Geodesic
Products of abortive transcription can prime synthesis of chimeric oligonucleotides
Matematičeskaâ biologiâ i bioinformatika, Tome 19 (2024), pp. 453-471.

Voir la notice de l'article provenant de la source Math-Net.Ru

The aim of the study was to search for signal RNAs potentially utilized by bacteria for intercellular interactions. This was not limited to a certain category of regulatory RNAs, which are contained in large numbers in all domains of life. The search was performed using RNA-seq data obtained for a wild-type strain of E. coli and its mutant derivative $(\Delta dps)$ lacking the gene encoding nucleoid protein Dps. This protein can bind RNAs and is found in membrane structures, which indicates the possibility of its participation in their secretion. Since the spectra of intracellular and secreted RNAs differed, it was assumed that the secreted RNAs are somehow selected for secretion. Therefore, in the RNA sets with Dps-dependent secretion, we searched for and found reads with non-template nucleotides at the ends, point nucleotide substitutions, insertions and deletions, as well as regularly detected chimeras. One chimera with a 9-mer GCCAAGGCG at the 5'-end and a transcript from the fimA-fimI intergenic region at the 3'-end was chosen for detailed study. It was found that the 9-mer is a product of abortive transcription from the antisense promoter inside the ravA gene. It is efficiently secreted and forms chimeras with many RNAs, including their 5'-ends and fragments shortened from this terminus. Analysis of the 5'-ends of the 9-mer partners in different chimeras revealed their coding sites in the genome, a feature of which was the ability to form stable secondary structures and therefore cause transcription stops or pauses. The discovery of different chimeras with the 9-mer at the 5'-end witnesses that they are formed as a result of primed synthesis rather than random ligation. The possible biological role of transcription primed by abortive products, whose regulatory role has been established for the first time, is discussed. 
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     title = {Products of abortive transcription can prime synthesis of chimeric oligonucleotides},
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K. S. Shavkunov; N. Yu. Markelova; O. V. Alikina; O. A. Glazunova; V. V. Panyukov; N. P. Kolzhetsov; S. S. Kiselev; O. N. Ozoline. Products of abortive transcription can prime synthesis of chimeric oligonucleotides. Matematičeskaâ biologiâ i bioinformatika, Tome 19 (2024), pp. 453-471. http://geodesic.mathdoc.fr/item/MBB_2024_19_a6/

[1] M. Lybecker, I. Bilusic, R. Raghavan, “Pervasive transcription: detecting functional RNAs in bacteria”, Transcription, 5 (2014), e944039 <ext-link ext-link-type='doi' href='https://doi.org/10.4161/21541272.2014.944039'>10.4161/21541272.2014.944039</ext-link>

[2] E. Soltani-Fard, S. Taghvimi, Z. Abedi Kichi, C. Weber, Z. Shabaninejad, M. Taheri-Anganeh, S. Hossein Khatami, P. Mousavi, A. Movahedpour, L. Natarelli, “Insights into the function of regulatory RNAs in bacteria and archaea”, Int. J. Transl. Med, 1 (2021), 403–423 <ext-link ext-link-type='doi' href='https://doi.org/10.3390/ijtm1030024'>10.3390/ijtm1030024</ext-link>

[3] F. A. Lagunas-Rangel, “Role of circular RNAs in DNA repair”, RNA Biol, 21 (2024), 149–161 <ext-link ext-link-type='doi' href='https://doi.org/10.1080/15476286.2024.2429945'>10.1080/15476286.2024.2429945</ext-link>

[4] A. Dance, “Circular logic: understanding RNA's strangest form yet”, Nature, 635 (2024), 511–513 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/d41586-024-03683-w'>10.1038/d41586-024-03683-w</ext-link>

[5] A. L. Mamuye, E. Merelli, L. Tesei, A graph grammar for modelling RNA folding, 2016, arXiv: <ext-link ext-link-type='uri' href='https://arxiv.org/abs/1612.01639'>1612.01639</ext-link><ext-link ext-link-type='doi' href='https://doi.org/10.48550/arXiv.1612.01639'>10.48550/arXiv.1612.01639</ext-link>

