A Small, MicroRNA-size, Ribonucleic Acid Regulating Gene Expression and Development of Shiga Toxin-converting Bacteriophage Φ24Β

Overview

Journal Sci Rep

Specialty Science

Date 2015 May 12

PMID 25962117

Citations 21

Authors

Bozena Nejman-Falenczyk

Sylwia Bloch

Katarzyna Licznerska

Aleksandra Dydecka

Agnieszka Felczykowska

Gracja Topka

Alicja Wegrzyn

Grzegorz Wegrzyn

Affiliations

Soon will be listed here.

Abstract

A microRNA-size (20-nt long) molecule has been identified in Escherichia coli after induction of Shiga toxin-converting bacteriophage Φ24B. This small RNA, named 24B_1, is encoded in the lom-vb_24B_43 region of the phage genome, and apparently it is produced by cleavage of a larger transcript. A phage devoid of 24B_1 revealed decreased efficiency of lysogenization, quicker prophage induction after provoking the SOS response, higher efficiency of progeny phage production during the lytic cycle and less efficient adsorption on the host cells. Expression of most of phage genes was drastically increased after infection of E. coli by the Φ24BΔ24B_1 phage. Since 24B_1 may impair expression of the d_ant gene, coding for an anti-repressor, these results may explain the mechanism of regulations of the physiological processes by this small RNA due to impaired activity of the cI repressor and changed expression of vast majority of phage genes. To our knowledge, this is the first example of functional microRNA-size molecule in bacterial cells.

Citing Articles

A review on gut microbiota and miRNA crosstalk: implications for Alzheimer's disease.

Ayyanar M, Vijayan M Geroscience. 2024; 47(1):339-385.

PMID: 39562408 PMC: 11872870. DOI: 10.1007/s11357-024-01432-5.

Analysis of Phage Regulatory RNAs: Sequencing Library Construction from the Fraction of Small Prokaryotic RNAs Less Than 50 Nucleotides in Length.

Bloch S, Lewandowska N, Wesolowski W, Lukasiak A, Mach P, Nejman-Falenczyk B Methods Mol Biol. 2024; 2741:25-34.

PMID: 38217647 DOI: 10.1007/978-1-0716-3565-0_3.

Bacteriophage-encoded 24B_1 molecule resembles herpesviral microRNAs and plays a crucial role in the development of both the virus and its host.

Bloch S, Lewandowska N, Zwolenkiewicz J, Mach P, Lukasiak A, Olejniczak M PLoS One. 2023; 18(12):e0296038.

PMID: 38117844 PMC: 10732415. DOI: 10.1371/journal.pone.0296038.

The Burden of Survivors: How Can Phage Infection Impact Non-Infected Bacteria?.

Letarov A, Letarova M Int J Mol Sci. 2023; 24(3).

PMID: 36769055 PMC: 9917116. DOI: 10.3390/ijms24032733.

The Interplay Between Gut Microbiota and miRNAs in Cardiovascular Diseases.

Ionescu R, Enache R, Cretoiu S, Cretoiu D Front Cardiovasc Med. 2022; 9:856901.

PMID: 35369298 PMC: 8965857. DOI: 10.3389/fcvm.2022.856901.

References

Bloch S, Nejman-Falenczyk B, Dydecka A, Los J, Felczykowska A, Wegrzyn A . Different expression patterns of genes from the exo-xis region of bacteriophage λ and Shiga toxin-converting bacteriophage Ф24B following infection or prophage induction in Escherichia coli. PLoS One. 2014; 9(10):e108233. PMC: 4195576. DOI: 10.1371/journal.pone.0108233. View

Borges A, Tsai S, Caldas D . Validation of reference genes for RT-qPCR normalization in common bean during biotic and abiotic stresses. Plant Cell Rep. 2011; 31(5):827-38. DOI: 10.1007/s00299-011-1204-x. View

Jensen K . The Escherichia coli K-12 "wild types" W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels. J Bacteriol. 1993; 175(11):3401-7. PMC: 204738. DOI: 10.1128/jb.175.11.3401-3407.1993. View

Gottesman S, McCullen C, Guillier M, Vanderpool C, Majdalani N, Benhammou J . Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol. 2007; 71:1-11. PMC: 3592358. DOI: 10.1101/sqb.2006.71.016. View

Gottesman S, Storz G . Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol. 2010; 3(12). PMC: 3225950. DOI: 10.1101/cshperspect.a003798. View

