The Evolution of Host Specialization in the Vertebrate Gut Symbiont
Recent research has provided mechanistic insight into the important contributions of the gut microbiota to vertebrate biology, but questions remain about the evolutionary processes that have shaped this symbiosis. In the present study, we showed in experiments with gnotobiotic mice that the evolution of Lactobacillus reuteri with rodents resulted in the emergence of host specialization. To identify genomic events marking adaptations to the murine host, we compared the genome of the rodent isolate L. reuteri 100-23 with that of the human isolate L. reuteri F275, and we identified hundreds of genes that were specific to each strain. In order to differentiate true host-specific genome content from strain-level differences, comparative genome hybridizations were performed to query 57 L. reuteri strains originating from six different vertebrate hosts in combination with genome sequence comparisons of nine strains encompassing five phylogenetic lineages of the species. This approach revealed that rodent strains, although showing a high degree of genomic plasticity, possessed a specific genome inventory that was rare or absent in strains from other vertebrate hosts. The distinct genome content of L. reuteri lineages reflected the niche characteristics in the gastrointestinal tracts of their respective hosts, and inactivation of seven out of eight representative rodent-specific genes in L. reuteri 100-23 resulted in impaired ecological performance in the gut of mice. The comparative genomic analyses suggested fundamentally different trends of genome evolution in rodent and human L. reuteri populations, with the former possessing a large and adaptable pan-genome while the latter being subjected to a process of reductive evolution. In conclusion, this study provided experimental evidence and a molecular basis for the evolution of host specificity in a vertebrate gut symbiont, and it identified genomic events that have shaped this process.
Vyšlo v časopise:
The Evolution of Host Specialization in the Vertebrate Gut Symbiont. PLoS Genet 7(2): e32767. doi:10.1371/journal.pgen.1001314
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001314
Souhrn
Recent research has provided mechanistic insight into the important contributions of the gut microbiota to vertebrate biology, but questions remain about the evolutionary processes that have shaped this symbiosis. In the present study, we showed in experiments with gnotobiotic mice that the evolution of Lactobacillus reuteri with rodents resulted in the emergence of host specialization. To identify genomic events marking adaptations to the murine host, we compared the genome of the rodent isolate L. reuteri 100-23 with that of the human isolate L. reuteri F275, and we identified hundreds of genes that were specific to each strain. In order to differentiate true host-specific genome content from strain-level differences, comparative genome hybridizations were performed to query 57 L. reuteri strains originating from six different vertebrate hosts in combination with genome sequence comparisons of nine strains encompassing five phylogenetic lineages of the species. This approach revealed that rodent strains, although showing a high degree of genomic plasticity, possessed a specific genome inventory that was rare or absent in strains from other vertebrate hosts. The distinct genome content of L. reuteri lineages reflected the niche characteristics in the gastrointestinal tracts of their respective hosts, and inactivation of seven out of eight representative rodent-specific genes in L. reuteri 100-23 resulted in impaired ecological performance in the gut of mice. The comparative genomic analyses suggested fundamentally different trends of genome evolution in rodent and human L. reuteri populations, with the former possessing a large and adaptable pan-genome while the latter being subjected to a process of reductive evolution. In conclusion, this study provided experimental evidence and a molecular basis for the evolution of host specificity in a vertebrate gut symbiont, and it identified genomic events that have shaped this process.
