
abstractNote = {Cyanobacteria are diverse photosynthetic microbes with the ability to convert CO2 into useful products. However, metabolic engineering of cyanobacteria remains challenging because of the limited resources for modifying the expression of endogenous and exogenous biochemical pathways. Fine-tuned control of protein production will be critical to optimize the biological conversion of CO2 into desirable molecules. Messenger RNA (mRNA) are labile intermediates that play critical roles in determining the translation rate and steady state protein concentrations in the cell. The majority of studies on mRNA turnover have focused on the model heterotrophic bacteria Escherichia coli and Bacillus subtilis. These studies have elucidated many RNA modifying and processing enzymes and have highlighted the differences between these Gram-negative and Gram-positive bacteria, respectively. In contrast, much less is known about mRNA turnover in cyanobacteria. We generated a compendium of the major ribonucleases (RNases) and provide an in-depth analysis of RNase III-like enzymes in commonly studied and diverse cyanobacteria. Furthermore, using targeted gene deletion, we genetically dissected the RNases in Synechococcus sp. PCC 7002, one of the fastest growing and industrially attractive cyanobacterial strains. We found that all three cyanobacterial homologs of RNase III and a member of the RNase II/R family are not essential under standard laboratory conditions, while homologs of RNase E/G, RNase J1/J2, PNPase, and a different member of the RNase II/R family appear to be essential for growth. In conclusion, this work will enhance our understanding of native control of gene expression and will facilitate the development of an RNA-based toolkit for metabolic engineering in cyanobacteria.},
doi = {10.1007/s11120-015-0076-2},
journal = {Photosynthesis Research},
number = 1,
volume = 126,
place = {United States},
year = {Sat Jan 17 00:00:00 EST 2015},
month = {Sat Jan 17 00:00:00 EST 2015}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 15 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
A protein is involved in accessibility of the inhibitor acetazolamide to the carbonic anhydrase(s) in the cyanobacterium Synechocystis PCC 6803
journal, February 1995
- Beuf, Laurent; B�du, Sylvie; Cami, Brigitte
- Plant Molecular Biology, Vol. 27, Issue 4
Positive Regulation of psbA Gene Expression by cis-Encoded Antisense RNAs in Synechocystis sp. PCC 6803
journal, August 2012
- Sakurai, Isamu; Stazic, Damir; Eisenhut, Marion
- Plant Physiology, Vol. 160, Issue 2
RNase E polypeptides lacking a carboxyl-terminal half suppress a mukB mutation in Escherichia coli.
journal, July 1996
- Kido, M.; Yamanaka, K.; Mitani, T.
- Journal of Bacteriology, Vol. 178, Issue 13
Properties of a Mutant from Synechocystis PCC6803 Resistant to Acetazolamide, an Inhibitor of Carbonic Anhydrase
journal, August 1990
- Bédu, Sylvie; Peltier, Gilles; Sarrey, Frédéric
- Plant Physiology, Vol. 93, Issue 4
The endoribonucleolytic N-terminal half of Escherichia coli RNase E is evolutionarily conserved in Synechocystis sp. and other bacteria but not the C-terminal half, which is sufficient for degradosome assembly
journal, September 1998
- Kaberdin, V. R.; Miczak, A.; Jakobsen, J. S.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 20
The phylogenetic distribution of bacterial ribonucleases
journal, December 2002
- Condon, C.
- Nucleic Acids Research, Vol. 30, Issue 24
Proteins associated with RNase E in a multicomponent ribonucleolytic complex.
journal, April 1996
- Miczak, A.; Kaberdin, V. R.; Wei, C. L.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 9
Function in Escherichia coli of the non-catalytic part of RNase E: role in the degradation of ribosome-free mRNA: The non-catalytic part of RNase E in vivo
journal, September 2002
- Leroy, Anne; Vanzo, Nathalie F.; Sousa, Sandra
- Molecular Microbiology, Vol. 45, Issue 5
Degradation of RNA in Escherichia coli: A hypothesis
journal, January 1973
- Apirion, David
- MGG Molecular & General Genetics, Vol. 122, Issue 4
An Organic Acid Based Counter Selection System for Cyanobacteria
journal, October 2013
- Begemann, Matthew B.; Zess, Erin K.; Walters, Eric M.
- PLoS ONE, Vol. 8, Issue 10
A DEAD-box RNA helicase in the Escherichia coli RNA degradosome
journal, May 1996
- Py, Béatrice; Higgins, Christopher F.; Krisch, Henry M.
