1887

Abstract

In recent years, it has become increasingly evident that post-transcriptional control mechanisms are the principal source of gene regulation for a large number of prokaryotic genetic pathways, particularly those involved in virulence and environmental adaptation. Post-transcriptional regulation is largely governed by RNA stability, which itself is determined by target accessibility to RNase degradation. In most Firmicutes species, mRNA stability is strongly impacted by the activity of two recently discovered RNases referred to as RNase J1 and RNase J2. Little is known about RNase J1 function in bacteria and even less is known about RNase J2. In the current study, we mutated both RNase J orthologues in to determine their functional roles in the cell. Single and double RNase J mutants were viable, but grew very slowly on agar plates. All of the mutants shared substantial defects in growth, morphology, acid tolerance, natural competence and biofilm formation. However, most of these defects were more severe in the RNase J2 mutant. Phenotypic suppression results also implicate a role for RNase J2 as a regulator of RNase J1 function. Unlike , RNase J2 is a major pleiotropic regulator in , which indicates some fundamental differences from in global gene regulation. Key conserved residues among the RNase J2 orthologues of lactic acid bacteria may hint at a greater role for RNase J2 in these species.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000039
2015-04-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/4/797.html?itemId=/content/journal/micro/10.1099/mic.0.000039&mimeType=html&fmt=ahah