Zdroje
1. LeyRE
PetersonDA
GordonJI
2006 Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124 837 848
2. CeruttiA
RescignoM
2008 The biology of intestinal immunoglobulin A responses. Immunity 28 740 750
3. DethlefsenL
McFall-NgaiM
RelmanDA
2007 An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449 811 818
4. LeyRE
HamadyM
LozuponeC
TurnbaughPJ
RameyRR
2008 Evolution of mammals and their gut microbes. Science 320 1647 1651
5. WalterJ
BrittonRA
RoosS
2010 Microbes and Health Sackler Colloquium: Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc Natl Acad Sci U S A Epub ahead of print
6. McFall-NgaiM
2007 Adaptive immunity: care for the community. Nature 445 153
7. StevensCE
HumeID
1998 Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78 393 427
8. LeyRE
LozuponeCA
HamadyM
KnightR
GordonJI
2008 Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6 776 788
9. SelaDA
ChapmanJ
AdeuyaA
KimJH
ChenF
2008 The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci U S A 105 18964 18969
10. XuJ
MahowaldMA
LeyRE
LozuponeCA
HamadyM
2007 Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol 5 e156 10.1371/journal.pbio.0050156
11. TurnbaughPJ
LeyRE
HamadyM
Fraser-LiggettCM
KnightR
2007 The human microbiome project. Nature 449 804 810
12. LinzB
BallouxF
MoodleyY
ManicaA
LiuH
2007 An African origin for the intimate association between humans and Helicobacter pylori. Nature 445 915 918
13. TenaillonO
SkurnikD
PicardB
DenamurE
2010 The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8 207 217
14. TouchonM
HoedeC
TenaillonO
BarbeV
BaeriswylS
2009 Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5 e1000344 10.1371/journal.pgen.1000344
15. BrooksSP
McAllisterM
SandozM
KalmokoffML
2003 Culture-independent phylogenetic analysis of the faecal flora of the rat. Can J Microbiol 49 589 601
16. LeserTD
AmenuvorJZ
JensenTK
LindecronaRH
BoyeM
2002 Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68 673 690
17. SalzmanNH
de JongH
PatersonY
HarmsenHJ
WellingGW
2002 Analysis of 16S libraries of mouse gastrointestinal microflora reveals a large new group of mouse intestinal bacteria. Microbiology 148 3651 3660
18. TannockGW
1992 Lactic microbiota of pigs, mice and rats.
WoodBJB
The Lactic Acid Bacteria in Health and Disease London Elsevier Applied Science 21 48
19. WalterJ
2008 Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol 74 4985 4996
20. OhPL
BensonAK
PetersonDA
PatilPB
MoriyamaEN
2010 Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. ISME J 4 377 387
21. CarbajalN
CasasIA
DobrogoszWJ
1999 Effect of host-specific Lactobacillus reuteri on ileal tissue development in gnotobiotic BALB/c mice. Microbial Ecol Health Dis 11 (Abst.) 184
22. CasasIA
DobrogoszWJ
2000 Validation of the Probiotic Concept: Lactobacillus reuteri Confers Broad-spectrum Protection against Disease in Humans and Animals. Microb Ecol Health Dis 12 247 285
23. MollerPL
PaerregaardA
GadM
KristensenNN
ClaessonMH
2005 Colitic scid mice fed Lactobacillus spp. show an ameliorated gut histopathology and an altered cytokine profile by local T cells. Inflamm Bowel Dis 11 814 819
24. SchreiberO
PeterssonJ
PhillipsonM
PerryM
RoosS
2009 Lactobacillus reuteri prevents colitis by reducing P-selectin-associated leukocyte- and platelet-endothelial cell interactions. Am J Physiol Gastrointest Liver Physiol 296 G534 542
25. LinJH-C
SavageDC
1984 Host specificity of the colonization of murine gastric epithelium by lactobacilli. FEMS Microbiol Letters 24 67 71
26. WesneyE
TannockGW
1979 Association of rat, pig, and fowl biotypes of lactobacilli with the stomach of gnotobiotic mice. Microb Ecol 5 35 42
27. SuegaraN
MorotomiM
WatanabeT
KawalY
MutaiM
1975 Behavior of microflora in the rat stomach: adhesion of lactobacilli to the keratinized epithelial cells of the rat stomach in vitro. Infect Immun 12 173 179
28. TannockGW
CrichtonC
WellingGW
KoopmanJP
MidtvedtT
1988 Reconstitution of the gastrointestinal microflora of Lactobacillus-free mice. Appl Environ Microbiol 54 2971 2975
29. MandelMJ
WollenbergMS
StabbEV
VisickKL
RubyEG
2009 A single regulatory gene is sufficient to alter bacterial host range. Nature 458 215 218
30. MoranNA
2007 Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci U S A 104 Suppl 1 8627 8633
31. MoranNA
PlagueGR
