Inflammation Fuels Colicin Ib-Dependent Competition of Serovar Typhimurium and in Blooms

English version České info

The host's immune system plays a key role in modulating growth of pathogens and the intestinal microbiota in the gut. In particular, inflammatory bowel disorders and pathogen infections induce shifts of the resident commensal microbiota which can result in overgrowth of Enterobacteriaceae (“inflammation-inflicted blooms”). Here, we investigated competition of the human pathogenic Salmonella enterica serovar Typhimurium strain SL1344 (S. Tm) and commensal E. coli in inflammation-inflicted blooms. S. Tm produces colicin Ib (ColIb), which is a narrow-spectrum protein toxin active against related Enterobacteriaceae. Production of ColIb conferred a competitive advantage to S. Tm over sensitive E. coli strains in the inflamed gut. In contrast, an avirulent S. Tm mutant strain defective in triggering gut inflammation did not benefit from ColIb. Expression of ColIb (cib) is regulated by iron limitation and the SOS response. CirA, the cognate outer membrane receptor of ColIb on colicin-sensitive E. coli, is induced upon iron limitation. We demonstrate that growth in inflammation-induced blooms favours expression of both S. Tm ColIb and the receptor CirA, thereby fuelling ColIb dependent competition of S. Tm and commensal E. coli in the gut. In conclusion, this study uncovers a so-far unappreciated role of inflammation-inflicted blooms as an environment favouring ColIb-dependent competition of pathogenic and commensal representatives of the Enterobacteriaceae family.

Vyšlo v časopise: Inflammation Fuels Colicin Ib-Dependent Competition of Serovar Typhimurium and in Blooms. PLoS Pathog 10(1): e32767. doi:10.1371/journal.ppat.1003844
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003844

Souhrn

Zdroje

1. MushinR, DubosR (1965) Colonization of the mouse intestine with Escherichia coli. J Exp Med 122 : 745–757.

2. BarthelM, HapfelmeierS, Quintanilla-MartinezL, KremerM, RohdeM, et al. (2003) Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 71 : 2839–2858.

3. StecherB, HardtWD (2010) Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol 14(1): 82–91.

4. SansonettiPJ (2008) Host-bacteria homeostasis in the healthy and inflamed gut. Curr Opin Gastroenterol 24 : 435–439.

5. LuppC, RobertsonML, WickhamME, SekirovI, ChampionOL, et al. (2007) Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of enterobacteriaceae. Cell, host and microbe 2 : 119–129.

6. StecherB, RobbianiR, WalkerAW, WestendorfAM, BarthelM, et al. (2007) Salmonella enterica Serovar Typhimurium Exploits Inflammation to Compete with the Intestinal Microbiota. PLoS Biol 5: e244.

7. StecherB, DenzlerR, MaierL, BernetF, SandersMJ, et al. (2012) Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc Natl Acad Sci U S A 109 : 1269–1274.

8. StecherB, MaierL, HardtWD (2013) ‘Blooming’ in the gut: how dysbiosis might contribute to pathogen evolution. Nat Rev Microbiol 11 : 277–284.

9. RaffatelluM, GeorgeMD, AkiyamaY, HornsbyMJ, NuccioSP, et al. (2009) Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5 : 476–486.

10. LoetscherY, WieserA, LengefeldJ, KaiserP, SchubertS, et al. (2012) Salmonella transiently reside in luminal neutrophils in the inflamed gut. PLoS ONE 7: e34812.

11. WinterSE, ThiennimitrP, WinterMG, ButlerBP, HusebyDL, et al. (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467 : 426–429.

12. WinterSE, WinterMG, XavierMN, ThiennimitrP, PoonV, et al. (2013) Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339 : 708–711.

13. LopezCA, WinterSE, Rivera-ChavezF, XavierMN, PoonV, et al. (2012) Phage-mediated acquisition of a type III secreted effector protein boosts growth of salmonella by nitrate respiration. MBio 3.

