RNase III-Binding-mRNAs Revealed Novel Complementary Transcripts in Streptomyces

. 2017 ; 8 () : 2693. [epub] 20180115

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid29379487

cis-Antisense RNAs (asRNAs) provide very simple and effective gene expression control due to the perfect complementarity between regulated and regulatory transcripts. In Streptomyces, the antibiotic-producing clade, the antisense control system is not yet understood, although it might direct the organism's complex development. Initial studies in Streptomyces have found a number of asRNAs. Apart from this, hundreds of mRNAs have been shown to bind RNase III, the double strand-specific endoribonuclease. In this study, we tested 17 mRNAs that have been previously co-precipitated with RNase III for antisense expression. Our RACE mapping showed that all of these mRNAs possess cognate asRNA. Additional tests for antisense expression uncovered as-adpA, as-rnc, as3983, as-sigB, as-sigH, and as-sigR RNAs. Northern blots detected the expression profiles of 18 novel transcripts. Noteworthy, we also found that only a minority of asRNAs respond to the absence of RNase III enzyme by increasing their cellular levels. Our findings suggest that antisense expression is widespread in Streptomyces, including genes of such important developmental regulators, as AdpA, RNase III, and sigma factors.

Zobrazit více v PubMed

Aceti D. J., Champness W. C. (1998). Transcriptional regulation of Streptomyces coelicolor pathway-specific antibiotic regulators by the absA and absB loci. J. Bacteriol. 180, 3100–3106. PubMed PMC

Adamidis T., Champness W. (1992). Genetic analysis of absB, a Streptomyces coelicolor locus involved in global antibiotic regulation. J. Bacteriol. 174, 4622–4628. 10.1128/jb.174.14.4622-4628.1992 PubMed DOI PMC

Blomberg P., Wagner E. G., Nordström K. (1990). Control of replication of plasmid R1: the duplex between the antisense RNA, CopA, and its target, CopT, is processed specifically in vivo and in vitro by RNase III. EMBO J. 9, 2331–2340. PubMed PMC

Bobek J., Strakova E., Zikova A., Vohradsky J. (2014). Changes in activity of metabolic and regulatory pathways during germination of S. coelicolor. BMC Genomics 15:1173. 10.1186/1471-2164-15-1173 PubMed DOI PMC

Carpousis A. J., Luisi B. F., McDowall K. J. (2009). Endonucleolytic initiation of mRNA decay in Escherichia coli. Prog. Mol. Biol. Transl. Sci. 85, 91–135. 10.1016/S0079-6603(08)00803-9 PubMed DOI

Chang S. A., Bralley P., Jones G. H. (2005). The absB gene encodes a double strand-specific endoribonuclease that cleaves the read-through transcript of the rpsO-pnp operon in Streptomyces coelicolor. J. Biol. Chem. 280, 33213–33219. 10.1074/jbc.M503440200 PubMed DOI

Chater K., Losick R. (1997). Mycelial life style of Streptomyces coelicolor A3 (2) and its relatives, in Bacteria as Multicellular Organisms, eds Chater K. F., Losick R., American Society for Microbiology (New York, NY: Oxford University Press; ), 149–182.

Conrad C., Rauhut R. (2002). Ribonuclease III: new sense from nuisance. Int. J. Biochem. Cell Biol. 34, 116–129. 10.1016/S1357-2725(01)00112-1 PubMed DOI

D'Alia D., Nieselt K., Steigele S., Müller J., Verburg I., Takano E. (2010). Noncoding RNA of glutamine synthetase I modulates antibiotic production in Streptomyces coelicolor A3(2). J. Bacteriol. 192, 1160–1164. 10.1128/JB.01374-09 PubMed DOI PMC

Drider D., Condon C. (2004). The continuing story of endoribonuclease III. J. Mol. Microbiol. Biotechnol. 8, 195–200. 10.1159/000086700 PubMed DOI

