Selection of Orphan Rhs Toxin Expression in Evolved Serovar Typhimurium

English version České info

Salmonella Typhimurium is a bacterium that causes intestinal diseases in a number of animals including humans. In mice, this pathogen invades tissues, causing symptoms similar to typhoid fever. In an effort to understand the evolution of this pathogen, we grew S. Typhimurium in either liquid broth or in mice for many generations and examined the resulting “evolved” strains to determine if they were different from the original “parent” culture. We found that many of these evolved strains inhibited the growth of the parent after they were mixed together, and that this growth inhibition requires that the evolved and parental cells are in close contact. Genetic analysis showed that this contact-dependent growth inhibition requires Rhs protein, which has a toxic tip. Salmonella is normally resistant to its Rhs toxin because it also produces an immunity protein that blocks toxin activity. However, evolved cells have undergone a DNA rearrangement that allows them to express a different Rhs toxic tip that inhibits growth of the parental cells, which lack immunity to it. This allows the evolved cells to outgrow the original parental cells. Our work indicates that populations of Salmonella are dynamic, with individuals battling with each other for dominance.

Vyšlo v časopise: Selection of Orphan Rhs Toxin Expression in Evolved Serovar Typhimurium. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004255
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004255

Souhrn

Zdroje

1. LopezD, VlamakisH, KolterR (2010) Biofilms. Cold Spring Harb Perspect Biol 2: a000398.

2. KoskiniemiS, LamoureuxJG, NikolakakisKC, t'Kint de RoodenbekeC, KaplanMD, et al. (2013) Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci U S A 110 : 7032–7037.

3. HillCW (1999) Large genomic sequence repetitions in bacteria: lessons from rRNA operons and Rhs elements. Res Microbiol 150 : 665–674.

4. LinRJ, CapageM, HillCW (1984) A repetitive DNA sequence, rhs, responsible for duplications within the Escherichia coli K-12 chromosome. J Mol Biol 177 : 1–18.

5. FosterSJ (1993) Molecular analysis of three major wall-associated proteins of Bacillus subtilis 168: evidence for processing of the product of a gene encoding a 258 kDa precursor two-domain ligand-binding protein. Mol Microbiol 8 : 299–310.

6. PooleSJ, DinerEJ, AokiSK, BraatenBA, t'Kint de RoodenbekeC, et al. (2011) Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet 7: e1002217.

7. KoskiniemiS, SunS, BergOG, AnderssonDI (2012) Selection-driven gene loss in bacteria. PLoS Genet 8: e1002787.

8. NilssonAI, KugelbergE, BergOG, AnderssonDI (2004) Experimental adaptation of Salmonella typhimurium to mice. Genetics 168 : 1119–1130.

9. AokiSK, PammaR, HerndayAD, BickhamJE, BraatenBA, et al. (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309 : 1245–1248.

10. LovettST, HurleyRL, SuteraVAJr, AubuchonRH, LebedevaMA (2002) Crossing over between regions of limited homology in Escherichia coli. RecA-dependent and RecA-independent pathways. Genetics 160 : 851–859.

11. SilvermanJM, BrunetYR, CascalesE, MougousJD (2012) Structure and regulation of the type VI secretion system. Annu Rev Microbiol 66 : 453–472.

12. ShneiderMM, ButhSA, HoBT, BaslerM, MekalanosJJ, et al. (2013) PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500 : 350–353.

13. BusbyJN, PanjikarS, LandsbergMJ, HurstMR, LottJS (2013) The BC component of ABC toxins is an RHS-repeat-containing protein encapsulation device. Nature 501 : 547–550.

14. ReamsAB, KofoidE, SavageauM, RothJR (2010) Duplication frequency in a population of Salmonella enterica rapidly approaches steady state with or without recombination. Genetics 184 : 1077–1094.

15. AndersonP, RothJ (1981) Spontaneous tandem genetic duplications in Salmonella typhimurium arise by unequal recombination between rRNA (rrn) cistrons. Proc Natl Acad Sci U S A 78 : 3113–3117.

16. BergthorssonU, AnderssonDI, RothJR (2007) Ohno's dilemma: evolution of new genes under continuous selection. Proc Natl Acad Sci U S A 104 : 17004–17009.

17. PetterssonME, SunS, AnderssonDI, BergOG (2009) Evolution of new gene functions: simulation and analysis of the amplification model. Genetica 135 : 309–324.

18. NasvallJ, SunL, RothJR, AnderssonDI (2012) Real-time evolution of new genes by innovation, amplification, and divergence. Science 338 : 384–387.

19. FolkessonA, LofdahlS, NormarkS (2002) The Salmonella enterica subspecies I specific centisome 7 genomic island encodes novel protein families present in bacteria living in close contact with eukaryotic cells. Res Microbiol 153 : 537–545.

20. BlondelCJ, JimenezJC, ContrerasI, SantiviagoCA (2009) Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 10 : 354.

21. MulderDT, CooperCA, CoombesBK (2012) Type VI secretion system-associated gene clusters contribute to pathogenesis of Salmonella enterica serovar Typhimurium. Infect Immun 80 : 1996–2007.

22. ChaudhuriRR, MorganE, PetersSE, PleasanceSJ, HudsonDL, et al. (2013) Comprehensive assignment of roles for Salmonella typhimurium genes in intestinal colonization of food-producing animals. PLoS Genet 9: e1003456.

23. SheppardM, WebbC, HeathF, MallowsV, EmilianusR, et al. (2003) Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell Microbiol 5 : 593–600.

24. BarnesPD, BergmanMA, MecsasJ, IsbergRR (2006) Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine. J Exp Med 203 : 1591–1601.

25. OellerichMF, JacobiCA, FreundS, NiedungK, BachA, et al. (2007) Yersinia enterocolitica infection of mice reveals clonal invasion and abscess formation. Infect Immun 75 : 3802–3811.

26. KungVL, KhareS, StehlikC, BaconEM, HughesAJ, et al. (2012) An rhs gene of Pseudomonas aeruginosa encodes a virulence protein that activates the inflammasome. Proc Natl Acad Sci U S A 109 : 1275–1280.

27. ScottJR (1968) Genetic studies on bacteriophage P1. Virology 36 : 564–574.

28. DatsenkoKA, WannerBL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97 : 6640–6645.

29. AiyarA, XiangY, LeisJ (1996) Site-directed mutagenesis using overlap extension PCR. Methods Mol Biol 57 : 177–191.

30. HayesCS, SauerRT (2003) Cleavage of the A site mRNA codon during ribosome pausing provides a mechanism for translational quality control. Mol Cell 12 : 903–911.

31. RuheZC, HayesCS (2010) The N-terminus of GalE induces tmRNA activity in Escherichia coli. PLoS One 5: e15207.

32. DinerEJ, BeckCM, WebbJS, LowDA, HayesCS (2012) Identification of a target cell permissive factor required for contact-dependent growth inhibition (CDI). Genes Dev 26 : 515–525.

33. Garza-SanchezF, GinJG, HayesCS (2008) Amino acid starvation and colicin D treatment induce A-site mRNA cleavage in Escherichia coli. J Mol Biol 378 : 505–519.