14. Rivera-ChavezF, WinterSE, LopezCA, XavierMN, WinterMG, et al. (2013) Salmonella uses energy taxis to benefit from intestinal inflammation. PLoS Pathog 9: e1003267.

15. CascalesE, BuchananSK, DucheD, KleanthousC, LloubesR, et al. (2007) Colicin biology. Microbiol Mol Biol Rev 71 : 158–229.

16. ScheinSJ, KaganBL, FinkelsteinA (1978) Colicin K acts by forming voltage-dependent channels in phospholipid bilayer membranes. Nature 276 : 159–163.

17. KoniskyJ (1972) Characterization of colicin Ia and colicin Ib. Chemical studies of protein structure. J Biol Chem 247 : 3750–3755.

18. CardelliJ, KoniskyJ (1974) Isolation and characterization of an Escherichia coli mutant tolerant to colicins Ia and Ib. J Bacteriol 119 : 379–385.

19. LazdunskiCJ, BouveretE, RigalA, JournetL, LloubesR, et al. (1998) Colicin import into Escherichia coli cells. J Bacteriol 180 : 4993–5002.

20. BuchananSK, LukacikP, GrizotS, GhirlandoR, AliMM, et al. (2007) Structure of colicin I receptor bound to the R-domain of colicin Ia: implications for protein import. EMBO J 26 : 2594–2604.

21. JakesKS, FinkelsteinA (2010) The colicin Ia receptor, Cir, is also the translocator for colicin Ia. Mol Microbiol 75 : 567–578.

22. WeaverCA, KaganBL, FinkelsteinA, KoniskyJ (1981) Mode of action of colicin ib: formation of ion-permeable membrane channels. Biochim Biophys Acta 645 : 137–142.

23. MankovichJA, LaiPH, GokulN, KoniskyJ (1984) Organization of the colicin Ib gene. Promoter structure and immunity domain. J Biol Chem 259 : 8764–8768.

24. DaviesJK, ReevesP (1975) Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group B. J Bacteriol 123 : 96–101.

25. MankovichJA, HsuCH, KoniskyJ (1986) DNA and amino acid sequence analysis of structural and immunity genes of colicins Ia and Ib. J Bacteriol 168 : 228–236.

26. EscolarL, Perez-MartinJ, de LorenzoV (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181 : 6223–6229.

27. ButalaM, Zgur-BertokD, BusbySJ (2009) The bacterial LexA transcriptional repressor. Cell Mol Life Sci 66 : 82–93.

28. KelleyWL (2006) Lex marks the spot: the virulent side of SOS and a closer look at the LexA regulon. Mol Microbiol 62 : 1228–1238.

29. RileyMA, WertzJE (2002) Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56 : 117–137.

30. GillorO, GiladiI, RileyMA (2009) Persistence of colicinogenic Escherichia coli in the mouse gastrointestinal tract. BMC Microbiol 9 : 165.

31. KirkupBC, RileyMA (2004) Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature 428 : 412–414.

32. IkariNS, KentonDM, YoungVM (1969) Interaction in the germfree mouse intestine of colicinogenic and colicin-sensitive microorganisms. Proc Soc Exp Biol Med 130 : 1280–1284.

33. KelstrupJ, GibbonsRJ (1969) Inactivation of bacteriocins in the intestinal canal and oral cavity. J Bacteriol 99 : 888–890.

34. CravenJA, MiniatsOP, BarnumDA (1971) Role of colicins in antagonism between strains of Escherichia coli in dual-infected gnotobiotic pigs. Am J Vet Res 32 : 1775–1779.

35. BraunV, FrenzJ, HantkeK, SchallerK (1980) Penetration of colicin M into cells of Escherichia coli. J Bacteriol 142 : 162–168.

36. de GraafFK (1973) Effects of cloacin DF13 on the functioning of the cytoplasmic membrane. Antonie Van Leeuwenhoek 39 : 109–119.