[6] H. Wu, H. Yu, Y. Zhang, B. Yang, W. Sun, L. Ren, Y. Li, Q. Li, B. Liu, Y. Ding, H. Zhang, “Unveiling RNA structure-mediated regulations of RNA stability in wheat”, Nat. Commun, 15 (2024), 10042 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/s41467-024-54172-7'>10.1038/s41467-024-54172-7</ext-link>

[7] S. E. Harris, M. S. Alexis, G. Giri, F. F. Cavazos Jr, Y. Hu, J. Murn, M. M. Aleman, C. B. Burge, D. Dominguez, “Understanding species-specific and conserved RNA-protein interactions in vivo and in vitro”, Nat. Commun, 15 (2024), 8400 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/s41467-024-52231-7'>10.1038/s41467-024-52231-7</ext-link>

[8] T. C. Nguyen, K. Zaleta-Rivera, X. Huang, X. Dai, S. Zhong, “RNA. Action through Interactions”, Trends Genet, 34 (2018), 867–882 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.tig.2018.08.001'>10.1016/j.tig.2018.08.001</ext-link>

[9] M. Zhou, M. S. Xiao, Z. G. Li, C. Huang, “New progresses of circular RNA biology: from nuclear export to degradation”, RNA Biol, 18 (2021), 1365–1373 <ext-link ext-link-type='doi' href='https://doi.org/10.1080/15476286.2020.1853977'>10.1080/15476286.2020.1853977</ext-link>

[10] N. Innocenti, H. S. Nguyen, A. F. d'Herouel, E. Aurell, An observation of circular RNAs in bacterial RNA-seq data, 2016, arXiv: <ext-link ext-link-type='uri' href='https://arxiv.org/abs/1606.04576'>1606.04576</ext-link><ext-link ext-link-type='doi' href='https://doi.org/10.48550/arXiv.1606.04576'>10.48550/arXiv.1606.04576</ext-link>

[11] K. S. Shavkunov, N. Y. Markelova, O. A. Glazunova, N. P. Kolzhetsov, V. V. Panyukov, O. N. Ozoline, “The fate and functionality of alien tRNA fragments in culturing medium and cells of Escherichia coli”, Int. J. Mol. Sci, 24 (2023), 12960 <ext-link ext-link-type='doi' href='https://doi.org/10.3390/ijms241612960'>10.3390/ijms241612960</ext-link>

[12] M. C. Carrier, D. Lalaouna, E. Masse, “Broadening the definition of bacterial small RNAs: characteristics and mechanisms of action”, Annu. Rev. Microbiol, 72 (2018), 141–161 <ext-link ext-link-type='doi' href='https://doi.org/10.1146/annurev-micro-090817-062607'>10.1146/annurev-micro-090817-062607</ext-link>

[13] E. G.H. Wagner, P. Romby, “Small RNAs in bacteria and archaea: who they are, what they do, and how they do it”, Adv. Genet, 90 (2015), 133–208 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/bs.adgen.2015.05.001'>10.1016/bs.adgen.2015.05.001</ext-link>

[14] M. Miyakoshi, Y. Chao, J. Vogel, “Regulatory small RNAs from the 3' regions of bacterial mRNAs”, Curr. Opin. Microbiol, 24 (2015), 132–139 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.mib.2015.01.013'>10.1016/j.mib.2015.01.013</ext-link>

[15] Y. Chao, J. Vogel, “A 3' UTR-derived small RNA provides the regulatory noncoding arm of the inner membrane stress response”, Mol. Cell, 61 (2016), 352–363 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.molcel.2015.12.023'>10.1016/j.molcel.2015.12.023</ext-link>

[16] G. X. Ren, X. P. Guo, Y. C. Sun, “Regulatory 3'-untranslated regions of bacterial mRNAs”, Front. Microbiol, 8 (2017), 1276 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fmicb.2017.01276'>10.3389/fmicb.2017.01276</ext-link>

