Like Will to Like: Abundances of Closely Related Species Can Predict Susceptibility to Intestinal Colonization by Pathogenic and Commensal Bacteria

English version České info

The intestinal ecosystem is formed by a complex, yet highly characteristic microbial community. The parameters defining whether this community permits invasion of a new bacterial species are unclear. In particular, inhibition of enteropathogen infection by the gut microbiota ( = colonization resistance) is poorly understood. To analyze the mechanisms of microbiota-mediated protection from Salmonella enterica induced enterocolitis, we used a mouse infection model and large scale high-throughput pyrosequencing. In contrast to conventional mice (CON), mice with a gut microbiota of low complexity (LCM) were highly susceptible to S. enterica induced colonization and enterocolitis. Colonization resistance was partially restored in LCM-animals by co-housing with conventional mice for 21 days (LCM^con21). 16S rRNA sequence analysis comparing LCM, LCM^con21 and CON gut microbiota revealed that gut microbiota complexity increased upon conventionalization and correlated with increased resistance to S. enterica infection. Comparative microbiota analysis of mice with varying degrees of colonization resistance allowed us to identify intestinal ecosystem characteristics associated with susceptibility to S. enterica infection. Moreover, this system enabled us to gain further insights into the general principles of gut ecosystem invasion by non-pathogenic, commensal bacteria. Mice harboring high commensal E. coli densities were more susceptible to S. enterica induced gut inflammation. Similarly, mice with high titers of Lactobacilli were more efficiently colonized by a commensal Lactobacillus reuteri ^RR strain after oral inoculation. Upon examination of 16S rRNA sequence data from 9 CON mice we found that closely related phylotypes generally display significantly correlated abundances (co-occurrence), more so than distantly related phylotypes. Thus, in essence, the presence of closely related species can increase the chance of invasion of newly incoming species into the gut ecosystem. We provide evidence that this principle might be of general validity for invasion of bacteria in preformed gut ecosystems. This might be of relevance for human enteropathogen infections as well as therapeutic use of probiotic commensal bacteria.

Vyšlo v časopise: Like Will to Like: Abundances of Closely Related Species Can Predict Susceptibility to Intestinal Colonization by Pathogenic and Commensal Bacteria. PLoS Pathog 6(1): e32767. doi:10.1371/journal.ppat.1000711
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000711

Souhrn

Zdroje

1. PalmerC

BikEM

DigiulioDB

RelmanDA

BrownPO

2007 Development of the Human Infant Intestinal Microbiota. PLoS Biol 5 e177 doi:10.1371/journal.pbio.0050177

2. DethlefsenL

HuseS

SoginML

RelmanDA

2008 The Pervasive Effects of an Antibiotic on the Human Gut Microbiota, as Revealed by Deep 16S rRNA Sequencing. PLoS Biol 6 e280 doi:10.1371/journal.pbio.0060280

3. LeyRE

HamadyM

LozuponeC

TurnbaughPJ

RameyRR

2008 Evolution of mammals and their gut microbes. Science 320 1647 1651

4. TurnbaughPJ

HamadyM

YatsunenkoT

CantarelBL

DuncanA

2009 A core gut microbiome in obese and lean twins. Nature 457 480 484

5. van der WaaijD

Berghuis-de VriesJM

LekkerkerkL-v

1971 Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J Hyg (Lond) 69 405 411

6. WilsonKH

SheagrenJN

FreterR

WeatherbeeL

LyerlyD

1986 Gnotobiotic models for study of the microbial ecology of Clostridium difficile and Escherichia coli. J Infect Dis 153 547 551

7. StecherB

HardtWD

2008 The role of microbiota in infectious disease. Trends Microbiol 16 107 114

8. QueJU

HentgesDJ

1985 Effect of streptomycin administration on colonization resistance to Salmonella typhimurium in mice. Infect Immun 48 169 174

9. KellyCP

LaMontJT

1998 Clostridium difficile infection. Annu Rev Med 49 375 390

10. VollaardEJ

ClasenerHA

van SaeneHK

MullerNF

1990 Effect on colonization resistance: an important criterion in selecting antibiotics. Dicp 24 60 66

11. StecherB

MacphersonAJ

HapfelmeierS

KremerM

StallmachT

2005 Comparison of Salmonella enterica Serovar Typhimurium Colitis in Germfree Mice and Mice Pretreated with Streptomycin. Infect Immun 73 3228 3241

