Identification of a large noncoding RNA in extremophilic eubacteria

We have discovered a large and highly conserved RNA motif that typically resides in a noncoding section of a multigene messenger RNA in extremophilic Gram-positive eubacteria. RNAs of this class adopt an ornate secondary structure, are large compared with most other noncoding RNAs, and have been identified only in certain extremophilic bacteria. These ornate, large, extremophilic (OLE) RNAs have a length of ≈610 nucleotides, and the 35 representatives examined exhibit extraordinary conservation of nucleotide sequence and base pairing. Structural probing of the OLE RNA from Bacillus halodurans corroborates a complex secondary structure model predicted from comparative sequence analysis. The patterns of structural conservation, and its unique phylogenetic distribution, suggest that OLE RNA carries out a complex and critical function only in certain extremophilic bacteria.

[1]  R. Cavicchioli,et al.  Biology of the cold adapted archaeon, Methanococcoides burtonii determined by proteomics using liquid chromatography-tandem mass spectrometry. , 2004, Journal of proteome research.

[2]  S. Gottesman.  The small RNA regulators of Escherichia coli: roles and mechanisms*. , 2004, Annual review of microbiology.

[3]  P. Visscher,et al.  Microbial lithification in marine stromatolites and hypersaline mats. , 2005, Trends in microbiology.

[4]  Jeffrey E. Barrick,et al.  Riboswitches Control Fundamental Biochemical Pathways in Bacillus subtilis and Other Bacteria , 2003, Cell.

[5]  R. Breaker,et al.  Gene regulation by riboswitches , 2004, Nature Reviews Molecular Cell Biology.

[6]  Jennifer A. Doudna,et al.  A universal mode of helix packing in RNA , 2001, Nature Structural Biology.

[7]  A. Omer,et al.  Small non-coding RNAs in Archaea. , 2005, Current opinion in microbiology.

[8]  G. Storz,et al.  Identification of novel small RNAs using comparative genomics and microarrays. , 2001, Genes & development.

[9]  Ricardo Ciria,et al.  Conserved regulatory motifs in bacteria: riboswitches and beyond. , 2004, Trends in genetics : TIG.

[10]  S. Eddy,et al.  Computational identification of noncoding RNAs in E. coli by comparative genomics , 2001, Current Biology.

[11]  C. Zwieb,et al.  Comparative sequence analysis of tmRNA. , 1999, Nucleic acids research.

[12]  J. Vogel,et al.  RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. , 2003, Nucleic acids research.

[13]  S. Eddy,et al.  Noncoding RNA genes identified in AT-rich hyperthermophiles , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[14]  A. Hüttenhofer,et al.  Non-coding RNAs: hope or hype? , 2005, Trends in genetics : TIG.

[15]  W. L. Ruzzo,et al.  6S RNA is a widespread regulator of eubacterial RNA polymerase that resembles an open promoter. , 2005, RNA.

[16]  B. Meyer,et al.  Sensitive detection of bacterial transcription initiation sites and differentiation from RNA processing sites in the pheromone-induced plasmid transfer system of Enterococcus faecalis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Zasha Weinberg,et al.  CMfinder - a covariance model based RNA motif finding algorithm , 2006, Bioinform..

[18]  Michael T. McManus,et al.  Gene silencing in mammals by small interfering RNAs , 2002, Nature Reviews Genetics.

[19]  F. Costa,et al.  Non-coding RNAs: new players in eukaryotic biology. , 2005, Gene.

[20]  Jeffrey E. Barrick,et al.  New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[21]  G. Ourisson,et al.  Prokaryotic hopanoids and other polyterpenoid sterol surrogates. , 1987, Annual review of microbiology.

[22]  H. Margalit,et al.  Novel small RNA-encoding genes in the intergenic regions of Escherichia coli , 2001, Current Biology.

[23]  J. Mattick,et al.  Non-coding RNA. , 2006, Human molecular genetics.