[17] A. C. Manna, S. Kim, L. Cengher, A. Corvaglia, S. Leo, P. Francois, A. L. Cheung, “Small RNA teg49 is derived from a sarA transcript and regulates virulence genes independent of SarA in Staphylococcus aureus”, Infect. Immun, 86 (2018), e00635-17 <ext-link ext-link-type='doi' href='https://doi.org/10.1128/IAI.00635-17'>10.1128/IAI.00635-17</ext-link>

[18] D. Lalaouna, M. C. Carrier, S. Semsey, J. S. Brouard, J. Wang, J. T. Wade, E. Masse, “A 3' external transcribed spacer in a tRNA transcript acts as a sponge for small RNAs to prevent transcriptional noise”, Mol. Cell, 58 (2015), 393–405 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.molcel.2015.03.013'>10.1016/j.molcel.2015.03.013</ext-link>

[19] J. Shepherd, M. Ibba, “Bacterial transfer RNAs”, FEMS Microbiol. Rev, 39 (2015), 280–300 <ext-link ext-link-type='doi' href='https://doi.org/10.1093/femsre/fuv004'>10.1093/femsre/fuv004</ext-link>

[20] K. W. Diebel, K. Zhou, A. B. Clarke, L. T. Bemis, “Beyond the ribosome: extra-translational functions of tRNA fragments”, Biomark. Insights., 11, Suppl. 1 (2016), 1–8 <ext-link ext-link-type='doi' href='https://doi.org/10.4137/BMI.S35904'>10.4137/BMI.S35904</ext-link>

[21] J. Hou, Q. Li, J. Wang, W. Lu, “tRFs and tRNA halves: novel cellular defenders in multiple biological processes”, Curr. Issues Mol. Biol, 44 (2022), 5949–5962 <ext-link ext-link-type='doi' href='https://doi.org/10.3390/cimb44120405'>10.3390/cimb44120405</ext-link>

[22] S. George, M. Rafi, M. Aldarmaki, M. ElSiddig, M. Al Nuaimi, K. M.A. Amiri, “tRNA derived small RNAs small players with big roles”, Front. Genet, 13 (2022), 997780 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fgene.2022.997780'>10.3389/fgene.2022.997780</ext-link>

[23] Z. Li, B. A. Stanton, “Transfer RNA-derived fragments, the underappreciated regulatory small RNAs in microbial pathogenesis”, Front. Microbiol, 12 (2021), 687632 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fmicb.2021.687632'>10.3389/fmicb.2021.687632</ext-link>

[24] B. Ren, X. Wang, J. Duan, J. Ma, “Rhizobial tRNA-derived small RNAs are signal molecules regulating plant nodulation”, Science, 365 (2019), 919–922 <ext-link ext-link-type='doi' href='https://doi.org/10.1126/science.aav8907'>10.1126/science.aav8907</ext-link>

[25] I. Morad, D. Chapman-Shimshoni, M. Amitsur, G. Kaufmann, “Functional expression and properties of the tRNA(Lys)-specific core anticodon nuclease encoded by Escherichia coli prrC”, J. Biol. Chem, 268 (1993), 26842–26849 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/S0021-9258(19)74188-X'>10.1016/S0021-9258(19)74188-X</ext-link>

[26] K. Tomita, T. Ogawa, T. Uozumi, K. Watanabe, H. Masaki, “A cytotoxic ribonuclease which specifically cleaves four isoaccepting arginine tRNAs at their anticodon loops”, Proc. Natl. Acad. Sci. USA, 97 (2000), 8278–8283 <ext-link ext-link-type='doi' href='https://doi.org/10.1073/pnas.140213797'>10.1073/pnas.140213797</ext-link>

[27] K. Y. Cao, Y. Pan, T. M. Yan, P. Tao, Y. Xiao, Z. H. Jiang, “Antitumor activities of tRNA derived fragments and tRNA halves from non-pathogenic Escherichia coli strains on colorectal cancer and their structure-activity relationship”, mSystems, 7 (2022), e00164-22 <ext-link ext-link-type='doi' href='https://doi.org/10.1128/msystems.00164-22'>10.1128/msystems.00164-22</ext-link>

