Identification of a novel nanoRNase in Free

Abstract

In only one essential oligoribonuclease (Orn) can degrade oligoribonucleotides of five residues and shorter in length (nanoRNA). In NrnA and NrnB, which do not show any sequence similarity to Orn, have been identified as functional analogues of Orn. Sequence comparisons did not identify , or homologues in the genomes of the / and family members. Screening a genomic library from a member of the , for genes that can complement a conditional mutant in , we identified BA0969 (NrnC) as a functional analogue of Orn. NrnC is highly conserved (more than 80 % identity) in the genomes sequenced to date. Biochemical characterization showed that this protein exhibits oligo RNA degradation activity (nanoRNase activity). Like Orn from , NrnC is inhibited by micromolar amounts of 3′-phosphoadenosine 5′-phosphate . NrnC homologues are widely present in genomes of . Knock down of decreases the growth ability of , demonstrating the importance of nanoRNase activity in this bacterium.

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2012-04-01
2024-03-29
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References

  1. Alsmark C. M., Frank A. C., Karlberg E. O., Legault B. A., Ardell D. H., Canbäck B., Eriksson A. S., Näslund A. K., Handley S. A. & other authors ( 2004). The louse-borne human pathogen Bartonella quintana is a genomic derivative of the zoonotic agent Bartonella henselae . Proc Natl Acad Sci U S A 101:9716–9721 [View Article][PubMed]
    [Google Scholar]
  2. Arraiano C. M., Andrade J. M., Domingues S., Guinote I. B., Malecki M., Matos R. G., Moreira R. N., Pobre V., Reis F. P. & other authors ( 2010). The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol Rev 34:883–923[PubMed]
    [Google Scholar]
  3. Breitschwerdt E. B., Maggi R. G., Chomel B. B., Lappin M. R. ( 2010). Bartonellosis: an emerging infectious disease of zoonotic importance to animals and human beings. J Vet Emerg Crit Care (San Antonio) 20:8–30 [View Article][PubMed]
    [Google Scholar]
  4. Cheng Z. F., Deutscher M. P. ( 2002). Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison with RNase II. J Biol Chem 277:21624–21629 [View Article][PubMed]
    [Google Scholar]
  5. Chomel B. B., Boulouis H. J., Breitschwerdt E. B., Kasten R. W., Vayssier-Taussat M., Birtles R. J., Koehler J. E., Dehio C. ( 2009). Ecological fitness and strategies of adaptation of Bartonella species to their hosts and vectors. Vet Res 40:29 [View Article][PubMed]
    [Google Scholar]
  6. Condon C. ( 2007). Maturation and degradation of RNA in bacteria. Curr Opin Microbiol 10:271–278 [View Article][PubMed]
    [Google Scholar]
  7. Datta A. K., Niyogi K. ( 1975). A novel oligoribonuclease of Escherichia coli. II. Mechanism of action. J Biol Chem 250:7313–7319[PubMed]
    [Google Scholar]
  8. Dower W. J., Miller J. F., Ragsdale C. W. ( 1988). High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res 16:6127–6145 [View Article][PubMed]
    [Google Scholar]
  9. Fang M., Zeisberg W. M., Condon C., Ogryzko V., Danchin A., Mechold U. ( 2009). Degradation of nanoRNA is performed by multiple redundant RNases in Bacillus subtilis . Nucleic Acids Res 37:5114–5125 [View Article][PubMed]
    [Google Scholar]
  10. Ghosh S., Deutscher M. P. ( 1999). Oligoribonuclease is an essential component of the mRNA decay pathway. Proc Natl Acad Sci U S A 96:4372–4377 [View Article][PubMed]
    [Google Scholar]
  11. Gillaspie D., Perkins I., Larsen K., McCord A., Pangonis S., Sweger D., Seleem M. N., Sriranganathan N., Anderson B. E. ( 2009). Plasmid-based system for high-level gene expression and antisense gene knockdown in Bartonella henselae . Appl Environ Microbiol 75:5434–5436 [View Article][PubMed]
    [Google Scholar]
  12. Goldman S. R., Sharp J. S., Vvedenskaya I. O., Livny J., Dove S. L., Nickels B. E. ( 2011). NanoRNAs prime transcription initiation in vivo . Mol Cell 42:817–825 [View Article][PubMed]
    [Google Scholar]
  13. Guerra H. ( 2007). The Brucellae and their success as pathogens. Crit Rev Microbiol 33:325–331 [View Article][PubMed]
