Browse > Article
http://dx.doi.org/10.4014/jmb.1309.09046

Biofilm Formation and Antibiotic Resistance in Salmonella Typhimurium Are Affected by Different Ribonucleases  

Saramago, Margarida (Instituto de Tecnologia Quimica e Biologica, Universidade Nova de Lisboa)
Domingues, Susana (Instituto de Tecnologia Quimica e Biologica, Universidade Nova de Lisboa)
Viegas, Sandra Cristina (Instituto de Tecnologia Quimica e Biologica, Universidade Nova de Lisboa)
Arraiano, Cecilia Maria (Instituto de Tecnologia Quimica e Biologica, Universidade Nova de Lisboa)
Publication Information
Journal of Microbiology and Biotechnology / v.24, no.1, 2014 , pp. 8-12 More about this Journal
Abstract
Biofilm formation and antibiotic resistance are important determinants for bacterial pathogenicity. Ribonucleases control RNA degradation and there is increasing evidence that they have an important role in virulence mechanisms. In this report, we show that ribonucleases affect susceptibility against ribosome-targeting antibiotics and biofilm formation in Salmonella.
Keywords
Salmonella; biofilms; antibiotics; RNases; RNA;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Viegas SC, Mil-Homens D, Fialho AM, Arraiano CM. 2013. The virulence of Salmonella Typhimurium in the insect model Galleria mellonella is impaired by mutations in endoribonucleases E and III. Appl. Environ. Microbiol. 79: 6124-6133.   DOI
2 Viegas SC, Pfeiffer V, Sittka A, Silva IJ, Vogel J, Arraiano CM. 2007. Characterization of the role of ribonucleases in Salmonella small RNA decay. Nucleic Acids Res. 35: 7651- 7664.   DOI
3 Viegas SC, Silva IJ, Saramago M, Domingues S, Arraiano CM. 2011. Regulation of the small regulatory RNA MicA by ribonuclease III: a target-dependent pathway. Nucleic Acids Res. 39: 2918-2930.   DOI
4 Vioque A, de la Cruz J. 2003. Trans-translation and protein synthesis inhibitors. FEMS Microbiol. Lett. 218: 9-14.   DOI
5 Wang RF, Kushner SR. 1991. Construction of versatile lowcopy- number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100: 195-199.   DOI
6 Wei Q, Tarighi S, Dotsch A, Haussler S, Musken M, Wright VJ, et al. 2011. Phenotypic and genome-wide analysis of an antibiotic-resistant small colony variant (SCV) of Pseudomonas aeruginosa. PLoS One 6: e29276.   DOI
7 Zakikhany K, Harrington CR, Nimtz M, Hinton JC, Romling U. 2010. Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 77: 771-786.   DOI   ScienceOn
8 Romling U. 2005. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol. Life Sci. 62: 1234-1246.   DOI   ScienceOn
9 Romling U, Bian Z, Hammar M, Sierralta WD, Normark S. 1998. Curli fibers are highly conserved between Salmonella Typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 180: 722-731.
10 Rouf SF, Ahmad I, Anwar N, Vodnala SK, Kader A, Romling U, Rhen M. 2011. Opposing contributions of polynucleotide phosphorylase and the membrane protein NlpI to biofilm formation by Salmonella enterica serovar Typhimurium. J. Bacteriol. 193: 580-582.   DOI
11 Siibak T, Peil L, Xiong L, Mankin A, Remme J, Tenson T. 2009. Erythromycin- and chloramphenicol-induced ribosomal assembly defects are secondary effects of protein synthesis inhibition. Antimicrob. Agents Chemother. 53: 563-571.   DOI
12 Silva IJ, Saramago M, Dressaire C, Domingues S, Viegas SC, Arraiano CM. 2011. Importance and key events of prokaryotic RNA decay: the ultimate fate of an RNA molecule. Wiley Interdiscip. Rev. RNA 2: 818-836.   DOI
13 Sim SH, Yeom JH, Shin C, Song WS, Shin E, Kim HM, et al. 2010. Escherichia coli ribonuclease III activity is downregulated by osmotic stress: consequences for the degradation of bdm mRNA in biofilm formation. Mol. Microbiol. 75: 413-425.   DOI   ScienceOn
14 Solano C, Garcia B, Valle J, Berasain C, Ghigo JM, Gamazo C, Lasa I. 2002. Genetic analysis of Salmonella Enteritidis biofilm formation: critical role of cellulose. Mol. Microbiol. 43: 793-808.   DOI   ScienceOn
15 Stewart PS. 2002. Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol. 292: 107-113.   DOI   ScienceOn
16 Usary J, Champney WS. 2001. Erythromycin inhibition of 50S ribosomal subunit formation in Escherichia coli cells. Mol. Microbiol. 40: 951-962.   DOI
17 Viegas SC, Arraiano CM. 2008. Regulating the regulators: how ribonucleases dictate the rules in the control of small non-coding RNAs. RNA Biol. 5: 230-243.   DOI
18 Luidalepp H, Hallier M, Felden B, Tenson T. 2005. tmRNA decreases the bactericidal activity of aminoglycosides and the susceptibility to inhibitors of cell wall synthesis. RNA Biol. 2: 70-74.   DOI
19 Jorgensen MG, Nielsen JS, Boysen A, Franch T, Moller- Jensen J, Valentin-Hansen P. 2012. Small regulatory RNAs control the multi-cellular adhesive lifestyle of Escherichia coli. Mol. Microbiol. 84: 36-50.   DOI
20 Kint G, De Coster D, Marchal K, Vanderleyden J, De Keersmaecker SC. 2010. The small regulatory RNA molecule MicA is involved in Salmonella enterica s erovar T yph imurium biofilm formation. BMC Microbiol. 10: 276.   DOI
21 Magnet S, Blanchard JS. 2005. Molecular insights into aminoglycoside action and resistance. Chem. Rev. 105: 477-498.   DOI   ScienceOn
22 Mah TF, O'Toole GA. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9: 34-39.   DOI   ScienceOn
23 Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, et al. 2010. T h e global b urden of n ontyph oidal Salmonella gastroenteritis. Clin. Infect. Dis. 50: 882-889.   DOI
24 Merritt JH, Kadouri DE, O'Toole GA. 2005. Growing and analyzing static biofilms. Curr. Protoc. Microbiol. Chapter 1: Unit 1B 1.