[28] E. G. Wagner, R. W. Simons, “Antisense RNA control in bacteria, phages, and plasmids”, Annu. Rev. Microbiol, 48 (1994), 713–742 <ext-link ext-link-type='doi' href='https://doi.org/10.1146/annurev.mi.48.100194.003433'>10.1146/annurev.mi.48.100194.003433</ext-link>

[29] Y. Zhang, X. S. Liu, Q. R. Liu, L. Wei, “Genome-wide in silico identification and analysis of cis natural antisense transcripts (cis-NATs) in ten species”, Nucleic Acids Res, 34 (2006), 3465–3475 <ext-link ext-link-type='doi' href='https://doi.org/10.1093/nar/gkl473'>10.1093/nar/gkl473</ext-link>

[30] M. N. Tutukina, K. S. Shavkunov, I. S. Masulis, O. N. Ozoline, “Antisense transcription within the hns locus of Escherichia coli”, Mol. Biol, 44 (2010), 439–447 <ext-link ext-link-type='doi' href='https://doi.org/10.1134/S002689331003012X'>10.1134/S002689331003012X</ext-link>

[31] M. N. Tutukina, A. I. Dakhnovets, A. D. Kaznadzey, M. S. Gelfand, O. N. Ozoline, “Sense and antisense RNA products of the uxuR gene can affect motility and chemotaxis acting independent of the UxuR protein”, Front. Mol. Biosci, 10 (2023), 1121376 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fmolb.2023.1121376'>10.3389/fmolb.2023.1121376</ext-link>

[32] S. Schwenk, K. B. Arnvig, “Regulatory RNA in Mycobacterium tuberculosis, back to basics”, Pathog. Dis, 76 (2018), fty035 <ext-link ext-link-type='doi' href='https://doi.org/10.1093/femspd/fty035'>10.1093/femspd/fty035</ext-link>

[33] I. Coban, J. P. Lamping, A. G. Hirsch, S. Wasilewski, O. Shomroni, O. Giesbrecht, G. Salinas, H. Krebber, “dsRNA formation leads to preferential nuclear export and gene expression”, Nature, 631 (2024), 432–438 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/s41586-024-07576-w'>10.1038/s41586-024-07576-w</ext-link>

[34] J. Hor, G. Matera, J. Vogel, S. Gottesman, G. Storz, “Trans-acting small RNAs and their effects on gene expression in Escherichia coli and Salmonella enterica”, EcoSal Plus, 9 (2020), 0030–2019 <ext-link ext-link-type='doi' href='https://doi.org/10.1128/ecosalplus.ESP-0030-2019'>10.1128/ecosalplus.ESP-0030-2019</ext-link>

[35] P. Boudry, E. Piattelli, E. Drouineau, J. Peltier, A. Boutserin, M. Lejars, E. Hajnsdorf, M. Monot, B. Dupuy, I. Martin-Verstraete et al, “Identification of RNAs bound by Hfq reveals widespread RNA partners and a sporulation regulator in the human pathogen Clostridioides difficile”, RNA Biol, 18 (2021), 1931–1952 <ext-link ext-link-type='doi' href='https://doi.org/10.1080/15476286.2021.1882180'>10.1080/15476286.2021.1882180</ext-link>

[36] P. Mandin, S. Gottesman, “Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA”, EMBO J., 29 (2010), 3094–3107 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/emboj.2010.179'>10.1038/emboj.2010.179</ext-link>

[37] A. Ghosal, B. B. Upadhyaya, J. V. Fritz, A. Heintz-Buschart, M. S. Desai, D. Yusuf, D. Huang, A. Baumuratov, K. Wang, D. Galas, P. Wilmes, “The extracellular RNA complement of Escherichia coli”, Microbiologyopen, 4 (2015), 252–266 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/mbo3.235'>10.1002/mbo3.235</ext-link>