[24]  E. Boye,et al.  The gene for 2-phosphoglycolate phosphatase (gph) in Escherichia coli is located in the same operon as dam and at least five other diverse genes. , 1999, Biochimica et biophysica acta.

[25]  G. Storz,et al.  An abundance of RNA regulators. , 2005, Annual review of biochemistry.

[26]  S. Tringe,et al.  Comparative Metagenomics of Microbial Communities , 2004, Science.

[27]  Roland K. Hartmann,et al.  6S RNA – an ancient regulator of bacterial RNA polymerase rediscovered , 2005, Biological chemistry.

[28]  R. Breaker,et al.  Regulation of bacterial gene expression by riboswitches. , 2005, Annual review of microbiology.

[29]  K. Wassarman,et al.  A highly conserved 6S RNA structure is required for regulation of transcription , 2005, Nature Structural &Molecular Biology.

[30]  Scott R. Miller,et al.  Unexpected Diversity and Complexity of the Guerrero Negro Hypersaline Microbial Mat , 2006, Applied and Environmental Microbiology.

[31]  P. Avner,et al.  Employment opportunities for non‐coding RNAs , 2004, FEBS letters.

[32]  Zasha Weinberg,et al.  A Glycine-Dependent Riboswitch That Uses Cooperative Binding to Control Gene Expression , 2004, Science.

[33]  G. Storz,et al.  Detection of 5′- and 3′-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli , 2005, Nucleic acids research.

[34]  H. Gemerden.  Microbial mats: A joint venture , 1993 .

[35]  Y Endo,et al.  Ribotoxin recognition of ribosomal RNA and a proposal for the mechanism of translocation. , 1992, Trends in biochemical sciences.

[36]  Jeffrey E. Barrick,et al.  Evidence for a second class of S-adenosylmethionine riboswitches and other regulatory RNA motifs in alpha-proteobacteria , 2005, Genome Biology.

[37]  M. Gelfand,et al.  Regulation of lysine biosynthesis and transport genes in bacteria: yet another RNA riboswitch? , 2003, Nucleic acids research.

[38]  G. Soukup,et al.  Riboswitches exert genetic control through metabolite-induced conformational change. , 2004, Current opinion in structural biology.

[39]  Stefan Schouten,et al.  Membrane lipids of mesophilic anaerobic bacteria thriving in peats have typical archaeal traits. , 2006, Environmental microbiology.

[40]  Zasha Weinberg,et al.  Sequence-based heuristics for faster annotation of non-coding RNA families , 2006, Bioinform..

[41]  M. Winkler,et al.  The mutL repair gene of Escherichia coli K‐12 forms a superoperon with a gene encoding a new cell‐wall amidase , 1994, Molecular microbiology.

[42]  Jörg Vogel,et al.  How to find small non-coding RNAs in bacteria , 2005, Biological chemistry.

[43]  Tatiana Tatusova,et al.  NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins , 2004, Nucleic Acids Res..

[44]  Joaquín Dopazo,et al.  PupasView: a visual tool for selecting suitable SNPs, with putative pathological effect in genes, for genotyping purposes , 2005, Nucleic Acids Res..

[45]  R R Breaker,et al.  Relationship between internucleotide linkage geometry and the stability of RNA. , 1999, RNA.

[46]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[47]  Thomas A. Steitz,et al.  RNA tertiary interactions in the large ribosomal subunit: The A-minor motif , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[48]  T. Henkin,et al.  The T box and S box transcription termination control systems. , 2003, Frontiers in bioscience : a journal and virtual library.

[49]  S. Gottesman.  Micros for microbes: non-coding regulatory RNAs in bacteria. , 2005, Trends in genetics : TIG.

[50]  O. White,et al.  Environmental Genome Shotgun Sequencing of the Sargasso Sea , 2004, Science.

[51]  J. Banfield,et al.  Community structure and metabolism through reconstruction of microbial genomes from the environment , 2004, Nature.