Vanderpool C, Balasubramanian D, Lloyd C . Dual-function RNA regulators in bacteria. Biochimie. 2011; 93(11):1943-9. PMC: 3185123. DOI: 10.1016/j.biochi.2011.07.016. View

Los J, Golec P, Wegrzyn G, Wegrzyn A, Los M . Simple method for plating Escherichia coli bacteriophages forming very small plaques or no plaques under standard conditions. Appl Environ Microbiol. 2008; 74(16):5113-20. PMC: 2519272. DOI: 10.1128/AEM.00306-08. View

Bloch S, Nejman-Falenczyk B, Los J, Baranska S, Lepek K, Felczykowska A . Genes from the exo-xis region of λ and Shiga toxin-converting bacteriophages influence lysogenization and prophage induction. Arch Microbiol. 2013; 195(10-11):693-703. PMC: 3824215. DOI: 10.1007/s00203-013-0920-8. View

Ramakers C, Ruijter J, Lekanne Deprez R, Moorman A . Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett. 2003; 339(1):62-6. DOI: 10.1016/s0304-3940(02)01423-4. View

10.

Richards G, Vanderpool C . Molecular call and response: the physiology of bacterial small RNAs. Biochim Biophys Acta. 2011; 1809(10):525-31. PMC: 3186873. DOI: 10.1016/j.bbagrm.2011.07.013. View

11.

Macke T, Ecker D, Gutell R, Gautheret D, Case D, Sampath R . RNAMotif, an RNA secondary structure definition and search algorithm. Nucleic Acids Res. 2001; 29(22):4724-35. PMC: 92549. DOI: 10.1093/nar/29.22.4724. View

12.

Aglawe S, Fakrudin B, Patole C, Bhairappanavar S, Koti R, Krishnaraj P . Quantitative RT-PCR analysis of 20 transcription factor genes of MADS, ARF, HAP2, MBF and HB families in moisture stressed shoot and root tissues of sorghum. Physiol Mol Biol Plants. 2013; 18(4):287-300. PMC: 3550552. DOI: 10.1007/s12298-012-0135-5. View

13.

Gautheret D, Lambert A . Direct RNA motif definition and identification from multiple sequence alignments using secondary structure profiles. J Mol Biol. 2001; 313(5):1003-11. DOI: 10.1006/jmbi.2001.5102. View

14.

Fogg P, Gossage S, Smith D, Saunders J, McCarthy A, Allison H . Identification of multiple integration sites for Stx-phage Phi24B in the Escherichia coli genome, description of a novel integrase and evidence for a functional anti-repressor. Microbiology (Reading). 2007; 153(Pt 12):4098-4110. DOI: 10.1099/mic.0.2007/011205-0. View

15.

Kang S, Choi J, Lee Y, Hong S, Lee H . Identification of microRNA-size, small RNAs in Escherichia coli. Curr Microbiol. 2013; 67(5):609-13. DOI: 10.1007/s00284-013-0411-9. View

16.

Riley L, Veses-Garcia M, Hillman J, Handfield M, McCarthy A, Allison H . Identification of genes expressed in cultures of E. coli lysogens carrying the Shiga toxin-encoding prophage Φ24B. BMC Microbiol. 2012; 12:42. PMC: 3342100. DOI: 10.1186/1471-2180-12-42. View

17.

Hayes S, SZYBALSKI W . Control of short leftward transcripts from the immunity and ori regions in induced coliphage lambda. Mol Gen Genet. 1973; 126(4):275-90. DOI: 10.1007/BF00269438. View

18.

Guerin M, Robichon N, Geiselmann J, Rahmouni A . A simple polypyrimidine repeat acts as an artificial Rho-dependent terminator in vivo and in vitro. Nucleic Acids Res. 1998; 26(21):4895-900. PMC: 147931. DOI: 10.1093/nar/26.21.4895. View

19.

Nowicki D, Bloch S, Nejman-Falenczyk B, Szalewska-Palasz A, Wegrzyn A, Wegrzyn G . Defects in RNA polyadenylation impair both lysogenization by and lytic development of Shiga toxin-converting bacteriophages. J Gen Virol. 2015; 96(Pt 7):1957-68. DOI: 10.1099/vir.0.000102. View

20.

Allison H, Sergeant M, James C, Saunders J, Smith D, Sharp R . Immunity profiles of wild-type and recombinant shiga-like toxin-encoding bacteriophages and characterization of novel double lysogens. Infect Immun. 2003; 71(6):3409-18. PMC: 155745. DOI: 10.1128/IAI.71.6.3409-3418.2003. View