Durand S., Gilet L., Bessières P., Nicolas P., Condon C. (2012). Three essential ribonucleases-RNase Y, J1, and III-control the abundance of a majority of Bacillus subtilis mRNAs. PLoS Genet. 8:e1002520. 10.1371/journal.pgen.1002520 PubMed DOI PMC

Gatewood M. L., Bralley P., Weil M. R., Jones G. H. (2012). RNA-Seq and RNA immunoprecipitation analyses of the transcriptome of Streptomyces coelicolor identify substrates for RNase III. J. Bacteriol. 194, 2228–2237. 10.1128/JB.06541-11 PubMed DOI PMC

Geissmann T., Marzi S., Romby P. (2009). The role of mRNA structure in translational control in bacteria. RNA Biol. 6, 153–160. 10.4161/rna.6.2.8047 PubMed DOI

Georg J., Hess W. R. (2011). cis-antisense RNA, another level of gene regulation in bacteria. Microbiol. Mol. Biol. Rev. 75, 286–300. 10.1128/MMBR.00032-10 PubMed DOI PMC

Gerdes K., Nielsen A., Thorsted P., Wagner E. G. (1992). Mechanism of killer gene activation. Antisense RNA-dependent RNase III cleavage ensures rapid turn-over of the stable hok, srnB and pndA effector messenger RNAs. J. Mol. Biol. 226, 637–649. 10.1016/0022-2836(92)90621-P PubMed DOI

Gruber T. M., Gross C. A. (2003). Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 57, 441–466. 10.1146/annurev.micro.57.030502.090913 PubMed DOI

Higo A., Hara H., Horinouchi S., Ohnishi Y. (2012). Genome-wide distribution of AdpA, a global regulator for secondary metabolism and morphological differentiation in Streptomyces, revealed the extent and complexity of the AdpA regulatory network. DNA Res. 19, 259–273. 10.1093/dnares/dss010 PubMed DOI PMC

Hindra Moody M. J., Jones S. E., Elliot M. A. (2014). Complex intra-operonic dynamics mediated by a small RNA in Streptomyces coelicolor. PLoS ONE 9:e85856. 10.1371/journal.pone.0085856 PubMed DOI PMC

Huang J., Shi J., Molle V., Sohlberg B., Weaver D., Bibb M. J., et al. . (2005). Cross-regulation among disparate antibiotic biosynthetic pathways of Streptomyces coelicolor. Mol. Microbiol. 58, 1276–1287. 10.1111/j.1365-2958.2005.04879.x PubMed DOI

Jones S. E., Leong V., Ortega J., Elliot M. A. (2014). Development, antibiotic production, and ribosome assembly in Streptomyces venezuelae are impacted by RNase J and RNase III deletion. J. Bacteriol. 196, 4253–4267. 10.1128/JB.02205-14 PubMed DOI PMC

Kieser T. B. M., Buttner M. J., Chater K. F., Hopwood D. A. (2000). Practical Streptomyces Genetics, 2nd Edn. Norwich: John Innes Foundation.

Lasa I., Toledo-Arana A., Dobin A., Villanueva M., de los Mozos I. R., Vergara-Irigaray M., et al. . (2011). Genome-wide antisense transcription drives mRNA processing in bacteria. Proc. Natl. Acad. Sci. U.S.A. 108, 20172–20177. 10.1073/pnas.1113521108 PubMed DOI PMC

Lasa I., Toledo-Arana A., Gingeras T. R. (2012). An effort to make sense of antisense transcription in bacteria. RNA Biol. 9, 1039–1044. 10.4161/rna.21167 PubMed DOI PMC

Lee J. H., Gatewood M. L., Jones G. H. (2013). RNase III is required for actinomycin production in Streptomyces antibioticus. Appl. Environ. Microbiol. 79, 6447–6451. 10.1128/AEM.02272-13 PubMed DOI PMC

