Trade-Off between Bile Resistance and Nutritional Competence Drives Diversification in the Mouse Gut
Bacterial diversification is often observed, but underlying mechanisms are difficult to disentangle and remain generally unknown. Moreover, controlled diversification experiments in ecologically relevant environments are lacking. We studied bacterial diversification in the mammalian gut, one of the most complex bacterial environments, where usually hundreds of species and thousands of bacterial strains stably coexist. Herein we show rapid genetic diversification of an Escherichia coli strain upon colonisation of previously germ-free mice. In addition to the previously described mutations in the EnvZ/OmpR operon, we describe the rapid and systematic selection of mutations in the flagellar flhDC operon and in malT, the transcriptional activator of the maltose regulon. Moreover, within each mouse, the three mutant types coexisted at different levels after one month of colonisation. By combining in vivo studies and determination of the fitness advantages of the selected mutations in controlled in vitro experiments, we provide evidence that the selective forces that drive E. coli diversification in the mouse gut are the presence of bile salts and competition for nutrients. Altogether our results indicate that a trade-off between stress resistance and nutritional competence generates sympatric diversification of the gut microbiota. These results illustrate how experimental evolution in natural environments enables identification of both the selective pressures that organisms face in their natural environment and the diversification mechanisms.
Vyšlo v časopise:
Trade-Off between Bile Resistance and Nutritional Competence Drives Diversification in the Mouse Gut. PLoS Genet 7(6): e32767. doi:10.1371/journal.pgen.1002107
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002107
Souhrn
Bacterial diversification is often observed, but underlying mechanisms are difficult to disentangle and remain generally unknown. Moreover, controlled diversification experiments in ecologically relevant environments are lacking. We studied bacterial diversification in the mammalian gut, one of the most complex bacterial environments, where usually hundreds of species and thousands of bacterial strains stably coexist. Herein we show rapid genetic diversification of an Escherichia coli strain upon colonisation of previously germ-free mice. In addition to the previously described mutations in the EnvZ/OmpR operon, we describe the rapid and systematic selection of mutations in the flagellar flhDC operon and in malT, the transcriptional activator of the maltose regulon. Moreover, within each mouse, the three mutant types coexisted at different levels after one month of colonisation. By combining in vivo studies and determination of the fitness advantages of the selected mutations in controlled in vitro experiments, we provide evidence that the selective forces that drive E. coli diversification in the mouse gut are the presence of bile salts and competition for nutrients. Altogether our results indicate that a trade-off between stress resistance and nutritional competence generates sympatric diversification of the gut microbiota. These results illustrate how experimental evolution in natural environments enables identification of both the selective pressures that organisms face in their natural environment and the diversification mechanisms.
Zdroje
1. RaineyPBTravisanoM 1998 Adaptive radiation in a heterogeneous environment. Nature 394 69 72
2. MacLeanRCBellG 2002 Experimental adaptive radiation in Pseudomonas. Am Nat 160 569 581
3. MaharjanRSeetoSNotley-McRobbLFerenciT 2006 Clonal adaptive radiation in a constant environment. Science 313 514 517
4. BucklingACraig MacleanRBrockhurstMAColegraveN 2009 The Beagle in a bottle. Nature 457 824 829
5. LeyREPetersonDAGordonJI 2006 Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124 837 848
6. ZhangHDiBaiseJKZuccoloAKudrnaDBraidottiM 2009 Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A 106 2365 2370
7. QinJLiRRaesJArumugamMBurgdorfKS 2010 A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464 59 65
8. SonnenburgJLAngenentLTGordonJI 2004 Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nat Immunol 5 569 573
9. MahowaldMAReyFESeedorfHTurnbaughPJFultonRS 2009 Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc Natl Acad Sci U S A 106 5859 5864
10. DenouERezzonicoEPanoffJMArigoniFBrussowH 2009 A Mesocosm of Lactobacillus johnsonii, Bifidobacterium longum, and Escherichia coli in the Mouse Gut. DNA Cell Biol
11. ThauerRK 1973 CO 2 reduction to formate in Clostridium acidi-urici. J Bacteriol 114 443 444