37. HapfelmeierS, StecherB, BarthelM, KremerM, MüllerA, et al. (2005) The Salmonella Pathogenicity Island (SPI)-1 and SPI-2 Type III Secretion Systems Allow Salmonella Serovar Typhimurium to trigger Colitis via MyD88-Dependent and MyD88-Independent Mechanisms. J Immunol 174 : 1675–1685.

38. TaylorCM, OsmanD, CavetJS (2009) Differential expression from two iron-responsive promoters in Salmonella enterica serovar Typhimurium reveals the presence of iron in macrophage-phagosomes. Microb Pathog 46 : 114–118.

39. GriggsDW, TharpBB, KoniskyJ (1987) Cloning and promoter identification of the iron-regulated cir gene of Escherichia coli. J Bacteriol 169 : 5343–5352.

40. WinterSE, LopezCA, BaumlerAJ (2013) The dynamics of gut-associated microbial communities during inflammation. EMBO Rep 14 : 319–327.

41. ThiennimitrP, WinterSE, WinterMG, XavierMN, TolstikovV, et al. (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci U S A 108 : 17480–17485.

42. Apperloo-RenkemaHZ, Van der WaaijBD, Van der WaaijD (1990) Determination of colonization resistance of the digestive tract by biotyping of Enterobacteriaceae. Epidemiol Infect 105 : 355–361.

43. WardPP, Uribe-LunaS, ConneelyOM (2002) Lactoferrin and host defense. Biochem Cell Biol 80 : 95–102.

44. BachmanMA, MillerVL, WeiserJN (2009) Mucosal lipocalin 2 has pro-inflammatory and iron-sequestering effects in response to bacterial enterobactin. PLoS Pathog 5: e1000622.

45. BaumlerAJ, NorrisTL, LascoT, VoightW, ReissbrodtR, et al. (1998) IroN, a novel outer membrane siderophore receptor characteristic of Salmonella enterica. J Bacteriol 180 : 1446–1453.

46. FischbachMA, LinH, ZhouL, YuY, AbergelRJ, et al. (2006) The pathogen-associated iroA gene cluster mediates bacterial evasion of lipocalin 2. Proc Natl Acad Sci U S A 103 : 16502–16507.

47. MillerC, ThomsenLE, GaggeroC, MosseriR, IngmerH, et al. (2004) SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305 : 1629–1631.

48. GoerlichO, QuillardetP, HofnungM (1989) Induction of the SOS response by hydrogen peroxide in various Escherichia coli mutants with altered protection against oxidative DNA damage. J Bacteriol 171 : 6141–6147.

49. SegalAW (2005) How neutrophils kill microbes. Annu Rev Immunol 23 : 197–223.

50. SchumannS, AlpertC, EngstW, LohG, BlautM (2012) Dextran sodium sulfate-induced inflammation alters the expression of proteins by intestinal Escherichia coli strains in a gnotobiotic mouse model. Appl Environ Microbiol 78 : 1513–1522.

51. HantkeK (1990) Dihydroxybenzoylserine–a siderophore for E. coli. FEMS Microbiol Lett 55 : 5–8.

52. NikaidoH, RosenbergEY (1990) Cir and Fiu proteins in the outer membrane of Escherichia coli catalyze transport of monomeric catechols: study with beta-lactam antibiotics containing catechol and analogous groups. J Bacteriol 172 : 1361–1367.

53. OhkawaI, ShigaS, KageyamaM (1980) Effect of iron concentration in the growth medium on the sensitivity of Pseudomonas aeruginosa to pyocin S2. J Biochem 87 : 323–331.

54. RileyMA, GordonDM (1999) The ecological role of bacteriocins in bacterial competition. Trends Microbiol 7 : 129–133.

55. HardyKG (1975) Colicinogeny and related phenomena. Bacteriol Rev 39 : 464–515.

56. WadolkowskiEA, LauxDC, CohenPS (1988) Colonization of the streptomycin-treated mouse large intestine by a human fecal Escherichia coli strain: role of growth in mucus. Infect Immun 56 : 1030–1035.