Le Rhun A., Beer Y. Y., Reimegård J., Chylinski K., Charpentier E. (2016). RNA sequencing uncovers antisense RNAs and novel small RNAs in Streptococcus pyogenes. RNA Biol. 13, 177–195. 10.1080/15476286.2015.1110674 PubMed DOI PMC

Lioliou E., Sharma C. M., Caldelari I., Helfer A. C., Fechter P., Vandenesch F., et al. . (2012). Global regulatory functions of the Staphylococcus aureus endoribonuclease III in gene expression. PLoS Genet. 8:e1002782. 10.1371/journal.pgen.1002782 PubMed DOI PMC

Lybecker M., Bilusic I., Raghavan R. (2014a). Pervasive transcription: detecting functional RNAs in bacteria. Transcription 5:e944039. 10.4161/21541272.2014.944039 PubMed DOI PMC

Lybecker M., Zimmermann B., Bilusic I., Tukhtubaeva N., Schroeder R. (2014b). The double-stranded transcriptome of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 111, 3134–3139. 10.1073/pnas.1315974111 PubMed DOI PMC

MacRae I. J., Doudna J. A. (2007). Ribonuclease revisited: structural insights into ribonuclease III family enzymes. Curr. Opin. Struct. Biol. 17, 138–145. 10.1016/j.sbi.2006.12.002 PubMed DOI

Mikulík K., Bobek J., Zídková J., Felsberg J. (2014). 6S RNA modulates growth and antibiotic production in Streptomyces coelicolor. Appl. Microbiol. Biotechnol. 98, 7185–7197. 10.1007/s00253-014-5806-4 PubMed DOI

Mitschke J., Georg J., Scholz I., Sharma C. M., Dienst D., Bantscheff J., et al. . (2011a). An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc. Natl. Acad. Sci. U.S.A. 108, 2124–2129. 10.1073/pnas.1015154108 PubMed DOI PMC

Mitschke J., Vioque A., Haas F., Hess W. R., Muro-Pastor A. M. (2011b). Dynamics of transcriptional start site selection during nitrogen stress-induced cell differentiation in Anabaena sp. PCC7120. Proc. Natl. Acad. Sci. U.S.A. 108, 20130–20135. 10.1073/pnas.1112724108 PubMed DOI PMC

Moody M. J., Young R. A., Jones S. E., Elliot M. A. (2013). Comparative analysis of non-coding RNAs in the antibiotic-producing Streptomyces bacteria. BMC Genomics 14:558. 10.1186/1471-2164-14-558 PubMed DOI PMC

Nicolas P., Mäder U., Dervyn E., Rochat T., Leduc A., Pigeonneau N., et al. . (2012). Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335, 1103–1106. 10.1126/science.1206848 PubMed DOI

Palecková P., Felsberg J., Bobek J., Mikulík K. (2007). tmRNA abundance in Streptomyces aureofaciens, S. griseus and S. collinus under stress-inducing conditions. Folia Microbiol. (Praha) 52, 463–470. 10.1007/BF02932105 PubMed DOI

Pánek J., Bobek J., Mikulík K., Basler M., Vohradský J. (2008). Biocomputational prediction of small non-coding RNAs in Streptomyces. BMC Genomics 9:217. 10.1186/1471-2164-9-217 PubMed DOI PMC

Papenfort K., Vogel J. (2009). Multiple target regulation by small noncoding RNAs rewires gene expression at the post-transcriptional level. Res. Microbiol. 160, 278–287. 10.1016/j.resmic.2009.03.004 PubMed DOI

Price B., Adamidis T., Kong R., Champness W. (1999). A Streptomyces coelicolor antibiotic regulatory gene, absB, encodes an RNase III homolog. J. Bacteriol. 181, 6142–6151. PubMed PMC

Robertson H. D. (1982). Escherichia coli ribonuclease III cleavage sites. Cell 30, 669–672. 10.1016/0092-8674(82)90270-7 PubMed DOI

Romby P., Charpentier E. (2010). An overview of RNAs with regulatory functions in gram-positive bacteria. Cell. Mol. Life Sci. 67, 217–237. 10.1007/s00018-009-0162-8 PubMed DOI PMC