    [Google Scholar]
  14. Guptill L. ( 2010). Bartonellosis. Vet Microbiol 140:347–359 [View Article][PubMed]
    [Google Scholar]
  15. Guzman L. M., Belin D., Carson M. J., Beckwith J. ( 1995). Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121–4130[PubMed]
    [Google Scholar]
  16. Laemmli U. K. ( 1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [View Article][PubMed]
    [Google Scholar]
  17. Lagesen K., Ussery D. W., Wassenaar T. M. ( 2010). Genome update: the 1000th genome – a cautionary tale. Microbiology 156:603–608 [View Article][PubMed]
    [Google Scholar]
  18. Mechold U., Ogryzko V., Ngo S., Danchin A. ( 2006). Oligoribonuclease is a common downstream target of lithium-induced pAp accumulation in Escherichia coli and human cells. Nucleic Acids Res 34:2364–2373 [View Article][PubMed]
    [Google Scholar]
  19. Mechold U., Fang G., Ngo S., Ogryzko V., Danchin A. ( 2007). YtqI from Bacillus subtilis has both oligoribonuclease and pAp-phosphatase activity. Nucleic Acids Res 35:4552–4561 [View Article][PubMed]
    [Google Scholar]
  20. Miller J. H. ( 1972). Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  21. Minnick M. F., Battisti J. M. ( 2009). Pestilence, persistence and pathogenicity: infection strategies of Bartonella . Future Microbiol 4:743–758 [View Article][PubMed]
    [Google Scholar]
  22. Mueller K., González J. E. ( 2011). Complex regulation of symbiotic functions is coordinated by MucR and quorum sensing in Sinorhizobium meliloti . J Bacteriol 193:485–496 [View Article][PubMed]
    [Google Scholar]
  23. Nickels B. E., Dove S. L. ( 2011). NanoRNAs: a class of small RNAs that can prime transcription initiation in bacteria. J Mol Biol 412:772–781 [View Article][PubMed]
    [Google Scholar]
  24. Niyogi S. K., Datta A. K. ( 1975). A novel oligoribonuclease of Escherichia coli. I. Isolation and properties. J Biol Chem 250:7307–7312[PubMed]
    [Google Scholar]
  25. Postic G., Danchin A., Mechold U. ( 2012). Characterization of NrnA homologs from Mycobacterium tuberculosis and Mycoplasma pneumoniae . RNA 18:155–165[PubMed] [CrossRef]
    [Google Scholar]
  26. Riess T., Anderson B., Fackelmayer A., Autenrieth I. B., Kempf V. A. J. ( 2003). Rapid and efficient transposon mutagenesis of Bartonella henselae by transposome technology. Gene 313:103–109 [View Article][PubMed]
    [Google Scholar]
  27. Riess T., Dietrich F., Schmidt K. V., Kaiser P. O., Schwarz H., Schäfer A., Kempf V. A. ( 2008). Analysis of a novel insect cell culture medium-based growth medium for Bartonella species. Appl Environ Microbiol 74:5224–5227 [View Article][PubMed]
    [Google Scholar]
  28. Sambrook J., Fritsch E. F., Maniatis T. ( 1989). Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  29. Stacey G., Libault M., Brechenmacher L., Wan J., May G. D. ( 2006). Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol 9:110–121[PubMed]
    [Google Scholar]
  30. Vincent H. A., Deutscher M. P. ( 2006). Substrate recognition and catalysis by the exoribonuclease RNase R. J Biol Chem 281:29769–29775[PubMed]
    [Google Scholar]
  31. Yu D., Deutscher M. P. ( 1995). Oligoribonuclease is distinct from the other known exoribonucleases of Escherichia coli . J Bacteriol 177:4137–4139[PubMed]
    [Google Scholar]
  32. Zhang J., Biswas I. ( 2009). 3′-Phosphoadenosine-5′-phosphate phosphatase activity is required for superoxide stress tolerance in Streptococcus mutans . J Bacteriol 191:4330–4340 [View Article][PubMed]
    [Google Scholar]
  33. Zhang X., Zhu L., Deutscher M. P. ( 1998). Oligoribonuclease is encoded by a highly conserved gene in the 3′-5′ exonuclease superfamily. J Bacteriol 180:2779–2781[PubMed]
    [Google Scholar]
  34. Zuo Y., Deutscher M. P. ( 2001). Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res 29:1017–1026 [View Article][PubMed]
    [Google Scholar]
  35. Zuo Y., Wang Y., Malhotra A. ( 2005). Crystal structure of Escherichia coli RNase D, an exoribonuclease involved in structured RNA processing. Structure 13:973–984 [View Article][PubMed]
    [Google Scholar]
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