DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Distinct and redundant functions of three homologs of RNase III in the cyanobacterium Synechococcus sp. strain PCC 7002

Journal Article · · Nucleic Acids Research
DOI: https://doi.org/10.1093/nar/gky041 · OSTI ID:1430778
 [1];  [2]; ORCiD logo [1]
  1. Univ. of Wisconsin, Madison, WI (United States). Dept. of Chemical and Biological Engineering, and Microbiology Doctoral Training Program
  2. Univ. of Wisconsin, Madison, WI (United States). Dept. of Chemical and Biological Engineering; Univ. of Colorado, Boulder, CO (United States). Dept. of Chemistry and Biochemistry

RNase III is a ribonuclease that recognizes and cleaves double-stranded RNA. Across bacteria, RNase III is involved in rRNA maturation, CRISPR RNA maturation, controlling gene expression, and turnover of messenger RNAs. Many organisms have only one RNase III while others have both a full-length RNase III and another version that lacks a double-stranded RNA binding domain (mini-III). The genome of the cyanobacterium Synechococcus sp. strain PCC 7002 (PCC 7002) encodes three homologs of RNase III, two full-length and one mini-III, that are not essential even when deleted in combination. To discern if each enzyme had distinct responsibilities, we collected and sequenced global RNA samples from the wild type strain, the single, double, and triple RNase III mutants. Approximately 20% of genes were differentially expressed in various mutants with some operons and regulons showing complex changes in expression levels between mutants. Two RNase III's had a role in 23S rRNA maturation and the third was involved in copy number regulation one of six native plasmids. In vitro, purified RNase III enzymes were capable of cleaving some of the known Escherichia coli RNase III target sequences, highlighting the remarkably conserved substrate specificity between organisms yet complex regulation of gene expression.

Research Organization:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC); USDOE
Grant/Contract Number:
SC0010329
OSTI ID:
1430778
Alternate ID(s):
OSTI ID: 1502458
Journal Information:
Nucleic Acids Research, Vol. 46, Issue 4; ISSN 0305-1048
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (88)