12. StecherB

RobbianiR

WalkerAW

WestendorfAM

BarthelM

2007 Salmonella enterica Serovar Typhimurium Exploits Inflammation to Compete with the Intestinal Microbiota. PLoS Biol 5 e244 doi:10.1371/journal.pbio.0050244

13. SaxelinM

PessiT

SalminenS

1995 Fecal recovery following oral administration of Lactobacillus strain GG (ATCC 53103) in gelatine capsules to healthy volunteers. Int J Food Microbiol 25 199 203

14. AlanderM

SatokariR

KorpelaR

SaxelinM

Vilpponen-SalmelaT

1999 Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl Environ Microbiol 65 351 354

15. DunneC

MurphyL

FlynnS

O'MahonyL

O'HalloranS

1999 Probiotics: from myth to reality. Demonstration of functionality in animal models of disease and in human clinical trials. Antonie Van Leeuwenhoek 76 279 292

16. PrilassnigM

WenischC

DaxboeckF

FeierlG

2007 Are probiotics detectable in human feces after oral uptake by healthy volunteers? Wien Klin Wochenschr 119 456 462

17. DenouE

PridmoreRD

BergerB

PanoffJM

ArigoniF

2008 Identification of genes associated with the long-gut-persistence phenotype of the probiotic Lactobacillus johnsonii strain NCC533 using a combination of genomics and transcriptome analysis. J Bacteriol 190 3161 3168

18. BarthelM

HapfelmeierS

Quintanilla-MartinezL

KremerM

RohdeM

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

19. JungS

AlibertiJ

GraemmelP

SunshineMJ

KreutzbergGW

2000 Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20 4106 4114

20. AdachiO

KawaiT

TakedaK

MatsumotoM

TsutsuiH

1998 Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9 143 150

21. HapfelmeierS

MullerAJ

StecherB

KaiserP

BarthelM

2008 Microbe sampling by mucosal dendritic cells is a discrete, MyD88-independent step in DeltainvG S. Typhimurium colitis. J Exp Med 205 437 450

22. SuarM

JantschJ

HapfelmeierS

KremerM

StallmachT

2006 Virulence of broad- and narrow-host-range Salmonella enterica serovars in the streptomycin-pretreated mouse model. Infect Immun 74 632 644

23. HoisethSK

StockerBA

1981 Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291 238 239

24. HapfelmeierS

EhrbarK

StecherB

BarthelM

KremerM

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

25. WhiteJR

NagarajanN

PopM

2009 Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5 e1000352 doi:10.1371/journal.pcbi.1000352

26. Sarma-RupavtarmRB

GeZ

SchauerDB

FoxJG

PolzMF

2004 Spatial distribution and stability of the eight microbial species of the altered schaedler flora in the mouse gastrointestinal tract. Appl Environ Microbiol 70 2791 2800

27. WeisburgWG

BarnsSM

PelletierDA

LaneDJ

1991 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173 697 703

28. ColeJR

WangQ

CardenasE

FishJ

ChaiB

2009 The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37 D141 145

29. KuninV

EngelbrektsonA

OchmanH

HugenholtzP

2009 Wrinkles in the rare biosphere: pyrosequencing errors lead to artificial inflation of diversity estimates. Environ Microbiol

30. HuseSM

DethlefsenL

HuberJA

WelchDM

RelmanDA

2008 Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4 e1000255 doi:10.1371/journal.pgen.1000255

31. DeSantisTZ

HugenholtzP

LarsenN

RojasM

BrodieEL

2006 Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72 5069 5072

32. EddySR

2002 A memory-efficient dynamic programming algorithm for optimal alignment of a sequence to an RNA secondary structure. BMC Bioinformatics 3 18

33. WangQ

GarrityGM

TiedjeJM

ColeJR

2007 Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73 5261 5267

34. SoginML

MorrisonHG

HuberJA

WelchDM

HuseSM

2006 Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc Natl Acad Sci U S A 103 12115 12120