Sello J. K., Buttner M. J. (2008). The gene encoding RNase III in Streptomyces coelicolor is transcribed during exponential phase and is required for antibiotic production and for proper sporulation. J. Bacteriol. 190, 4079–4083. 10.1128/JB.01889-07 PubMed DOI PMC

Sharma C. M., Hoffmann S., Darfeuille F., Reignier J., Findeiss S., Sittka A., et al. . (2010). The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464, 250–255. 10.1038/nature08756 PubMed DOI

Strakova E., Bobek J., Zikova A., Rehulka P., Benada O., Rehulkova H., et al. . (2013). Systems insight into the spore germination of Streptomyces coelicolor. J. Proteome Res. 12, 525–536. 10.1021/pr300980v PubMed DOI

Sun X., Zhulin I., Wartell R. M. (2002). Predicted structure and phyletic distribution of the RNA-binding protein Hfq. Nucleic Acids Res. 30, 3662–3671. 10.1093/nar/gkf508 PubMed DOI PMC

Swiercz J. P., Hindra Bobek J., Bobek J., Haiser H. J., Di Berardo C., et al. . (2008). Small non-coding RNAs in Streptomyces coelicolor. Nucleic Acids Res. 36, 7240–7251. 10.1093/nar/gkn898 PubMed DOI PMC

Taverniti V., Forti F., Ghisotti D., Putzer H. (2011). Mycobacterium smegmatis RNase J is a 5'-3' exo-/endoribonuclease and both RNase J and RNase E are involved in ribosomal RNA maturation. Mol. Microbiol. 82, 1260–1276. 10.1111/j.1365-2958.2011.07888.x PubMed DOI

Thomason M. K., Storz G. (2010). Bacterial antisense RNAs: how many are there, and what are they doing? Annu. Rev. Genet. 44, 167–188. 10.1146/annurev-genet-102209-163523 PubMed DOI PMC

Untergasser A., Cutcutache I., Koressaar T., Ye J., Faircloth B. C., Remm M., et al. . (2012). Primer3–new capabilities and interfaces. Nucleic Acids Res. 40:e115. 10.1093/nar/gks596 PubMed DOI PMC

Van Dessel W., Van Mellaert L., Geukens N., Lammertyn E., Anné J. (2004). Isolation of high quality RNA from Streptomyces. J. Microbiol. Methods 58, 135–137. 10.1016/j.mimet.2004.03.015 PubMed DOI

Viegas S. C., Pfeiffer V., Sittka A., Silva I. J., Vogel J., Arraiano C. M. (2007). Characterization of the role of ribonucleases in Salmonella small RNA decay. Nucleic Acids Res. 35, 7651–7664. 10.1093/nar/gkm916 PubMed DOI PMC

Vockenhuber M. P., Sharma C. M., Statt M. G., Schmidt D., Xu Z., Dietrich S., et al. . (2011). Deep sequencing-based identification of small non-coding RNAs in Streptomyces coelicolor. RNA Biol. 8, 468–477. 10.4161/rna.8.3.14421 PubMed DOI PMC

Waters L. S., Storz G. (2009). Regulatory RNAs in bacteria. Cell 136, 615–628. 10.1016/j.cell.2009.01.043 PubMed DOI PMC

Xu W., Huang J., Cohen S. N. (2008). Autoregulation of AbsB (RNase III) expression in Streptomyces coelicolor by endoribonucleolytic cleavage of absB operon transcripts. J. Bacteriol. 190, 5526–5530. 10.1128/JB.00558-08 PubMed DOI PMC

Xu W., Huang J., Lin R., Shi J., Cohen S. N. (2010). Regulation of morphological differentiation in S. coelicolor by RNase III (AbsB) cleavage of mRNA encoding the AdpA transcription factor. Mol. Microbiol. 75, 781–791. 10.1111/j.1365-2958.2009.07023.x PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...