12. VaishampayanPAKuehlJVFroulaJLMorganJLOchmanH 2010 Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. 2010 Genome Biol Evol 53 66
13. Martinez-MedinaMAldeguerXLopez-SilesMGonzalez-HuixFLopez-OliuC 2009 Molecular diversity of Escherichia coli in the human gut: new ecological evidence supporting the role of adherent-invasive E. coli (AIEC) in Crohn's disease. Inflamm Bowel Dis 15 872 882
14. NowrouzianFLWoldAEAdlerberthI 2005 Escherichia coli strains belonging to phylogenetic group B2 have superior capacity to persist in the intestinal microflora of infants. J Infect Dis 191 1078 1083
15. GiraudAArousSDe PaepeMGaboriau-RouthiauVBambouJC 2008 Dissecting the genetic components of adaptation of Escherichia coli to the mouse gut. PLoS Genet 4 e2
16. CaseCCBukauBGranettSVillarejoMRBoosW 1986 Contrasting mechanisms of envZ control of mal and pho regulon genes in Escherichia coli. J Bacteriol 166 706 712
17. WannerBLSarthyABeckwithJ 1979 Escherichia coli pleiotropic mutant that reduces amounts of several periplasmic and outer membrane proteins. J Bacteriol 140 229 239
18. BoosWShumanH 1998 Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol Mol Biol Rev 62 204 229
19. ElenaSFLenskiRE 2003 Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4 457 469
20. RaineyPBBucklingAKassenRTravisanoM 2000 The emergence and maintenance of diversity: insights from experimental bacterial populations. Trends Ecol Evol 15 243 247
21. Rakoff-NahoumSPaglinoJEslami-VarzanehFEdbergSMedzhitovR 2004 Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118 229 241
22. PetersonDAMcNultyNPGurugeJLGordonJI 2007 IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2 328 339
23. StecherBRobbianiRWalkerAWWestendorfAMBarthelM 2007 Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5 2177 2189
24. WinterSEThiennimitrPWinterMGButlerBPHusebyDL 2010 Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467 426 429
25. GewirtzATNavasTALyonsSGodowskiPJMadaraJL 2001 Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167 1882 1885
26. BambouJCGiraudAMenardSBegueBRakotobeS 2004 In vitro and ex vivo activation of the TLR5 signaling pathway in intestinal epithelial cells by a commensal Escherichia coli strain. J Biol Chem 279 42984 42992
27. Gaboriau-RouthiauVRakotobeSLecuyerEMulderILanA 2009 The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31 677 689
28. CarvalhoFABarnichNSivignonADarchaCChanCH 2009 Crohn's disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. J Exp Med 206 2179 2189
29. FontaineFStewartEJLindnerABTaddeiF 2008 Mutations in two global regulators lower individual mortality in Escherichia coli. Mol Microbiol 67 2 14
30. DiardMBaeriswylSClermontOGouriouSPicardB 2007 Caenorhabditis elegans as a simple model to study phenotypic and genetic virulence determinants of extraintestinal pathogenic Escherichia coli. Microbes Infect 9 214 223
31. RamosHCRumboMSirardJC 2004 Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol 12 509 517
32. WrightKJSeedPCHultgrenSJ 2005 Uropathogenic Escherichia coli flagella aid in efficient urinary tract colonization. Infect Immun 73 7657 7668
33. MaurelliATFernandezREBlochCARodeCKFasanoA 1998 “Black holes” and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc Natl Acad Sci U S A 95 3943 3948
34. GironJA 2005 Role of Flagella in Mucosal Colonization. NataroJP Colonization of Mucosal Surfaces Washington ASM Press 213 236
35. MacLeanRC 2005 Adaptive radiation in microbial microcosms. J Evol Biol 18 1376 1386
36. BarrettRDMacLeanRCBellG 2005 Experimental evolution of Pseudomonas fluorescens in simple and complex environments. Am Nat 166 470 480
37. LeathamMPStevensonSJGaugerEJKrogfeltKALinsJJ 2005 Mouse intestine selects nonmotile flhDC mutants of Escherichia coli MG1655 with increased colonizing ability and better utilization of carbon sources. Infect Immun 73 8039 8049
38. GaugerEJLeathamMPMercado-LuboRLauxDCConwayT 2007 Role of motility and the flhDC Operon in Escherichia coli MG1655 colonization of the mouse intestine. Infect Immun 75 3315 3324
39. ChangDESmalleyDJTuckerDLLeathamMPNorrisWE 2004 Carbon nutrition of Escherichia coli in the mouse intestine. Proc Natl Acad Sci U S A 101 7427 7432
40. OshimaTAibaHMasudaYKanayaSSugiuraM 2002 Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol Microbiol 46 281 291
41. PrussBMCampbellJWVan DykTKZhuCKoganY 2003 FlhD/FlhC is a regulator of anaerobic respiration and the Entner-Doudoroff pathway through induction of the methyl-accepting chemotaxis protein Aer. J Bacteriol 185 534 543
42. PeekhausNConwayT 1998 What's for dinner?: Entner-Doudoroff metabolism in Escherichia coli. J Bacteriol 180 3495 3502