- Nature, Vol. 381, Issue 6578
Initiation of RNA Decay in Escherichia coli by 5′ Pyrophosphate Removal
journal, July 2007
- Celesnik, Helena; Deana, Atilio; Belasco, Joel G.
- Molecular Cell, Vol. 27, Issue 1
Messenger RNA Turnover Processes in Escherichia coli, Bacillus subtilis , and Emerging Studies in Staphylococcus aureus
journal, January 2009
- Anderson, Kelsi L.; Dunman, Paul M.
- International Journal of Microbiology, Vol. 2009
Specialized Techniques for Site-Directed Mutagenesis in Cyanobacteria
book, January 2007
- Clerico, Eugenia M.; Ditty, Jayna L.; Golden, Susan S.
- Methods in Molecular Biology
Copurification of E. coli RNAase E and PNPase: Evidence for a specific association between two enzymes important in RNA processing and degradation
journal, March 1994
- Carpousis, Agamemnon J.; Van Houwe, Griet; Ehretsmann, Claude
- Cell, Vol. 76, Issue 5
An internal antisense RNA regulates expression of the photosynthesis gene isiA
journal, April 2006
- Duhring, U.; Axmann, I. M.; Hess, W. R.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 18
Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome
journal, September 1998
- Vanzo, N. F.; Li, Y. S.; Py, B.
- Genes & Development, Vol. 12, Issue 17
RNase III-dependent down-regulation of ftsH by an artificial internal sense RNA in Anabaena sp. PCC 7120
journal, May 2013
- Gao, Yuan; Gong, Yangmin; Xu, Xudong
- FEMS Microbiology Letters, Vol. 344, Issue 2
Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing
journal, December 2012
- Shih, P. M.; Wu, D.; Latifi, A.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 3, p. 1053-1058
Enzymatic assembly of DNA molecules up to several hundred kilobases
journal, April 2009
- Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan
- Nature Methods, Vol. 6, Issue 5, p. 343-345
WebLogo: A Sequence Logo Generator
journal, May 2004
- Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc
- Genome Research, Vol. 14, Issue 6, p. 1188-1190
Rapid cleavage of RNA by RNase E in the absence of 5′ monophosphate stimulation: Rapid 5′ monophosphate-independent cleavage by E. coli RNase E
journal, November 2009
- Kime, Louise; Jourdan, Stefanie S.; Stead, Jonathan A.
- Molecular Microbiology, Vol. 76, Issue 3
Ribonucleases J1 and J2: two novel endoribonucleases in B.subtilis with functional homology to E.coli RNase E
journal, April 2005
- Even, S.
- Nucleic Acids Research, Vol. 33, Issue 7
RNase E: at the interface of bacterial RNA processing and decay
journal, December 2012
- Mackie, George A.
- Nature Reviews Microbiology, Vol. 11, Issue 1
RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis
journal, September 2009
- Shahbabian, Karen; Jamalli, Ailar; Zig, Léna
- The EMBO Journal, Vol. 28, Issue 22
Mapping and characterization of a mutation in Escherichia coli that reduces the level of ribonuclease III specific for double-stranded ribonucleic acid.
journal, January 1975
- Apirion, D.; Watson, N.
- Journal of Bacteriology, Vol. 124, Issue 1
Chapter 1 Analysis of RNA Decay, Processing, and Polyadenylation in Escherichia coli and Other Prokaryotes
book, January 2008
- Mohanty, Bijoy K.; Giladi, Hili; Maples, Valerie F.
- RNA Turnover in Bacteria, Archaea and Organelles
Analysis Tool Web Services from the EMBL-EBI
journal, May 2013
- McWilliam, Hamish; Li, Weizhong; Uludag, Mahmut
- Nucleic Acids Research, Vol. 41, Issue W1
Ribonuclease III is involved in motility of Escherichia coli.
journal, January 1978
- Apirion, D.; Watson, N.
- Journal of Bacteriology, Vol. 133, Issue 3
The Small Regulatory RNA SyR1/PsrR1 Controls Photosynthetic Functions in Cyanobacteria
journal, September 2014
- Georg, J.; Dienst, D.; Schurgers, N.
- The Plant Cell, Vol. 26, Issue 9
The rnb Gene of Synechocystis PCC6803 Encodes a RNA Hydrolase Displaying RNase II and Not RNase R Enzymatic Properties
journal, March 2012
- Matos, Rute G.; Fialho, Arsénio M.; Giloh, Mordechai
- PLoS ONE, Vol. 7, Issue 3
RNase E forms a complex with polynucleotide phosphorylase in cyanobacteria via a cyanobacterial-specific nonapeptide in the noncatalytic region
journal, February 2014
- Zhang, J. -Y.; Deng, X. -M.; Li, F. -P.