2004 Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14 627 633
32. MoyaA
PeretoJ
GilR
LatorreA
2008 Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9 218 229
33. DaleC
MoranNA
2006 Molecular interactions between bacterial symbionts and their hosts. Cell 126 453 465
34. MoritaH
TohH
FukudaS
HorikawaH
OshimaK
2008 Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobalamin production. DNA Res 15 151 161
35. NelsonKE
WeinstockGM
HighlanderSK
WorleyKC
CreasyHH
2010 A catalog of reference genomes from the human microbiome. Science 328 994 999
36. TannockGW
GhazallyS
WalterJ
LoachD
BrooksH
2005 Ecological behavior of Lactobacillus reuteri 100-23 is affected by mutation of the luxS gene. Appl Environ Microbiol 71 8419 8425
37. WalterJ
ChagnaudP
TannockGW
LoachDM
Dal BelloF
2005 A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl Environ Microbiol 71 979 986
38. WalterJ
HengNC
HammesWP
LoachDM
TannockGW
2003 Identification of Lactobacillus reuteri genes specifically induced in the mouse gastrointestinal tract. Appl Environ Microbiol 69 2044 2051
39. WalterJ
LoachDM
AlqumberM
RockelC
HermannC
2007 D-alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100-23 results in impaired colonization of the mouse gastrointestinal tract. Environ Microbiol 9 1750 1760
40. HoffmannM
RathE
HolzlwimmerG
Quintanilla-MartinezL
LoachD
2008 Lactobacillus reuteri 100-23 transiently activates intestinal epithelial cells of mice that have a complex microbiota during early stages of colonization. J Nutr 138 1684 1691
41. LivingstonM
LoachD
WilsonM
TannockGW
BairdM
2010 Gut commensal Lactobacillus reuteri 100-23 stimulates an immunoregulatory response. Immunol Cell Biol 88 99 102
42. HengNC
BateupJM
LoachDM
WuX
JenkinsonHF
1999 Influence of different functional elements of plasmid pGT232 on maintenance of recombinant plasmids in Lactobacillus reuteri populations in vitro and in vivo. Appl Environ Microbiol 65 5378 5385
43. SriramuluDD
LiangM
Hernandez-RomeroD
Raux-DeeryE
LunsdorfH
2008 Lactobacillus reuteri DSM 20016 produces cobalamin-dependent diol dehydratase in metabolosomes and metabolizes 1,2-propanediol by disproportionation. J Bacteriol 190 4559 4567
44. ReuterG
2001 The Lactobacillus and Bifidobacterium microflora of the human intestine: composition and succession. Curr Issues Intest Microbiol 2 43 53
45. ZhangC
ZhangM
JuJ
NietfeldtJ
WiseJ
2003 Genome diversification in phylogenetic lineages I and II of Listeria monocytogenes: identification of segments unique to lineage II populations. J Bacteriol 185 5573 5584
46. GorisJ
KonstantinidisKT
KlappenbachJA
CoenyeT
VandammeP
2007 DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57 81 91
47. LiYH
ChenYY
BurneRA
2000 Regulation of urease gene expression by Streptococcus salivarius growing in biofilms. Environ Microbiol 2 169 177
48. SjostromJE
LarssonH
1996 Factors affecting growth and antibiotic susceptibility of Helicobacter pylori: effect of pH and urea on the survival of a wild-type strain and a urease-deficient mutant. J Med Microbiol 44 425 433
49. RigelNW
BraunsteinM
2008 A new twist on an old pathway–accessory Sec [corrected] systems. Mol Microbiol 69 291 302
50. BensingBA
SullamPM
2009 Characterization of Streptococcus gordonii SecA2 as a paralogue of SecA. J Bacteriol 191 3482 3491
51. BensingBA
SullamPM
2002 An accessory sec locus of Streptococcus gordonii is required for export of the surface protein GspB and for normal levels of binding to human platelets. Mol Microbiol 44 1081 1094
52. FlynnS
van SinderenD
ThorntonGM
HoloH
NesIF
2002 Characterization of the genetic locus responsible for the production of ABP-118, a novel bacteriocin produced by the probiotic bacterium Lactobacillus salivarius subsp. salivarius UCC118. Microbiology 148 973 984
53. KleerebezemM
QuadriLE
KuipersOP
de VosWM
1997 Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol Microbiol 24 895 904
54. SturmeMH
FranckeC
SiezenRJ
de VosWM
KleerebezemM
2007 Making sense of quorum sensing in lactobacilli: a special focus on Lactobacillus plantarum WCFS1. Microbiology 153 3939 3947
55. TalaricoTL
AxelssonLT
NovotnyJ
FiuzatM
DobrogoszWJ
1990 Utilization of Glycerol as a Hydrogen Acceptor by Lactobacillus reuteri: Purification of 1,3-Propanediol:NAD Oxidoreductase. Appl Environ Microbiol 56 943 948