57. RileyMA, GordonDM (1992) A survey of Col plasmids in natural isolates of Escherichia coli and an investigation into the stability of Col-plasmid lineages. J Gen Microbiol 138 : 1345–1352.

58. ChaoL, LevinBR (1981) Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc Natl Acad Sci U S A 78 : 6324–6328.

59. HibbingME, FuquaC, ParsekMR, PetersonSB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8 : 15–25.

60. MrakP, PodlesekZ, van PuttenJP, Zgur-BertokD (2007) Heterogeneity in expression of the Escherichia coli colicin K activity gene cka is controlled by the SOS system and stochastic factors. Mol Genet Genomics 277 : 391–401.

61. KamensekS, PodlesekZ, GillorO, Zgur-BertokD (2010) Genes regulated by the Escherichia coli SOS repressor LexA exhibit heterogeneous expression. BMC Microbiol 10 : 283.

62. TenaillonO, SkurnikD, PicardB, DenamurE (2010) The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8 : 207–217.

63. ChangDE, SmalleyDJ, TuckerDL, LeathamMP, NorrisWE, et al. (2004) Carbon nutrition of Escherichia coli in the mouse intestine. Proc Natl Acad Sci U S A 101 : 7427–7432.

64. Conway TC, P.S. (2007) Escherichia coli at the Intestinal Mucosal Surface. American Society for Microbiology Press, Washington, D C 4th Edition Virulence Mechanisms of Bacterial Pathogens: 175–196,.

65. DewhirstFE, ChienCC, PasterBJ, EricsonRL, OrcuttRP, et al. (1999) Phylogeny of the defined murine microbiota: altered Schaedler flora. Appl Environ Microbiol 65 : 3287–3292.

66. StecherB, ChaffronS, KappeliR, HapfelmeierS, FreedrichS, et al. (2010) Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog 6: e1000711.

67. HapfelmeierS, EhrbarK, StecherB, BarthelM, KremerM, et al. (2004) Role of the Salmonella Pathogenicity Island 1 Effector Proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica Subspecies 1 Serovar Typhimurium Colitis in Streptomycin-Pretreated Mice. Infect Immun 72 : 795–809.

68. 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.

69. StecherB, HapfelmeierS, MullerC, KremerM, StallmachT, et al. (2004) Flagella and Chemotaxis Are Required for Efficient Induction of Salmonella enterica Serovar Typhimurium Colitis in Streptomycin-Pretreated Mice. Infect Immun 72 : 4138–4150.

70. GunnJS, Alpuche-ArandaCM, LoomisWP, BeldenWJ, MillerSI (1995) Characterization of the Salmonella typhimurium pagC/pagD chromosomal region. J Bacteriol 177 : 5040–5047.

71. WangRF, KushnerSR (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100 : 195–199.

72. GibsonDG, YoungL, ChuangRY, VenterJC, HutchisonCA3rd, et al. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6 : 343–345.

73. SalgadoH, Peralta-GilM, Gama-CastroS, Santos-ZavaletaA, Muniz-RascadoL, et al. (2013) RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more. Nucleic Acids Res 41: D203–213.

74. BaileyTL, GribskovM (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14 : 48–54.

75. GerlachRG, HolzerSU, JackelD, HenselM (2007) Rapid engineering of bacterial reporter gene fusions by using Red recombination. Appl Environ Microbiol 73 : 4234–4242.

76. LaemmliUK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 : 680–685.

77. HoisethSK, StockerBA (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291 : 238–239.

78. MollerAK, LeathamMP, ConwayT, NuijtenPJ, de HaanLA, et al. (2003) An Escherichia coli MG1655 lipopolysaccharide deep-rough core mutant grows and survives in mouse cecal mucus but fails to colonize the mouse large intestine. Infect Immun 71 : 2142–2152.