- RNA, Vol. 20, Issue 4
The Essential Function of B. subtilis RNase III Is to Silence Foreign Toxin Genes
journal, December 2012
- Durand, Sylvain; Gilet, Laetitia; Condon, Ciarán
- PLoS Genetics, Vol. 8, Issue 12
The Pfam protein families database
journal, November 2011
- Punta, M.; Coggill, P. C.; Eberhardt, R. Y.
- Nucleic Acids Research, Vol. 40, Issue D1
Chapter 3 Endonucleolytic Initiation of mRNA Decay in Escherichia coli
book, October 2009
- Carpousis, Agamemnon J.; Luisi, Ben F.; McDowall, Kenneth J.
- Progress in Molecular Biology and Translational Science
Maturation of the 5' end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1
journal, January 2007
- Britton, Robert A.; Wen, Tingyi; Schaefer, Laura
- Molecular Microbiology, Vol. 63, Issue 1
5′-to-3′ Exoribonuclease Activity in Bacteria: Role of RNase J1 in rRNA Maturation and 5′ Stability of mRNA
journal, May 2007
- Mathy, Nathalie; Bénard, Lionel; Pellegrini, Olivier
- Cell, Vol. 129, Issue 4
Mini-III, an unusual member of the RNase III family of enzymes, catalyses 23S ribosomal RNA maturation in B. subtilis
journal, June 2008
- Redko, Yulia; Bechhofer, David H.; Condon, Ciarán
- Molecular Microbiology, Vol. 68, Issue 5
RNase III: Genetics and Function; Structure and Mechanism
journal, November 2013
- Court, Donald L.; Gan, Jianhua; Liang, Yu-He
- Annual Review of Genetics, Vol. 47, Issue 1
Nucleotide sequence and further characterization of the Synechococcus sp. strain PCC 7002 recA gene: complementation of a cyanobacterial recA mutation by the Escherichia coli recA gene.
journal, February 1990
- Murphy, R. C.; Gasparich, G. E.; Bryant, D. A.
- Journal of Bacteriology, Vol. 172, Issue 2
Two pathways for RNase E action in Escherichia coli in vivo and bypass of its essentiality in mutants defective for Rho-dependent transcription termination: RNase E pathways and Rho-dependent transcription termination
journal, November 2011
- Anupama, K.; Leela, J. Krishna; Gowrishankar, J.
- Molecular Microbiology, Vol. 82, Issue 6
The bacterial enzyme RppH triggers messenger RNA degradation by 5′ pyrophosphate removal
journal, January 2008
- Deana, Atilio; Celesnik, Helena; Belasco, Joel G.
- Nature, Vol. 451, Issue 7176
What is the role of RNase J in mRNA turnover?
journal, May 2010
- Condon, Ciarán
- RNA Biology, Vol. 7, Issue 3
RNase E, an RNA processing enzyme from Escherichia coli.
journal, November 1979
- Misra, T. K.; Apirion, D.
- Journal of Biological Chemistry, Vol. 254, Issue 21
The Production of Hydrogen Peroxide by Blue-Green Algae: a Survey
journal, December 1973
- Stevens, S. E.; Patterson, C. O. Pat; Myers, Jack
- Journal of Phycology, Vol. 9, Issue 4
Works referencing / citing this record:
Inactivation of the RNA helicase CrhR impacts a specific subset of the transcriptome in the cyanobacterium Synechocystis sp. PCC 6803
journal, October 2018
- Georg, Jens; Rosana, Albert Remus R.; Chamot, Danuta
- RNA Biology, Vol. 16, Issue 9
Magnesium Deficiency Induced Global Transcriptome Change in Citrus sinensis Leaves Revealed by RNA-Seq
journal, June 2019
- Yang,
- International Journal of Molecular Sciences, Vol. 20, Issue 13
Distinct and redundant functions of three homologs of RNase III in the cyanobacterium Synechococcus sp. strain PCC 7002
journal, January 2018
- Gordon, Gina C.; Cameron, Jeffrey C.; Pfleger, Brian F.
- Nucleic Acids Research, Vol. 46, Issue 4
Distinct and redundant functions of three homologs of RNase III in the cyanobacterium Synechococcus sp. strain PCC 7002
journal, January 2018
- Gordon, Gina C.; Cameron, Jeffrey C.; Pfleger, Brian F.
- Nucleic Acids Research, Vol. 46, Issue 4