56. TalaricoTL
CasasIA
ChungTC
DobrogoszWJ
1988 Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri. Antimicrob Agents Chemother 32 1854 1858
57. FullerR
BarrowPA
BrookerBE
1978 Bacteria associated with the gastric epithelium of neonatal pigs. Appl Environ Microbiol 35 582 591
58. FullerR
BrookerBE
1974 Lactobacilli which attach to the crop epithelium of the fowl. Am J Clin Nutr 27 1305 1312
59. GoodmanAL
McNultyNP
ZhaoY
LeipD
MitraRD
2009 Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 6 279 289
60. SantosF
VeraJL
van der HeijdenR
ValdezG
de VosWM
2008 The complete coenzyme B12 biosynthesis gene cluster of Lactobacillus reuteri CRL1098. Microbiology 154 81 93
61. KikuchiY
HosokawaT
NikohN
MengXY
KamagataY
2009 Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biol 7 2
62. SullivanJT
RonsonCW
1998 Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci U S A 95 5145 5149
63. MediniD
DonatiC
TettelinH
MasignaniV
RappuoliR
2005 The microbial pan-genome. Curr Opin Genet Dev 15 589 594
64. TettelinH
MasignaniV
CieslewiczMJ
DonatiC
MediniD
2005 Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci U S A 102 13950 13955
65. RenoML
HeldNL
FieldsCJ
BurkePV
WhitakerRJ
2009 Biogeography of the Sulfolobus islandicus pan-genome. Proc Natl Acad Sci U S A 106 8605 8610
66. ProsserJI
BohannanBJ
CurtisTP
EllisRJ
FirestoneMK
2007 The role of ecological theory in microbial ecology. Nat Rev Microbiol 5 384 392
67. AchtmanM
2008 Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol 62 53 70
68. HoltKE
ParkhillJ
MazzoniCJ
RoumagnacP
WeillFX
2008 High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Genet 40 987 993
69. ChainPS
CarnielE
LarimerFW
LamerdinJ
StoutlandPO
2004 Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 101 13826 13831
70. BrightM
BulgheresiS
A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8 218 230
71. MoranNA
2003 Tracing the evolution of gene loss in obligate bacterial symbionts. Curr Opin Microbiol 6 512 518
72. EppingerM
BaarC
LinzB
RaddatzG
LanzC
2006 Who ate whom? Adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. PLoS Genet 2 e120 10.1371/journal.pgen.0020120
73. HoldenMT
HeatherZ
PaillotR
StewardKF
WebbK
2009 Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens. PLoS Pathog 5 e1000346 10.1371/journal.ppat.1000346
74. ParkhillJ
SebaihiaM
PrestonA
MurphyLD
ThomsonN
2003 Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35 32 40
75. LowderBV
GuinaneCM
Ben ZakourNL
WeinertLA
Conway-MorrisA
2009 Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad Sci U S A 106 19545 19550
76. CostelloEK
LauberCL
HamadyM
FiererN
GordonJI
2009 Bacterial Community Variation in Human Body Habitats Across Space and Time. Science
77. MedinaM
SachsJL
2010 Symbiont genomics, our new tangled bank. Genomics 95 129 137
78. RubyEG
UrbanowskiM
CampbellJ
DunnA
FainiM
2005 Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc Natl Acad Sci U S A 102 3004 3009
79. NormandP
LapierreP
TisaLS
GogartenJP
AlloisioN
2007 Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17 7 15
80. MarkowitzVM
SzetoE
PalaniappanK
GrechkinY
ChuK
2008 The integrated microbial genomes (IMG) system in 2007: data content and analysis tool extensions. Nucleic Acids Res 36 D528 533
81. CarverTJ
RutherfordKM
BerrimanM
RajandreamMA
BarrellBG
2005 ACT: the Artemis Comparison Tool. Bioinformatics 21 3422 3423
82. VernikosGS
ParkhillJ
2006 Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22 2196 2203
83. KonstantinidisKT
TiedjeJM
2005 Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 102 2567 2572
84. RouillardJM
ZukerM
GulariE
2003 OligoArray 2.0: design of oligonucleotide probes for DNA microarrays using a thermodynamic approach. Nucleic Acids Res 31 3057 3062
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 2
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Meta-Analysis of Genome-Wide Association Studies in Celiac Disease and Rheumatoid Arthritis Identifies Fourteen Non-HLA Shared Loci
- MiRNA Control of Vegetative Phase Change in Trees
- The Cardiac Transcription Network Modulated by Gata4, Mef2a, Nkx2.5, Srf, Histone Modifications, and MicroRNAs
- Genome-Wide Transcript Profiling of Endosperm without Paternal Contribution Identifies Parent-of-Origin–Dependent Regulation of