Intraspecies Competition for Niches in the Distal Gut Dictate Transmission during Persistent Infection

English version České info

Salmonella enterica serovars infect various mammalian hosts, causing disease ranging from self-limiting diarrhea to persistent systemic infections such as typhoid fever. Here we investigated the impact of an established intestinal S. Typhimurium population on fecal shedding in the presence of another challenging strain. This scenario arises during host-to-host transmission, as well as during chronic host-adapted infections when systemic Salmonella reseed the intestinal tract to be transmitted in feces. In a mouse model of persistent Salmonella infection, we found that distinct subpopulations formed in intestinal and systemic tissues. Expansion of the intestinal subpopulation was responsible for increases in fecal shedding, rather than increased secretion of systemic Salmonella. Furthermore, the Salmonella that initially colonized the gut excluded challengers from the cecum, colon, and feces. A challenging systemic strain could only be shed upon ablation of the established intestinal strain. This intraspecies colonization resistance requires Salmonella hydrogenase-mediated invasion of the distal gut and is maintained by the virulence effectors SPI1 and SPI2. We describe novel observations indicating that Salmonella virulence effectors that have been shown to subvert the host immune response and microbiota, also play a role in intraspecies competition for colonization of transmission niches.

Vyšlo v časopise: Intraspecies Competition for Niches in the Distal Gut Dictate Transmission during Persistent Infection. PLoS Pathog 10(12): e32767. doi:10.1371/journal.ppat.1004527
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004527

Souhrn

Zdroje

1. ParryCM, HienTT, DouganG, WhiteNJ, FarrarJJ (2002) Typhoid Fever. N Engl J Med 347: 1770–1782.

2. LevinMM, BlackRE, LanataC (1982) Precise Estimation of the Numbers of Chronic Carriers of Salmonella typhi in Santiago, Chile, an Endemic Area. J INFECT DIS 146: 724–726.

3. FeaseyNA, DouganG, KingsleyRA, HeydermanRS, GordonMA (2012) Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. The Lancet 379: 2489–2499.

4. GopinathS, CardenS, MonackD (2012) Shedding light on Salmonella carriers. Trends in Microbiology 20: 320–327.

5. KingsleyRA, MsefulaCL, ThomsonNR, KariukiS, HoltKE, et al. (2009) Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Research 19: 2279.

6. MacLennanCA, GilchristJJ, GordonMA, CunninghamAF, CobboldM, et al. (2010) Dysregulated Humoral Immunity to Nontyphoidal Salmonella in HIV-Infected African Adults. Science 328: 508–512.

7. BuchwaldDS, BlaserMJ (1984) A review of human salmonellosis: II. Duration of excretion following infection with nontyphi Salmonella. Rev Infect Dis 3: 345–56..

8. Sirinavin S, Garner P (1996) Antibiotics for treating salmonella gut infections. Sirinavin S, editor Chichester, UK: John Wiley & Sons, Ltd.

9. MonackDM, MuellerA, FalkowS (2004) Persistent bacterial infections: the interface of the pathogen and the host immune system. Nature Reviews Microbiology 2: 747–765.

10. Gonzalez-EscobedoG, MarshallJM, GunnJS (2010) Chronic and acute infection of the gall bladder by Salmonella Typhi: understanding the carrier state. Nature Reviews Microbiology 9: 9–14.

11. CostelloEK, StagamanK, DethlefsenLes, BohannanBJM, RelmanDA (2012) The Application of Ecological Theory Toward an Understanding of the Human Microbiome. Science 336: 1255–1261.

12. LevinBR (1999) Population Biology, Evolution, and Infectious Disease: Convergence and Synthesis. Science 283: 806–809.

13. Hanski I, Gaggiotti OE (2004) Metapopulation biology: past, present, and future. In: Hanski I and Gaggiotti OE, editors. Ecology, Genetics and Evolution of Metapopulations. Burlington: Elsevier Academic Press. pp 3–22.

14. Gaggiotti OE, Hanski I (2004) Mechanisms of population extinction. In: Hanski I and Gaggiotti OE, editors. Ecology, Genetics and Evolution of Metapopulations. Burlington: Elsevier Academic Press. pp 337–366.

15. HanskiI (1998) Metapopulation dynamics. Nature 396: 41–49.

16. Ovaskainen O, Hanski I (2004) Metapopulation dynamics in highly fragmented landscapes. In: Hanski I and Gaggiotti OE, editors. Ecology, Genetics and Evolution of Metapopulations. Burlington: Elsevier Academic Press. pp 73–103.