Autoregulation of RNase III operon by mRNA processing. journal November 1989
Transcriptional Regulation of the CO2-Concentrating Mechanism in a Euryhaline, Coastal Marine Cyanobacterium, Synechococcus sp. Strain PCC 7002: Role of NdhR/CcmR journal February 2007
Bacterial ribosomal RNA in pieces: rRNA fragmentation in bacteria journal May 2005
How deep is deep enough for RNA-Seq profiling of bacterial transcriptomes? journal January 2012
Efficient engineering of chromosomal ribosome binding site libraries in mismatch repair proficient Escherichia coli text January 2017
Secondary structure and domain architecture of the 23S and 5S rRNAs journal June 2013
RNase III-Dependent Expression of the rpsO-pnpOperon of Streptomyces coelicolor journal July 2011
Arabidopsis Chloroplast Mini-Ribonuclease III Participates in rRNA Maturation and Intron Recycling journal February 2015
RNase III Cleaves Eukaryotic Preribosomal RNA at a U3 snoRNP-Dependent Site journal April 1996
Recombinant organisms for production of industrial products journal March 2010
Microbial engineering for the production of advanced biofuels journal August 2012
Feedback regulation of ribosomal protein gene expression in Escherichia coli: structural homology of ribosomal RNA and ribosomal protein MRNA. journal December 1980
The Phyre2 web portal for protein modeling, prediction and analysis journal May 2015
Mfold web server for nucleic acid folding and hybridization prediction journal July 2003
A renaissance in RNA synthetic biology: new mechanisms, applications and tools for the future journal October 2015
Escherichia coli Ribonuclease III: Affinity Purification of Hexahistidine-Tagged Enzyme and Assays for Substrate Binding and Cleavage book January 2001
Synthetic Riboswitches That Induce Gene Expression in Diverse Bacterial Species journal March 2011
Metabolic Engineering for the Production of Natural Products journal July 2011
Postmaturational Cleavage of 23s Ribosomal Ribonucleic Acid and Its Metabolic Control in the Blue-Green Alga Anacystis nidulans journal January 1973
Enzymatic assembly of DNA molecules up to several hundred kilobases journal April 2009
Gene-expression tools for the metabolic engineering of bacteria journal November 1999
Structural features of the plasmid pMV158-encoded transcriptional repressor CopG, a protein sharing similarities with both helix-turn-helix and β-sheet DNA binding proteins journal August 1998
CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III journal March 2011
YmdB: a stress-responsive ribonuclease-binding regulator of E. coli RNase III activity journal December 2008
CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III journal March 2011
Global Regulatory Functions of the Staphylococcus aureus Endoribonuclease III in Gene Expression journal June 2012
Functional interaction between RNase III and the Escherichia coli ribosome journal January 2003
RNase III cleavage is obligate for maturation but not for function of Escherichia coli pre-23S rRNA. journal January 1984
RNase III stimulates the translation of the cIII gene of bacteriophage lambda. journal September 1987
HTSeq--a Python framework to work with high-throughput sequencing data journal September 2014
PNPase autocontrols its expression by degrading a double-stranded structure in the pnp mRNA leader journal December 2001
Divergent mechanisms of 5' 23S rRNA IVS processing in the alpha-proteobacteria journal December 2000
Analysis of current and alternative phenol based RNA extraction methodologies for cyanobacteria journal January 2009
Mini-III, an unusual member of the RNase III family of enzymes, catalyses 23S ribosomal RNA maturation in B. subtilis journal June 2008
Global Regulatory Functions of the Staphylococcus aureus Endoribonuclease III in Gene Expression journal June 2012
A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in Escherichia coli journal December 2015
Complementary sequences 1700 nucleotides apart form a ribonuclease III cleavage site in Escherichia coli ribosomal precursor RNA. journal August 1978
Direct regulation of Escherichia coli ribosomal protein promoters by the transcription factors ppGpp and DksA journal March 2011
Autoregulation of AbsB (RNase III) Expression in Streptomyces coelicolor by Endoribonucleolytic Cleavage of absB Operon Transcripts journal June 2008
Synthetic Riboswitches That Induce Gene Expression in Diverse Bacterial Species journal October 2010
Coordinated, Differential Expression of Two Genes through Directed mRNA Cleavage and Stabilization by Secondary Structures journal December 2000
The Essential Function of B. subtilis RNase III Is to Silence Foreign Toxin Genes journal December 2012
Translation initiation of the replication initiator repB gene of promiscuous plasmid pMV158 is led by an extended non-SD sequence journal July 2013
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
Preparation of RNA from Bacteria Infected with Bacteriophages: A Case Study from the Marine Unicellular Synechococcus sp. WH7803 Infected by Phage S-PM2 book January 2009
Efficient engineering of chromosomal ribosome binding site libraries in mismatch repair proficient Escherichia coli text January 2017
Recombinant organisms for production of industrial products journal March 2010
Tunable protein degradation in bacteria journal November 2014
Secondary structure and domain architecture of the 23S and 5S rRNAs journal June 2013
Arabidopsis Chloroplast Mini-Ribonuclease III Participates in rRNA Maturation and Intron Recycling journal February 2015
Artificial repressors for controlling gene expression in bacteria journal January 2013
Coupled Transcriptomics for Differential Expression Analysis and Determination of Transcription Start Sites: Design and Bioinformatics book January 2021
Microbial engineering for the production of advanced biofuels journal August 2012
Alterations in Global Patterns of Gene Expression in Synechocystis sp. PCC 6803 in Response to Inorganic Carbon Limitation and the Inactivation of ndhR , a LysR Family Regulator journal November 2003
Single-cell genomics unveils a canonical origin of the diverse mitochondrial genomes of euglenozoans text January 2021
Characterization of the biochemical properties of Campylobacter jejuni RNase III journal November 2013
Genetic and genomic analysis of RNases in model cyanobacteria journal January 2015
Network analysis of transcriptomics expands regulatory landscapes in Synechococcus sp. PCC 7002 journal August 2016
Divergent mechanisms of 5' 23S rRNA IVS processing in the alpha-proteobacteria journal December 2000
Feedback regulation of ribosomal protein gene expression in Escherichia coli: structural homology of ribosomal RNA and ribosomal protein MRNA. journal December 1980
Autoregulation of RNase III operon by mRNA processing. journal November 1989
Direct regulation of Escherichia coli ribosomal protein promoters by the transcription factors ppGpp and DksA journal March 2011
PNPase autocontrols its expression by degrading a double-stranded structure in the pnp mRNA leader journal December 2001
Replication control of plasmid pLS1: efficient regulation of plasmid copy number is exerted by the combined action of two plasmid components, CopG and RNA II journal December 1995
Persistence of adoptively transferred T cells with a kinetically engineered IL-2 receptor agonist journal January 2020
Morphological and genetic characterization of the first Isospora species (I. lugensae n. sp.) from a Kerguelen petrel (Lugensa brevirostris) journal January 2021
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
Replication of the streptococcal plasmid pMV158 and derivatives in cell-free extracts of Escherichia coli journal March 1987
HTSeq--a Python framework to work with high-throughput sequencing data journal September 2014
Genetic and genomic analysis of RNases in model cyanobacteria journal January 2015
Network analysis of transcriptomics expands regulatory landscapes in Synechococcus sp. PCC 7002 journal August 2016
Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays journal December 2010
A renaissance in RNA synthetic biology: new mechanisms, applications and tools for the future journal October 2015
Mfold web server for nucleic acid folding and hybridization prediction journal July 2003
Engineering mRNA stability inE. coli by the addition of synthetic hairpins using a 5′ cassette system journal August 1997
Enzymatic assembly of DNA molecules up to several hundred kilobases journal April 2009
RNA Sequencing Identifies New RNase III Cleavage Sites in Escherichia coli and Reveals Increased Regulation of mRNA journal March 2017
Synthetic RNA modules for fine-tuning gene expression levels in yeast by modulating RNase III activity journal July 2011
Efficient engineering of chromosomal ribosome binding site libraries in mismatch repair proficient Escherichia coli journal September 2017
RNase III cleavage is obligate for maturation but not for function of Escherichia coli pre-23S rRNA. journal January 1984
Mini-III, an unusual member of the RNase III family of enzymes, catalyses 23S ribosomal RNA maturation in B. subtilis journal June 2008
The Phyre2 web portal for protein modeling, prediction and analysis journal May 2015
The copy number of plasmid pLS1 is regulated by two trans-acting plasmid products: the antisense RNA II and the repressor protein, RepA journal January 1992
Regulation of the Cyanobacterial CO2-Concentrating Mechanism Involves Internal Sensing of NADP+ and α-Ketogutarate Levels by Transcription Factor CcmR journal July 2012
Analysis of current and alternative phenol based RNA extraction methodologies for cyanobacteria journal January 2009
RNase III stimulates the translation of the cIII gene of bacteriophage lambda. journal September 1987
YmdB: a stress-responsive ribonuclease-binding regulator of E. coli RNase III activity journal December 2008
RNase III is positively regulated by T7 protein kinase. journal May 1983

Cited By (2)

Genetic Responses of Metabolically Active Limnospira indica Strain PCC 8005 Exposed to γ-Radiation during Its Lifecycle journal July 2021
RNase III, Ribosome Biogenesis and Beyond journal December 2021

Figures / Tables (7)