35. KanagawaT

2003 Bias and artifacts in multitemplate polymerase chain reactions (PCR). J Biosci Bioeng 96 317 323

36. QuinceC

LanzenA

CurtisTP

DavenportRJ

HallN

2009 Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6 639 641

37. AshelfordKE

ChuzhanovaNA

FryJC

JonesAJ

WeightmanAJ

2006 New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72 5734 5741

38. SekirovI

TamNM

JogovaM

RobertsonML

LiY

2008 Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun 76 4726 4736

39. DewhirstFE

ChienCC

PasterBJ

EricsonRL

OrcuttRP

1999 Phylogeny of the defined murine microbiota: altered Schaedler flora. Appl Environ Microbiol 65 3287 3292

40. GeZ

FengY

TaylorNS

OhtaniM

PolzMF

2006 Colonization dynamics of altered Schaedler flora is influenced by gender, aging, and Helicobacter hepaticus infection in the intestines of Swiss Webster mice. Appl Environ Microbiol 72 5100 5103

41. CollinsFM

CarterPB

1978 Growth of salmonellae in orally infected germfree mice. Infect Immun 21 41 47

42. KoopmanJP

KennisHM

MullinkJW

PrinsRA

StadhoudersAM

1984 ‘Normalization’ of germfree mice with anaerobically cultured caecal flora of ‘normal’ mice. Lab Anim 18 188 194

43. FreterR

AbramsGD

1972 Function of various intestinal bacteria in converting germfree mice to the normal state. Infect Immun 6 119 126

44. FreterR

BricknerH

BotneyM

ClevenD

ArankiA

1983 Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect Immun 39 676 685

45. ItohK

FreterR

1989 Control of Escherichia coli populations by a combination of indigenous clostridia and lactobacilli in gnotobiotic mice and continuous-flow cultures. Infect Immun 57 559 565

46. SmithK

McCoyKD

MacphersonAJ

2007 Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin Immunol 19 59 69

47. CashHL

WhithamCV

BehrendtCL

HooperLV

2006 Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313 1126 1130

48. BrandlK

PlitasG

SchnablB

DeMatteoRP

PamerEG

2007 MyD88-mediated signals induce the bactericidal lectin RegIII gamma and protect mice against intestinal Listeria monocytogenes infection. J Exp Med 204 1891 1900

49. CandelaM

PernaF

CarnevaliP

VitaliB

CiatiR

2008 Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol 125 286 292

50. Filho-LimaJV

VieiraEC

NicoliJR

2000 Antagonistic effect of Lactobacillus acidophilus, Saccharomyces boulardii and Escherichia coli combinations against experimental infections with Shigella flexneri and Salmonella enteritidis subsp. typhimurium in gnotobiotic mice. J Appl Microbiol 88 365 370

51. CursinoL

SmajsD

SmardaJ

NardiRM

NicoliJR

2006 Exoproducts of the Escherichia coli strain H22 inhibiting some enteric pathogens both in vitro and in vivo. J Appl Microbiol 100 821 829

52. MilletteM

CornutG

DupontC

ShareckF

ArchambaultD

2008 Capacity of human nisin- and pediocin-producing lactic Acid bacteria to reduce intestinal colonization by vancomycin-resistant enterococci. Appl Environ Microbiol 74 1997 2003

53. GantoisI

DucatelleR

PasmansF

HaesebrouckF

HautefortI

2006 Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol 72 946 949

54. KoopmanJP

JanssenFG

van DrutenJA

1975 Oxidation-reduction potentials in the cecal contents of rats and mice. Proc Soc Exp Biol Med 149 995 999

55. MacfarlaneGT

MacfarlaneS

1997 Human colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria. Scand J Gastroenterol Suppl 222 3 9

56. MacfarlaneS

MacfarlaneGT

2003 Regulation of short-chain fatty acid production. Proc Nutr Soc 62 67 72

57. SavageDC

1977 Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31 107 133

58. HeG

ShankarRA

ChzhanM

SamouilovA

KuppusamyP

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

59. KomitopoulouE

BaintonNJ

AdamsMR

2004 Premature Salmonella Typhimurium growth inhibition in competition with other Gram-negative organisms is redox potential regulated via RpoS induction. J Appl Microbiol 97 964 972

60. LeeA

GemmellE

1972 Changes in the mouse intestinal microflora during weaning: role of volatile fatty acids. Infect Immun 5 1 7

61. VollaardEJ

ClasenerHA

1994 Colonization resistance. Antimicrob Agents Chemother 38 409 414

62. 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

63. van der WaaijD

1983 Colonization pattern of the digestive tract by potentially pathogenic microorganisms: colonization-controlling mechanisms and consequences for antibiotic treatment. Infection 11 Suppl 2 S90 92

64. LeathamMP

BanerjeeS

AutieriSM

Mercado-LuboR

ConwayT

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 77 2876 2886