17. Thomas CD, Hanski I (2004) Metapopulation dynamics in changing environments: butterfly responses to habitat and climate change. In: Hanski I and Gaggiotti OE, editors. Ecology, Genetics and Evolution of Metapopulations. Burlington: Elsevier Academic Press. pp 489–514.

18. Melton-WittJA, RafelskiSM, PortnoyDA, BakardjievAI (2012) Oral Infection with Signature-Tagged Listeria monocytogenes Reveals Organ-Specific Growth and Dissemination Routes in Guinea Pigs. Infection and Immunity 80: 720–732.

19. BarnesPD, BergmanMA, MecsasJ, IsbergRR (2006) Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine. Journal of Experimental Medicine 203: 1591–1601.

20. WaltersMS, LaneMC, VigilPD, SmithSN, WalkST, et al. (2011) Kinetics of Uropathogenic Escherichia coli Metapopulation Movement during Urinary Tract Infection. mBio 3: e00303–11–e00303–11.

21. OellerichMF, JacobiCA, FreundS, NiedungK, BachA, et al. (2007) Yersinia enterocolitica Infection of Mice Reveals Clonal Invasion and Abscess Formation. Infection and Immunity 75: 3802–3811.

22. KaiserP, SlackE, GrantAJ, HardtW-D, RegoesRR (2013) PLOS Pathogens: Lymph Node Colonization Dynamics after Oral Salmonella Typhimurium Infection in Mice. plospathogensorg 9: e1003532.

23. GrantAJ, RestifO, McKinleyTJ, SheppardM, MaskellD, et al. (2008) PLOS Biology: Modelling within-Host Spatiotemporal Dynamics of Invasive Bacterial Disease. PLoS Biology 6: e74.

24. LimCH, VoedischS, WahlB, RoufSF, GeffersR, et al. (2014) Independent Bottlenecks Characterize Colonization of Systemic Compartments and Gut Lymphoid Tissue by Salmonella. PLoS Pathog 10: e1004270.

25. SutherlandJP (1974) Multiple stable points in natural communities. The American Naturalist 108: 859–873.

26. ConnellJH, SlatyerRO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. The American Naturalist 111.

27. ShulmanMJ, OgdenJC, EbersoleJP, McFarlandWN, MillerSL, et al. (1983) Priority Effects in the Recruitment of Juvenile Coral Reef Fishes. Ecology 64: 1508.

28. KardolP, SouzaL, ClassenAT (2012) Resource availability mediates the importance of priority effects in plant community assembly and ecosystem function. Oikos 122: 84–94.

29. JiangL, TanJ, PuZ (2010) An Experimental Test of Darwin's Naturalization Hypothesis. Am Nat 175: 415–423.

30. MaierL, VyasR, CordovaCD, LindsayH, SchmidtTSB, et al. (2013) Microbiota-Derived Hydrogen Fuels Salmonella Typhimurium Invasion of the Gut Ecosystem. Cell Host & Microbe 14: 641–651.

31. MonackDM (2004) Salmonella typhimurium Persists within Macrophages in the Mesenteric Lymph Nodes of Chronically Infected Nramp1+/+ Mice and Can Be Reactivated by IFN Neutralization. Journal of Experimental Medicine 199: 231–241.

32. LawleyTD, ChanK, ThompsonLJ, KimCC, GovoniGR, et al. (2006) Genome-Wide Screen for Salmonella Genes Required for Long-Term Systemic Infection of the Mouse. PLoS Pathog 2: e11.

33. LawleyTD, BouleyDM, HoyYE, GerkeC, RelmanDA, et al. (2007) Host Transmission of Salmonella enterica Serovar Typhimurium Is Controlled by Virulence Factors and Indigenous Intestinal Microbiota. Infection and Immunity 76: 403–416.

34. PedronT, MuletC, DaugaC, FrangeulL, ChervauxC, et al. (2012) A Crypt-Specific Core Microbiota Resides in the Mouse Colon. mBio 3: e00116–12–e00116–12.

35. ShadeA, JonesSE, CaporasoJG, HandelsmanJ, KnightR, et al. (2014) Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity. mBio 4: e01371–14 doi:–10.1128/mBio.01371–14

36. BrayJR, CurtisJT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27: 325–349.

37. GopinathS, HotsonA, JohnsJ, NolanG, MonackD (2013) The Systemic Immune State of Super-shedder Mice Is Characterized by a Unique Neutrophil-dependent Blunting of TH1 Responses. PLoS Pathog 9: e1003408.