[38] K. Koeppen, T. H. Hampton, M. Jarek, M. Scharfe, S. A. Gerber, D. W. Mielcarz, E. G. Demers, E. L. Dolben, J. H. Hammond, D. A. Hogan, B. A. Stanton, “A novel mechanism of host pathogen interaction through sRNA in bacterial outer membrane vesicles”, PLoS Pathog, 12 (2016), e1005672 <ext-link ext-link-type='doi' href='https://doi.org/10.1371/journal.ppat.1005672'>10.1371/journal.ppat.1005672</ext-link>

[39] C. Blenkiron, D. Simonov, A. Muthukaruppan, P. Tsai, P. Dauros, S. Green, J. Hong, C. G. Print, S. Swift, A. R. Phillips, “Uropathogenic Escherichia coli releases extracellular vesicles that are associated with RNA”, PLoS One, 11 (2016), e0160440 <ext-link ext-link-type='doi' href='https://doi.org/10.1371/journal.pone.0160440'>10.1371/journal.pone.0160440</ext-link>

[40] O. V. Alikina, O. A. Glazunova, A. A. Bykov, S. S. Kiselev, M. N. Tutukina, K. S. Shavkunov, O. N. Ozoline, “A cohabiting bacterium alters the spectrum of short RNAs secreted by Escherichia coli”, FEMS Microbiol. Lett, 365 (2018), fny262 <ext-link ext-link-type='doi' href='https://doi.org/10.1093/femsle/fny262'>10.1093/femsle/fny262</ext-link>

[41] T. Pita, J. R. Feliciano, J. H. Leitao, “Extracellular RNAs in bacterial infections: from emerging key players on host-pathogen interactions to exploitable biomarkers and therapeutic targets”, Int. J. Mol. Sci, 21 (2020), 9634 <ext-link ext-link-type='doi' href='https://doi.org/10.3390/ijms21249634'>10.3390/ijms21249634</ext-link>

[42] A. Obregon-Henao, M. A. Duque-Correa, M. Rojas, L. F. Garcia, P. J. Brennan, B. L. Ortiz, J. T. Belisle, “Stable extracellular RNA fragments of Mycobacterium tuberculosis induce early apoptosis in human monocytes via a caspase-8 dependent mechanism”, PLoS One, 7 (2012), e29970 <ext-link ext-link-type='doi' href='https://doi.org/10.1371/journal.pone.0029970'>10.1371/journal.pone.0029970</ext-link>

[43] N. Markelova, O. Glazunova, O. Alikina, V. Panyukov, K. Shavkunov, O. Ozoline, “Suppression of Escherichia coli growth dynamics via RNAs secreted by competing bacteria”, Front. Mol. Biosci, 8 (2021), 609979 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fmolb.2021.609979'>10.3389/fmolb.2021.609979</ext-link>

[44] H. J. Lee, S. H. Hong, “Analysis of microRNA-size, small RNAs in Streptococcus mutans by deep sequencing”, FEMS Microbiol. Lett, 326 (2012), 131–136 <ext-link ext-link-type='doi' href='https://doi.org/10.1111/j.1574 6968.2011.02441.x'>10.1111/j.1574 6968.2011.02441.x</ext-link>

[45] I. Diallo, J. Ho, D. Lalaouna, E. Masse, P. Provost, “RNA sequencing unveils very small RNAs with potential regulatory functions in bacteria”, Front. Mol. Biosci, 9 (2022), 914991 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fmolb.2022.914991'>10.3389/fmolb.2022.914991</ext-link>

[46] A. Bykov, O. Glazunova, O. Alikina, N. Sukharicheva, I. Masulis, K. Shavkunov, O. Ozoline, “Excessive promoters as silencers of genes horizontally acquired by Escherichia coli”, Front. Mol. Biosci, 7 (2020), 28 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fmolb.2020.00028'>10.3389/fmolb.2020.00028</ext-link>

[47] E. Afgan, D. Baker, B. Batut, M. van den Beek, D. Bouvier, M. Cech, J. Chilton, D. Clements, N. Coraor, B. A. Gruning et al, “The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update”, Nucleic Acids Res., 46:W1 (2018), W537-W544 <ext-link ext-link-type='doi' href='https://doi.org/10.1093/nar/gky379'>10.1093/nar/gky379</ext-link>

