Next generation sequencing analysis reveals that the ribonucleases RNase II, RNase R and PNPase affect bacterial motility and biofilm formation in E. coli

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Pobre, Vânia ^a   Arraiano, Cecília M ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Biofilm formation; Exoribonucleases; Motility; PNPase; RNA Seq; RNase II; RNase R; Transcriptome

Indexed keywords

BACTERIAL RNA; EXORIBONUCLEASE; PNPASE; RIBONUCLEASE II; RIBONUCLEASE R; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; EXORIBONUCLEASE II; MESSENGER RNA; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RNR PROTEIN, E COLI;

ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL MOTILITY; BIOFILM; CELL MOTILITY; CONTROLLED STUDY; DOWN REGULATION; ESCHERICHIA COLI; GENE EXPRESSION; NEXT GENERATION SEQUENCING; NONHUMAN; POLYMERASE CHAIN REACTION; RNA SEQUENCE; TRANSCRIPTOMICS; CELL MOTION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; RNA STABILITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BIOFILMS; CELL MOVEMENT; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EXORIBONUCLEASES; GENE EXPRESSION REGULATION, BACTERIAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RNA STABILITY; RNA, MESSENGER;

EID: 84924341701     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1237-6     Document Type: Article

References (51)

1. Andrade JM, Pobre V, Silva IJ, Domingues S, Arraiano CM. The role of 3'-5' exoribonucleases in RNA degradation. Prog Mol Biol Transl Sci. 2009;85:187-229.
2. Arraiano CM, Andrade JM, Domingues S, Guinote IB, Malecki M, Matos RG, et al. The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol Rev. 2010;34(5):883-923.
3. Cannistraro VJ, Kennell D. The reaction mechanism of ribonuclease II and its interaction with nucleic acid secondary structures. Biochem et Biophys Acta. 1999;1433:170-87.
4. Spickler C, Mackie A. Action of RNases II and Polynucleotide Phosphorylase against RNAs containing stem-loops of defined structure. J Bacteriol. 2000;182:2422-7.
5. Coburn GA, Mackie GA. Overexpression, purification, and properties of Escherichia coli ribonuclease II. J Biol Chem. 1996;271(2):1048-53.
6. Folichon M, Marujo PE, Arluison V, Le Derout J, Pellegrini O, Hajnsdorf E, et al. Fate of mRNA extremities generated by intrinsic termination: detailed analysis of reactions catalyzed by ribonuclease II and poly(A) polymerase. Biochimie. 2005;87(9-10):819-26.
7. Hajnsdorf E, Steier O, Coscoy L, Teysset L, Régnier P. Roles of RNase E, RNase II and PNPase in the degradation of the rpsO transcripts of Escherichia coli: stabilizing function of RNase II and evidence for efficient degradation in an ams pnp rnb mutant. EMBO J. 1994;13(14):3368-77.
8. Marujo PE, Hajnsdorf E, Le Derout J, Andrade R, Arraiano CM, Régnier P. RNase II removes the oligo(A) tails that destabilize the rpsO mRNA of Escherichia coli. RNA. 2000;6(8):1185-93.
9. Mohanty BK, Kushner SR. Polynucleotide phosphorylase, RNase II and RNase E play different roles in the in vivo modulation of polyadenylation in Escherichia coli. Mol Microbiol. 2000;36(4):982-94.
10. Pepe CM, Maslesa-Galic S, Simons RW. Decay of the IS10 antisense RNA by 3' exoribonucleases: evidence that RNase II stabilizes RNA-OUT against PNPase attack. Mol Microbiol. 1994;13(6):1133-42.
11. Cheng ZF, Deutscher MP. Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison RNase II J Biol Chem. 2002;277(24):21624-9.
12. Vincent HA, Deutscher MP. Substrate recognition and catalysis by the exoribonuclease RNase R. J Biol Chem. 2006;281(40):29769-75.
13. Andrade JM, Hajnsdorf E, Régnier P, Arraiano CM. The poly(A)-dependent degradation pathway of rpsO mRNA is primarily mediated by RNase R. RNA. 2009;15(2):316-26.
14. Awano N, Rajagopal V, Arbing M, Patel S, Hunt J, Inouye M, et al. Escherichia coli RNase R has dual activities, helicase and RNase. J Bacteriol. 2010;192(5):1344-52.
15. Cheng ZF, Deutscher MP. Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proc Natl Acad Sci U S A. 2003;100(11):6388-93.
16. Cairrão F, Cruz A, Mori H, Arraiano CM. Cold shock induction of RNase R and its role in the maturation of the quality control mediator SsrA/tmRNA. Mol Microbiol. 2003;50(4):1349-60.
17. Andrade JM, Cairrão F, Arraiano CM. RNase R affects gene expression in stationary phase: regulation of ompA. Mol Microbiol. 2006;60(1):219-28.
18. Chen C, Deutscher MP. RNase R is a highly unstable protein regulated by growth phase and stress. RNA. 2010;16(4):667-72.
19. Liang W, Deutscher MP. Ribosomes regulate the stability and action of RNase R. J Biol Chem. 2013;288(48):34791-8.
20. Malecki M, Bárria C, Arraiano CM. Characterization of the RNase R association with ribosomes. BMC Microbiol. 2014;14:34.