38. CrawfordRW, Rosales-ReyesR, Ramirez-AguilarMDLL, Chapa-AzuelaO, Alpuche-ArandaC, et al. (2010) Gallstones play a significant role in Salmonella spp. gallbladder colonization and carriage. Proceedings of the National Academy of Sciences 107: 4353–4358.

39. EndtK, StecherB, ChaffronS, SlackE, TchitchekN, et al. (2010) The Microbiota Mediates Pathogen Clearance from the Gut Lumen after Non-Typhoidal Salmonella Diarrhea. PLoS Pathog 6: e1001097.

40. BohnhoffM, MillerCP (1962) Enhanced Susceptibility to Salmonella Infection in Streptomycin-Treated Mice. J INFECT DIS 111: 117–127.

41. 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. Infection and Immunity 71: 2839–2858.

42. GalanJE (2001) Salmonella interactions with host cells: Type III Secretion at Work. Annual Review of Cell and Developmental Biology 17: 53–86.

43. CoburnB, LiY, OwenD, VallanceBA, FinlayBB (2005) Salmonella enterica Serovar Typhimurium Pathogenicity Island 2 Is Necessary for Complete Virulence in a Mouse Model of Infectious Enterocolitis. Infection and Immunity 73: 3219–3227.

44. McGhieEJ, BrawnLC, HumePJ, HumphreysD, KoronakisV (2009) Salmonella takes control: effector-driven manipulation of the host. Current Opinion in Microbiology 12: 117–124.

45. KaiserP, RegoesRR, DolowschiakT, WotzkaSY, LengefeldJ, et al. (2014) Cecum Lymph Node Dendritic Cells Harbor Slow-Growing Bacteria Phenotypically Tolerant to Antibiotic Treatment. PLoS Biol 12: e1001793.

46. DiardM, SellinME, DolowschiakT, ArnoldiniM, AckermannM, et al. (2014) Antibiotic Treatment Selects for Cooperative Virulence of Salmonella Typhimurium. Current Biology 24: 2000–2005.

47. OnderdonkA, MarshallB, CisnerosR, LevyB (1981) Competition between congenic Escherichia coli K-12 strains in vivo. Infection and Immunity 1: 74.

48. LeeSM, DonaldsonGP, MikulskiZ, BoyajianS, LeyK, et al. (2013) Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501: 426–429.

49. LeathamMP, BanerjeeS, AutieriSM, Mercado-LuboR, ConwayT, et al. (2009) Precolonized Human Commensal Escherichia coli Strains Serve as a Barrier to E. coli O157:H7 Growth in the Streptomycin-Treated Mouse Intestine. Infect Immun 7: 2876–2886.

50. GrantAJ, CowardC, JonesMA, WoodallCA, BarrowPA, et al. (2005) Signature-Tagged Transposon Mutagenesis Studies Demonstrate the Dynamic Nature of Cecal Colonization of 2-Week-Old Chickens by Campylobacter jejuni. Appl Environ Microbiol 71: 8031–8041.

51. EverestP, WainJ, RobertsM, RookG, DouganG (2001) The molecular mechanisms of severe typhoid fever. Trends in Microbiology 9: 316–320.

52. VaishnaviC, SinghS, KochharR, BhasinD, SinghG, et al. (2005) Prevalence of Salmonella enterica serovar Typhi in bile and stool of patients with biliary disease and those requiring biliary drainage for other purposes. Japanese Journal of Infectious Disease 58: 363–365.

53. VogelsangTM, BoeJ (1948) Temporary and chronic carriers of Salmonella typhi and Salmonella paratyphi B. The Journal of Hygiene 46: 252–261.

54. RistoriC, RodriguezH, VicentP, FerreccioC, GarciaJ, et al. (1982) Persistence of the Salmonella Typhi-Paratyphi carrier state after gallbladder removal. Bull Pan Am Health Organ 16: 361–366.

55. DongolS, ThompsonCN, ClareS, NgaTVT, DuyPT, et al. (2012) The Microbiological and Clinical Characteristics of Invasive Salmonella in Gallbladders from Cholecystectomy Patients in Kathmandu, Nepal. PLoS ONE 7: e47342.

56. GoodpastureEW (1936) Concerning the pathogenesis of typhoid fever. American Journal of Pathology 13: 175–185.

57. EiseleNE, RubyT, JacobsonA, ManzanilloPS, CoxJS, et al. (2013) Salmonella Require the Fatty Acid Regulator PPARδ for the Establishment of a Metabolic Environment Essential for Long-Term Persistence. Cell Host & Microbe 14: 171–182.