25 Misra TK, Apirion D. 1979. RNase E, an RNA processing enzyme from Escherichia coli. J. Biol. Chem. 254: 11154-11159.
26 Noah JW, Dolan MA, Babin P, Wollenzien P. 1999. Effects of tetracycline and spectinomycin on the tertiary structure of ribosomal RNA in the Escherichia coli 30S ribosomal subunit. J. Biol. Chem. 274: 16576-16581.   DOI
27 Richards J, Mehta P, Karzai AW. 2006. RNase R degrades non-stop mRNAs selectively in an SmpB-tmRNA-dependent manner. Mol. Microbiol. 62: 1700-1712.   DOI
28 Cheng ZF, Deutscher MP. 2003. Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proc. Natl. Acad. Sci. USA 100: 6388-6393.   DOI
29 Domingues S, Matos RG, Reis FP, Fialho AM, Barbas A, Arraiano CM. 2009. Biochemical characterization of the RNase II family of exoribonucleases from the human pathogens Salmonella T yph miurium a nd Streptococcus pneumoniae. Biochemistry 48: 11848-11857.   DOI
30 de la Cruz J, Vioque A. 2001. Increased sensitivity to protein synthesis inhibitors in cells lacking tmRNA. RNA 7: 1708-1716.
31 Eidem TM, Roux CM, Dunman PM. 2012. RNA decay: a novel therapeutic target in bacteria. Wiley Interdiscip. Rev. RNA 3: 443-454.
32 Frazier AD, Champney WS. 2012. Impairment of ribosomal subunit synthesis in aminoglycoside-treated ribonuclease mutants of Escherichia coli. Arch. Microbiol. 194: 1033-1041.   DOI
33 Ghora BK, Apirion D. 1978. Structural analysis and in vitro processing to p5 rRNA of a 9S RNA molecule isolated from an rne mutant of E. coli. Cell 15: 1055-1066.   DOI   ScienceOn
34 Gualdi L, Tagliabue L, Bertagnoli S, Ierano T, De Castro C, Landini P. 2008. Cellulose modulates biofilm formation by counteracting curli-mediated colonization of solid surfaces in Escherichia coli. Microbiology 154: 2017-2024.   DOI
35 Hamilton S, Bongaerts RJ, Mulholland F, Cochrane B, Porter J, Lucchini S, et al. 2009. The transcriptional programme of Salmonella enterica serovar Typhimurium reveals a key role for tryptophan metabolism in biofilms. BMC Genomics 10: 599.   DOI
36 Heeb S, F letch er M P, C h habra S R, D iggle SP, W illiams P , Camara M. 2011. Quinolones: from antibiotics to autoinducers. FEMS Microbiol. Rev. 35: 247-274.   DOI
37 Hoiseth SK, Stocker BA. 1981. Aromatic-dependent Salmonella Typhimurium are non-virulent and effective as live vaccines. Nature 291: 238-239.   DOI   ScienceOn
38 Allas U, Liiv A, Remme J. 2003. Functional interaction between RNase III and the Escherichia coli ribosome. BMC Mol. Biol. 4: 8.   DOI
39 Andrews JM. 2001. Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 48(Suppl 1): 5-16.   DOI   ScienceOn
40 Arraiano CM, Andrade JM, Domingues S, Guinote IB, Malecki M, Matos RG, et al. 2010. The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol. Rev. 34: 883-923.   DOI
41 Arraiano CM, Mauxion F, Viegas SC, Matos RG, Seraphin B. 2013. Intracellular ribonucleases involved in transcript processing and decay: precision tools for RNA. Biochim. Biophys. Acta 1829: 491-513.   DOI
42 Bilgin N, Richter AA, Ehrenberg M, Dahlberg AE, Kurland CG. 1990. Ribosomal RNA and protein mutants resistant to spectinomycin. EMBO J. 9: 735-739.
43 Carzaniga T, Antoniani D, Deho G, Briani F, Landini P. 2012. The RNA processing enzyme polynucleotide phosphorylase negatively controls biofilm formation by repressing poly-Nacetylglucosamine (pNAG) production in Escherichia coli C. BMC Microbiol. 12: 270.   DOI
44 Lawal A, Jejelowo O, Chopra AK, Rosenzweig JA. 2011. Ribonucleases and bacterial virulence. Microb. Biotechnol. 4: 558-571.   DOI