21. Mohanty BK, Kushner SR. Polynucleotide phosphorylase functions both as a 3' right-arrow 5' exonuclease and a poly(A) polymerase in Escherichia coli. Proc Natl Acad Sci U S A. 2000;97(22):11966-71.
22. Slomovic S, Portnoy V, Yehudai-Resheff S, Bronshtein E, Schuster G. Polynucleotide phosphorylase and the archaeal exosome as poly(A)-polymerases. Biochim Biophys Acta. 2008;1779(4):247-55.
23. Mohanty BK, Kushner SR. The majority of Escherichia coli mRNAs undergo post-transcriptional modification in exponentially growing cells. Nucleic Acids Res. 2006;34(19):5695-704.
24. Clements MO, Eriksson S, Thompson A, Lucchini S, Hinton JC, Normark S, et al. Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica. Proc Natl Acad Sci U S A. 2002;99(13):8784-9.
25. Erova TE, Kosykh VG, Fadl AA, Sha J, Horneman AJ, Chopra AK. Cold shock exoribonuclease R (VacB) is involved in Aeromonas hydrophila pathogenesis. J Bacteriol. 2008;190(10):3467-74.
26. Haddad N, Tresse O, Rivoal K, Chevret D, Nonglaton Q, Burns CM, Prévost H, Cappelier JM: Polynucleotide phosphorylase has an impact on cell biology of Campylobacter jejuni. Front Cell Inf Microbio 2012: doi:10.3389/fcimb.2012.00030
27. Tobe T, Sasakawa C, Okada N, Honma Y, Yoshikawa M. vacB, a novel chromosomal gene required for expression of virulence genes on the large plasmid of Shigella flexneri. J Bacteriol. 1992;174(20):6359-67.
28. Josenhans C, Suerbaum S. The role of motility as a virulence factor in bacteria. Int J Med Microbiol IJMM. 2002;291(8):605-14.
29. de la Fuente-Nunez C, Reffuveille F, Fernandez L, Hancock RE. Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol. 2013;16(5):580-9.
30. Guttenplan SB, Kearns DB. Regulation of flagellar motility during biofilm formation. FEMS Microbiol Rev. 2013;37(6):849-71.
31. Mohanty BK, Kushner SR. Genomic analysis in Escherichia coli demonstrates differential roles for polynucleotide phosphorylase and RNase II in mRNA abundance and decay. Mol Microbiol. 2003;50(2):645-58.
32. Fonseca P, Moreno R, Rojo F. Genomic analysis of the role of RNase R in the turnover of Pseudomonas putida mRNAs. J Bacteriol. 2008;190(18):6258-63.
33. De Lay N, Gottesman S. Role of polynucleotide phosphorylase in sRNA function in Escherichia coli. RNA. 2011;17(6):1172-89.
34. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511-5.
35. Tabas Madrid D, Nogales-Cadenas R, Pascual-Montano A. GeneCodis3: a non-redundant and modular enrichment analysis tool for functional genomics. Nucleic Acids Res. 2012;40(Web Server issue):W478-83.
36. Ulett GC, Webb RI, Schembri MA. Antigen-43-mediated autoaggregation impairs motility in Escherichia coli. Microbiology. 2006;152(Pt 7):2101-10.
37. Andrade JM, Pobre V, Arraiano CM. Small RNA modules confer different stabilities and interact differently with multiple targets. PLoS One. 2013;8(1):e52866.
38. Andrade JM, Pobre V, Matos AM, Arraiano CM. The crucial role of PNPase in the degradation of small RNAs that are not associated with Hfq. RNA. 2012;18(4):844-55.
39. Danese PN, Pratt LA, Dove SL, Kolter R. The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol Microbiol. 2000;37(2):424-32.
40. Saramago M, Domingues S, Viegas SC, Arraiano CM. Biofilm formation and antibiotic resistance in Salmonella Typhimurium are affected by different ribonucleases. J Microbiol Biotechnol. 2014;24(1):8-12.
41. Schembri MA, Kjaergaard K, Klemm P. Global gene expression in Escherichia coli biofilms. Mol Microbiol. 2003;48(1):253-67.
42. Frazão C, McVey CE, Amblar M, Barbas A, Vonrhein C, Arraiano CM, et al. Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature. 2006;443:110-4.
43. Deutscher MP. Ribonuclease multiplicity, diversity, and complexity. J Biol Chem. 1993;268(18):13011-4.
44. Donovan WP, Kushner SR. Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc Natl Acad Sci USA. 1986;83:120-4.
45. Komeda Y. Transcriptional control of flagellar genes in Escherichia coli K-12. J Bacteriol. 1986;168(3):1315-8.
46. Arnosti DN, Chamberlin MJ. Secondary sigma factor controls transcription of flagellar and chemotaxis genes in Escherichia coli. Proc Natl Acad Sci U S A. 1989;86(3):830-4.
47. De Lay N, Gottesman S. A complex network of small non-coding RNAs regulate motility in Escherichia coli. Mol Microbiol. 2012;86(3):524-38.
48. Maes A, Gracia C, Hajnsdorf E, Régnier P. Search for poly(A) polymerase targets in E. coli reveals its implication in surveillance of Glu tRNA processing and degradation of stable RNAs. Mol Microbiol. 2012;83(2):436-51.
49. Arraiano CM, Yancey SD, Kushner SR. Stabilization of discrete mRNA breakdown products in ams pnp rnb multiple mutants of Escherichia coli K-12. J Bacteriol. 1988;170(10):4625-33.
50. Merritt JH, Kadouri DE, O'Toole GA: Growing and analyzing static biofilms. Current protocols in microbiology 2005, Chapter 1:Unit 1B 1.
51. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30(1):207-10.