58. BäumlerAJ, TsolisRM, BoweFA, KustersJG, HoffmannS, et al. (1995) The pef fimbrial operon of Salmonella typhimurium mediates adhesion to murine small intestine and is necessary for fluid accumulation in the infant mouse. Infection and Immunity 64: 61–68.

59. DorseyCW, LaarakkerMC, HumphriesAD, WeeningEH, BäumlerAJ (2005) Salmonella enterica serotype Typhimurium MisL is an intestinal colonization factor that binds fibronectin. Molecular Microbiology 57: 196–211.

60. MisselwitzB, BarrettN, KreibichS, VonaeschP, AndritschkeD, et al. (2012) Near Surface Swimming of Salmonella Typhimurium Explains Target-Site Selection and Cooperative Invasion. PLoS Pathog 8: e1002810.

61. GriffinAJ, McSorleySJ (2011) Development of protective immunity to Salmonella, a mucosal pathogen with a systemic agenda. Mucosal Immunology 4: 371–382.

62. WijburgOLC (2006) Innate secretory antibodies protect against natural Salmonella typhimurium infection. Journal of Experimental Medicine 203: 21–26.

63. BrozP, OhlsonMB, MonackDM (2012) Innate immune response to Salmonella typhimurium, a model enteric pathogen. Gut Microbes 3: 62–70.

64. PeayKG, BelisleM, FukamiT (2011) Phylogenetic relatedness predicts priority effects in nectar yeast communities. Proceedings of the Royal Society Biological Sciences 279: 749–758.

65. TanJ, PuZ, RybergWA, JiangL (2012) Species phylogenetic relatedness, priority effects, and ecosystem functioning. Ecology 93: 1164–1172.

66. FukamiT, BeaumontHJE, ZhangX-X (2007) Immigration history controls diversification in experimental adaptive radiation. Nature Letters 446: 436–439.

67. HernandezSB, CotaI, DucretA, AusselL (2012) Adaptation and Preadaptation of Salmonella enterica to Bile. PLoS Genet 8: e1002459.

68. DiardM, GarciaV, MaierL, Remus-EmsermannMNP, RegoesRR, et al. (2013) Stabilization of cooperative virulence by the expression of an avirulent phenotype. Nature 494: 353–356.

69. MastroeniP, MorganFJE, McKinleyTJ, ShawcroftE, ClareS, et al. (2011) Enhanced Virulence of Salmonella enterica Serovar Typhimurium after Passage through Mice. Infection and Immunity 79: 636–643.

70. MeesterLD, GomezA, OkamuraB, SchwenkK (2002) The Monopolization Hypothesis and the dispersal–gene flow paradox in aquatic organisms. Acta Oecologica 23: 121–135.

71. BrownNF, VallanceBA, CoombesBK, ValdezY, CoburnBA, et al. (2005) Salmonella Pathogenicity Island 2 Is Expressed Prior to Penetrating the Intestine. PLoS Pathog 1: e32.

72. BarmanM, UnoldD, ShifleyK, AmirE, HungK, et al. (2008) Enteric Salmonellosis Disrupts the Microbial Ecology of the Murine Gastrointestinal Tract. Infection and Immunity 76: 907–915.

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

74. ThiennimitrP, WinterSE, WinterMG, XavierMN, TolstikovV, et al. (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proceedings of the National Academy of Sciences 108: 17480–17485.

75. BeckerD, SelbachM, RollenhagenC, BallmaierM, MeyerTF, et al. (2006) Robust Salmonella metabolism limits possibilities for new antimicrobials. Nature 440: 303–307.

76. KaiserBLD, LiJ, SanfordJA, KimY-M, KronewitterSR, et al. (2013) A Multi-Omic View of Host-Pathogen-Commensal Interplay in Salmonella-Mediated Intestinal Infection. PLoS ONE 8: e67155.

77. SmithBP, Reina-GuerraM, JoisethSK, StockerBA, HabashaF, et al. (1984) Aromatic-dependent Salmonella typhimurium as modified live vaccines for calves. Am J Vet Res 1: 59–66.

78. HenryT, García-del PortilloF, GorvelJP (2005) Identification of Salmonella functions critical for bacterial cell division within eukaryotic cells. Molecular Microbiology 56: 252–267.

79. DatsenkoKA, WannerBL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proceedings of the National Academy of Sciences 97: 6640–6645.

80. BrozP, NewtonK, LamkanfiM, MariathasanS, DixitVM, et al. (2010) Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J Exp Med 207: 1745–1755.