References

  1. Ajdić D., McShan W. M., McLaughlin R. E., Savić G., Chang J., Carson M. B., Primeaux C., Tian R., Kenton S. et al. ( 2002;). Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. . Proc Natl Acad Sci U S A 99:, 14434–14439. [CrossRef][PubMed]
    [Google Scholar]
  2. Bechhofer D. H.. ( 2011;). Bacillus subtilis mRNA decay: new parts in the toolkit. . Wiley Interdiscip Rev RNA 2:, 387–394. [CrossRef][PubMed]
    [Google Scholar]
  3. Bugrysheva J. V., Scott J. R.. ( 2010;). The ribonucleases J1 and J2 are essential for growth and have independent roles in mRNA decay in Streptococcus pyogenes. . Mol Microbiol 75:, 731–743. [CrossRef][PubMed]
    [Google Scholar]
  4. Chen Y. Y., LeBlanc D. J.. ( 1992;). Genetic analysis of scrA and scrB from Streptococcus sobrinus 6715. . Infect Immun 60:, 3739–3746.[PubMed]
    [Google Scholar]
  5. Condon C.. ( 2010;). What is the role of RNase J in mRNA turnover?. RNA Biol 7:, 316–321. [CrossRef][PubMed]
    [Google Scholar]
  6. Dominski Z., Carpousis A. J., Clouet-d’Orval B.. ( 2013;). Emergence of the β-CASP ribonucleases: highly conserved and ubiquitous metallo-enzymes involved in messenger RNA maturation and degradation. . Biochim Biophys Acta 1829:, 532–551. [CrossRef][PubMed]
    [Google Scholar]
  7. Even S., Pellegrini O., Zig L., Labas V., Vinh J., Bréchemmier-Baey D., Putzer H.. ( 2005;). Ribonucleases J1 and J2: two novel endoribonucleases in B.subtilis with functional homology to E.coli RNase E. . Nucleic Acids Res 33:, 2141–2152. [CrossRef][PubMed]
    [Google Scholar]
  8. Figaro S., Durand S., Gilet L., Cayet N., Sachse M., Condon C.. ( 2013;). Bacillus subtilis mutants with knockouts of the genes encoding ribonucleases RNase Y and RNase J1 are viable, with major defects in cell morphology, sporulation, and competence. . J Bacteriol 195:, 2340–2348. [CrossRef][PubMed]
    [Google Scholar]
  9. Gao P., Pinkston K. L., Nallapareddy S. R., van Hoof A., Murray B. E., Harvey B. R.. ( 2010;). Enterococcus faecalis rnjB is required for pilin gene expression and biofilm formation. . J Bacteriol 192:, 5489–5498. [CrossRef][PubMed]
    [Google Scholar]
  10. Gripenland J., Netterling S., Loh E., Tiensuu T., Toledo-Arana A., Johansson J.. ( 2010;). RNAs: regulators of bacterial virulence. . Nat Rev Microbiol 8:, 857–866. [CrossRef][PubMed]
    [Google Scholar]
  11. Hoe C. H., Raabe C. A., Rozhdestvensky T. S., Tang T. H.. ( 2013;). Bacterial sRNAs: regulation in stress. . Int J Med Microbiol 303:, 217–229. [CrossRef][PubMed]
    [Google Scholar]
  12. Jamalli A., Hébert A., Zig L., Putzer H.. ( 2014;). Control of expression of the RNases J1 and J2 in Bacillus subtilis. . J Bacteriol 196:, 318–324. [CrossRef][PubMed]
    [Google Scholar]
  13. Jensen M. E., Wefel J. S.. ( 1989;). Human plaque pH responses to meals and the effects of chewing gum. . Br Dent J 167:, 204–208. [CrossRef][PubMed]
    [Google Scholar]
  14. Jensen M. E., Polansky P. J., Schachtele C. F.. ( 1982;). Plaque sampling and telemetry for monitoring acid production on human buccal tooth surfaces. . Arch Oral Biol 27:, 21–31. [CrossRef][PubMed]
    [Google Scholar]
  15. Khajotia S. S., Smart K. H., Pilula M., Thompson D. M.. ( 2013;). Concurrent quantification of cellular and extracellular components of biofilms. . J Vis Exp (82), e50639.[PubMed]
    [Google Scholar]
  16. Lehnik-Habrink M., Lewis R. J., Mäder U., Stülke J.. ( 2012;). RNA degradation in Bacillus subtilis: an interplay of essential endo- and exoribonucleases. . Mol Microbiol 84:, 1005–1017. [CrossRef][PubMed]
    [Google Scholar]
  17. Linder P., Lemeille S., Redder P.. ( 2014;). Transcriptome-wide analyses of 5′-ends in RNase J mutants of a gram-positive pathogen reveal a role in RNA maturation, regulation and degradation. . PLoS Genet 10:, e1004207. [CrossRef][PubMed]
    [Google Scholar]
  18. Liu N., Niu G., Xie Z., Chen Z., Itzek A., Kreth J., Gillaspy A., Zeng L., Burne R. et al. ( 2015;). The Streptococcus mutans irvA Gene Encodes a trans-Acting Riboregulatory mRNA. . Mol Cell 57:, 179–190. [CrossRef][PubMed]
    [Google Scholar]
  19. Mathy N., Bénard L., Pellegrini O., Daou R., Wen T., Condon C.. ( 2007;). 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA. . Cell 129:, 681–692. [CrossRef][PubMed]
    [Google Scholar]
  20. Mathy N., Hébert A., Mervelet P., Bénard L., Dorléans A., Li de la Sierra-Gallay I., Noirot P., Putzer H., Condon C.. ( 2010;). Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour. . Mol Microbiol 75:, 489–498. [CrossRef][PubMed]
    [Google Scholar]
  21. Matsui R., Cvitkovitch D.. ( 2010;). Acid tolerance mechanisms utilized by Streptococcus mutans. . Future Microbiol 5:, 403–417. [CrossRef][PubMed]
    [Google Scholar]
  22. Merritt J., Chen Z., Liu N., Kreth J.. ( 2014;). Posttranscriptional regulation of oral bacterial adaptive responses. . Curr Oral Health Rep 1:, 50–58. [CrossRef][PubMed]
    [Google Scholar]
  23. Newman J. A., Hewitt L., Rodrigues C., Solovyova A., Harwood C. R., Lewis R. J.. ( 2011;). Unusual, dual endo- and exonuclease activity in the degradosome explained by crystal structure analysis of RNase J1. . Structure 19:, 1241–1251. [CrossRef][PubMed]
    [Google Scholar]
  24. Repoila F., Majdalani N., Gottesman S.. ( 2003;). Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. . Mol Microbiol 48:, 855–861. [CrossRef][PubMed]
    [Google Scholar]
  25. Shahbabian K., Jamalli A., Zig L., Putzer H.. ( 2009;). RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. . EMBO J 28:, 3523–3533. [CrossRef][PubMed]
    [Google Scholar]
  26. Storz G., Vogel J., Wassarman K. M.. ( 2011;). Regulation by small RNAs in bacteria: expanding frontiers. . Mol Cell 43:, 880–891. [CrossRef][PubMed]
    [Google Scholar]
  27. Szostak M. P., Hensel A., Eko F. O., Klein R., Auer T., Mader H., Haslberger A., Bunka S., Wanner G., Lubitz W.. ( 1996;). Bacterial ghosts: non-living candidate vaccines. . J Biotechnol 44:, 161–170. [CrossRef][PubMed]
    [Google Scholar]
  28. Xie Z., Qi F., Merritt J.. ( 2013;). Cloning-independent plasmid construction for genetic studies in streptococci. . J Microbiol Methods 94:, 77–82. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000039
Loading
/content/journal/micro/10.1099/mic.0.000039
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error