[48] V. V. Panyukov, S. S. Kiselev, K. S. Shavkunov, I. S. Masulis, O. N. Ozoline, “Mixed promoter islands as genomic regions with specific structural and functional properties”, Math. Biol.. Bioinf, 8 (2013), 432–448 (In Russ.) <ext-link ext-link-type='doi' href='https://doi.org/10.17537/2013.8.432'>10.17537/2013.8.432</ext-link>

[49] V. V. Panyukov, O. N. Ozoline, “Promoters of Escherichia coli versus promoter islands: function and structure comparison”, PLoS One, 8 (2013), e62601 <ext-link ext-link-type='doi' href='https://doi.org/10.1371/journal.pone.0062601'>10.1371/journal.pone.0062601</ext-link>

[50] R. C. Edgar, “MUSCLE: multiple sequence alignment with high accuracy and high throughput”, Nucleic Acids Res, 32 (2004), 1792–1797 <ext-link ext-link-type='doi' href='https://doi.org/10.1093/nar/gkh340'>10.1093/nar/gkh340</ext-link>

[51] J. S. Reuter, D. H. Mathews, “RNAstructure: software for RNA secondary structure prediction and analysis”, BMC Bioinformatics, 11 (2010), 129 <ext-link ext-link-type='doi' href='https://doi.org/10.1186/1471-2105-11-129'>10.1186/1471-2105-11-129</ext-link>

[52] S. G. Wolf, D. Frenkiel, T. Arad, S. E. Finkel, R. Kolter, A. Minsky, “DNA protection by stress-induced biocrystallization”, Nature, 400 (1999), 83–85 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/21918'>10.1038/21918</ext-link>

[53] A. A. Bykov, K. S. Shavkunov, V. V. Panyukov, O. N. Ozoline, “Bacterial nucleoid protein Dps binds structured RNA molecules”, Math. Biol. Bioinf., 12, Suppl. (2017), t1–t11 <ext-link ext-link-type='doi' href='https://doi.org/10.17537/2017.12.t1'>10.17537/2017.12.t1</ext-link>

[54] Ghatak, P., K. Karmakar, S. Kasetty, D. Chatterji, “Unveiling the role of Dps in the organization of mycobacterial nucleoid”, PLoS One, 6 (2011), e16019 <ext-link ext-link-type='doi' href='https://doi.org/10.1371/journal.pone.0016019'>10.1371/journal.pone.0016019</ext-link>

[55] R. Janissen, M. M.A. Arens, N. N. Vtyurina, Z. Rivai, N. D. Sunday, B. Eslami-Mossallam, A. A. Gritsenko, L. Laan, D. de Ridder, I. Artsimovitch, N. H. Dekker, E. A. Abbondanzieri, A. S. Meyer, “Global DNA compaction in stationary-phase bacteria does not affect transcription”, Cell, 174 (2018), 1188–1199 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.cell.2018.06.049'>10.1016/j.cell.2018.06.049</ext-link>

[56] C. Park, Y. Jin, Y. J. Kim, H. Jeong, B. L. Seong, “RNA-binding as chaperones of DNA binding proteins from starved cells”, Biochem. Biophys. Res. Commun, 524 (2020), 484–489 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.bbrc.2020.01.121'>10.1016/j.bbrc.2020.01.121</ext-link>

[57] A. Lacqua, O. Wanner, T. Colangelo, M. G. Martinotti, P. Landini, “Emergence of biofilm forming subpopulations upon exposure of Escherichia coli to environmental bacteriophages”, Appl. Environ. Microbiol, 72 (2006), 956–959 <ext-link ext-link-type='doi' href='https://doi.org/10.1128/AEM.72.1.956-959.2006'>10.1128/AEM.72.1.956-959.2006</ext-link>

[58] J. R. Theoret, K. K. Cooper, B. Zekarias, K. L. Roland, B. F. Law, R. Curtiss 3rd, L.A. Joens, “The Campylobacter jejuni Dps homologue is important for in vitro biofilm formation and cecal colonization of poultry and may serve as a protective antigen for vaccination”, Clin. Vaccine Immunol, 19 (2012), 1426–1431 <ext-link ext-link-type='doi' href='https://doi.org/10.1128/CVI.00151-12'>10.1128/CVI.00151-12</ext-link>