43. Notley-McRobbLFerenciT 1999 The generation of multiple co-existing mal-regulatory mutations through polygenic evolution in glucose-limited populations of Escherichia coli. Environ Microbiol 1 45 52
44. PrussBMMatsumuraP 1996 A regulator of the flagellar regulon of Escherichia coli, flhD, also affects cell division. J Bacteriol 178 668 674
45. PrussBMMarkovicDMatsumuraP 1997 The Escherichia coli flagellar transcriptional activator flhD regulates cell division through induction of the acid response gene cadA. J Bacteriol 179 3818 3821
46. HeGShankarRAChzhanMSamouilovAKuppusamyP 1999 Noninvasive measurement of anatomic structure and intraluminal oxygenation in the gastrointestinal tract of living mice with spatial and spectral EPR imaging. Proc Natl Acad Sci U S A 96 4586 4591
47. MacnabRM 1992 Genetics and biogenesis of bacterial flagella. Annu Rev Genet 26 131 158
48. LiuXNgCFerenciT 2000 Global adaptations resulting from high population densities in Escherichia coli cultures. J Bacteriol 182 4158 4164
49. NikaidoH 2003 Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67 593 656
50. HsingWRussoFDBerndKKSilhavyTJ 1998 Mutations that alter the kinase and phosphatase activities of the two-component sensor EnvZ. J Bacteriol 180 4538 4546
51. Cerf-BensussanNGaboriau-RouthiauV 2010 The immune system and the gut microbiota: friends or foes? Nat Rev Immunol 10 735 744
52. BegleyMGahanCGHillC 2005 The interaction between bacteria and bile. FEMS Microbiol Rev 29 625 651
53. MerrittMEDonaldsonJR 2009 Effect of bile salts on the DNA and membrane integrity of enteric bacteria. J Med Microbiol 58 1533 1541
54. HazlettLWuM 2010 Defensins in innate immunity. Cell Tissue Res
55. JaffeAChabbertYASemoninO 1982 Role of porin proteins OmpF and OmpC in the permeation of beta-lactams. Antimicrob Agents Chemother 22 942 948
56. AmslerCDChoMMatsumuraP 1993 Multiple factors underlying the maximum motility of Escherichia coli as cultures enter post-exponential growth. J Bacteriol 175 6238 6244
57. ZhaoKLiuMBurgessRR 2007 Adaptation in bacterial flagellar and motility systems: from regulon members to ‘foraging’-like behavior in E. coli. Nucleic Acids Res 35 4441 4452
58. LiuMDurfeeTCabreraJEZhaoKJinDJ 2005 Global transcriptional programs reveal a carbon source foraging strategy by Escherichia coli. J Biol Chem 280 15921 15927
59. DeathANotleyLFerenciT 1993 Derepression of LamB protein facilitates outer membrane permeation of carbohydrates into Escherichia coli under conditions of nutrient stress. J Bacteriol 175 1475 1483
60. Notley-McRobbLSeetoSFerenciT 2003 The influence of cellular physiology on the initiation of mutational pathways in Escherichia coli populations. Proc Biol Sci 270 843 848
61. PelosiLKuhnLGuettaDGarinJGeiselmannJ 2006 Parallel changes in global protein profiles during long-term experimental evolution in Escherichia coli. Genetics 173 1851 1869
62. KingTIshihamaAKoriAFerenciT 2004 A regulatory trade-off as a source of strain variation in the species Escherichia coli. J Bacteriol 186 5614 5620
63. LenskiREHattinghSE 1986 Coexistence of two competitors on one resource and one inhibitor: a chemostat model based on bacteria and antibiotics. J Theor Biol 122 83 93
64. HsuSBLiYSWaltmanP 2000 Competition in the presence of a lethal external inhibitor. Math Biosci 167 177 199
65. GudeljIWeitzJSFerenciTClaire Horner-DevineMMarxCJ 2010 An integrative approach to understanding microbial diversity: from intracellular mechanisms to community structure. Ecol Lett 13 1073 1084
66. LevertMZamfirOClermontOBouvetOLespinatsS 2010 Molecular and evolutionary bases of within-patient genotypic and phenotypic diversity in Escherichia coli extraintestinal infections. PLoS Pathog 6
67. BlattnerFRPlunkettG3rdBlochCAPernaNTBurlandV 1997 The complete genome sequence of Escherichia coli K-12. Science 277 1453 1474
68. CornejoOERozenDEMayRMLevinBR 2009 Oscillations in continuous culture populations of Streptococcus pneumoniae: population dynamics and the evolution of clonal suicide. Proc Biol Sci 276 999 1008
69. GourseRLde BoerHANomuraM 1986 DNA determinants of rRNA synthesis in E. coli: growth rate dependent regulation, feedback inhibition, upstream activation, antitermination. Cell 44 197 205
70. LiangSBipatnathMXuYChenSDennisP 1999 Activities of constitutive promoters in Escherichia coli. J Mol Biol 292 19 37
71. MurrayHDGourseRL 2004 Unique roles of the rrn P2 rRNA promoters in Escherichia coli. Mol Microbiol 52 1375 1387
72. GiraudAMaticITenaillonOClaraARadmanM 2001 Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science 291 2606 2608
73. AugerEABennettGN 1989 Regulation of lysine decarboxylase activity in Escherichia coli K-12. Arch Microbiol 151 466 468
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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