[59] B. Pang, W. Hong, N. D. Kock, W. E. Swords, “Dps promotes survival of nontypeable Haemophilus influenzae in biofilm communities in vitro and resistance to clearance in vivo”, Front. Cell Infect. Microbiol, 2 (2012), 58 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fcimb.2012.00058'>10.3389/fcimb.2012.00058</ext-link>

[60] S. Leroy, I. Lebert, C. Andant, P. Micheau, R. Talon, “Investigating extracellular DNA release in Staphylococcus xylosus biofilm in vitro”, Microorganisms, 9 (2021) <ext-link ext-link-type='doi' href='https://doi.org/10.3390/microorganisms9112192'>10.3390/microorganisms9112192</ext-link>

[61] M. Kawano, A. A. Reynolds, J. Miranda-Rios, G. Storz, “Detection of 5'- and 3'-UTR derived small RNAs and cis-encoded antisense RNAs in Escherichia coli”, Nucleic Acids Res, 33 (2005), 1040–1050 <ext-link ext-link-type='doi' href='https://doi.org/10.1093/nar/gki256'>10.1093/nar/gki256</ext-link>

[62] K. M. Wassarman, G. Storz, “6S RNA regulates E coli RNA polymerase activity”, Cell, 101 (2000), 613–623 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/s0092-8674(00)80873-9'>10.1016/s0092-8674(00)80873-9</ext-link>

[63] K. Perumal, R. Reddy, “The 3' end formation in small RNAs”, Gene Expr, 10 (2002), 59–78

[64] A. Depaix, E. Grudzien-Nogalska, B. Fedorczyk, M. Kiledjian, J. Jemielity, J. Kowalska, “Preparation of RNAs with non-canonical 5' ends using novel di- and trinucleotide reagents for co-transcriptional capping”, Front. Mol. Biosci, 9 (2022), 854170 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fmolb.2022.854170'>10.3389/fmolb.2022.854170</ext-link>

[65] R. K. Vishwakarma, K. Brodolin, “The subunit-remodeling factors: an emerging paradigms of transcription regulation”, Front. Microbiol, 11 (2020), 1798 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fmicb.2020.01798'>10.3389/fmicb.2020.01798</ext-link>

[66] L. Pallesen, O. Madsen, P. Klemm, “Regulation of the phase switch controlling expression of type 1 fimbriae in Escherichia coli”, Mol. Microbiol, 3 (1989), 925–931 <ext-link ext-link-type='doi' href='https://doi.org/10.1111/j.1365-2958.1989.tb00242.x'>10.1111/j.1365-2958.1989.tb00242.x</ext-link>

[67] J. Greenblatt, T. F. Mah, P. Legault, J. Mogridge, J. Li, L. E. Kay, “Structure and mechanism in transcriptional antitermination by the bacteriophage $\lambda$ N protein”, Cold Spring Harb. Symp. Quant. Biol, 63 (1998), 327–336 <ext-link ext-link-type='doi' href='https://doi.org/10.1101/sqb.1998.63.327'>10.1101/sqb.1998.63.327</ext-link>

[68] Q. Huang, X. Cheng, M. K. Cheung, S. S. Kiselev, O. N. Ozoline, H. S. Kwan, “High-density transcriptional initiation signals underline genomic islands in bacteria”, PLoS One, 7 (2012), e33759 <ext-link ext-link-type='doi' href='https://doi.org/10.1371/journal.pone.0033759'>10.1371/journal.pone.0033759</ext-link>

[69] S. R. Goldman, J. S. Sharp, I. O. Vvedenskaya, J. Livny, S. L. Dove, B. E. Nickels, “NanoRNAs prime transcription initiation in vivo”, Mol. Cell, 42 (2011), 817–825 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.molcel.2011.06.005'>10.1016/j.molcel.2011.06.005</ext-link>