Host Imprints on Bacterial Genomes—Rapid, Divergent Evolution in Individual Patients
Bacteria lose or gain genetic material and through selection, new variants become fixed in the population. Here we provide the first, genome-wide example of a single bacterial strain's evolution in different deliberately colonized patients and the surprising insight that hosts appear to personalize their microflora. By first obtaining the complete genome sequence of the prototype asymptomatic bacteriuria strain E. coli 83972 and then resequencing its descendants after therapeutic bladder colonization of different patients, we identified 34 mutations, which affected metabolic and virulence-related genes. Further transcriptome and proteome analysis proved that these genome changes altered bacterial gene expression resulting in unique adaptation patterns in each patient. Our results provide evidence that, in addition to stochastic events, adaptive bacterial evolution is driven by individual host environments. Ongoing loss of gene function supports the hypothesis that evolution towards commensalism rather than virulence is favored during asymptomatic bladder colonization.
Vyšlo v časopise:
Host Imprints on Bacterial Genomes—Rapid, Divergent Evolution in Individual Patients. PLoS Pathog 6(8): e32767. doi:10.1371/journal.ppat.1001078
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1001078
Souhrn
Bacteria lose or gain genetic material and through selection, new variants become fixed in the population. Here we provide the first, genome-wide example of a single bacterial strain's evolution in different deliberately colonized patients and the surprising insight that hosts appear to personalize their microflora. By first obtaining the complete genome sequence of the prototype asymptomatic bacteriuria strain E. coli 83972 and then resequencing its descendants after therapeutic bladder colonization of different patients, we identified 34 mutations, which affected metabolic and virulence-related genes. Further transcriptome and proteome analysis proved that these genome changes altered bacterial gene expression resulting in unique adaptation patterns in each patient. Our results provide evidence that, in addition to stochastic events, adaptive bacterial evolution is driven by individual host environments. Ongoing loss of gene function supports the hypothesis that evolution towards commensalism rather than virulence is favored during asymptomatic bladder colonization.
Zdroje
1. ShihAC
HsiaoTC
HoMS
LiWH
2007 Simultaneous amino acid substitutions at antigenic sites drive influenza A hemagglutinin evolution. Proc Natl Acad Sci U S A 104 6283 6288
2. PalmerGH
BraytonKA
2007 Gene conversion is a convergent strategy for pathogen antigenic variation. Trends Parasitol 23 408 413
3. TempletonTJ
2009 The varieties of gene amplification, diversification and hypervariability in the human malaria parasite, Plasmodium falciparum. Mol Biochem Parasitol 166 109 116
4. DeitschKW
LukehartSA
StringerJR
2009 Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nat Rev Microbiol 7 493 503
5. LindbergU
ClaessonI
HansonLA
JodalU
1978 Asymptomatic bacteriuria in schoolgirls. VIII. Clinical course during a 3-year follow-up. J Pediatr 92 194 199
6. SundénF
HåkanssonL
LjunggrenE
WulltB
2006 Bacterial interference-is deliberate colonization with Escherichia coli 83972 an alternative treatment for patients with recurrent urinary tract infection? Int J Antimicrob Agents 28 Suppl 1 S26 29
7. KlemmP
RoosV
UlettGC
SvanborgC
SchembriMA
2006 Molecular characterization of the Escherichia coli asymptomatic bacteriuria strain 83972: the taming of a pathogen. Infect Immun 74 781 785
8. ZdziarskiJ
SvanborgC
WulltB
HackerJ
DobrindtU
2008 Molecular basis of commensalism in the urinary tract: low virulence or virulence attenuation? Infect Immun 76 695 703
9. SundénF
HåkanssonL
LjunggrenE
WulltB
2010 Escherichia coli 83972 bacteriuria protects against recurrent lower urinary tract infections in patients with incomplete bladder emptying. J Urol 184 179 185
10. GrozdanovL
RaaschC
SchulzeJ
SonnenbornU
GottschalkG
2004 Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J Bacteriol 186 5432 5441
11. HirakawaH
NishinoK
HirataT
YamaguchiA
2003 Comprehensive studies of drug resistance mediated by overexpression of response regulators of two-component signal transduction systems in Escherichia coli. J Bacteriol 185 1851 1856
12. MinagawaS
OgasawaraH
KatoA
YamamotoK
EguchiY
2003 Identification and molecular characterization of the Mg2+ stimulon of Escherichia coli. J Bacteriol 185 3696 3702
13. TomeniusH
PernestigAK
JonasK
GeorgellisD
MollbyR
2006 The Escherichia coli BarA-UvrY two-component system is a virulence determinant in the urinary tract. BMC Microbiol 6 27
14. DebarbieuxL
BohinA
BohinJP
1997 Topological analysis of the membrane-bound glycosyltransferase, MdoH, required for osmoregulated periplasmic glucan synthesis in Escherichia coli. J Bacteriol 179 6692 6698
15. LiuL
HausladenA
ZengM
QueL
HeitmanJ
2001 A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410 490 494
16. GreenbergJT
ChouJH
MonachPA
DempleB
1991 Activation of oxidative stress genes by mutations at the soxQ/cfxB/marA locus of Escherichia coli. J Bacteriol 173 4433 4439
17. JubelinG
VianneyA
BeloinC
GhigoJM
LazzaroniJC
2005 CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 187 2038 2049
18. PernestigAK
GeorgellisD
RomeoT
SuzukiK
TomeniusH
2003 The Escherichia coli BarA-UvrY two-component system is needed for efficient switching between glycolytic and gluconeogenic carbon sources. J Bacteriol 185 843 853
19. HerringCD
RaghunathanA
HonischC
PatelT
ApplebeeMK
2006 Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat Genet 38 1406 1412
20. PhilippeN
CrozatE
LenskiRE
SchneiderD
2007 Evolution of global regulatory networks during a long-term experiment with Escherichia coli. Bioessays 29 846 860
21. AnforaAT
HalladinDK
HaugenBJ
WelchRA
2008 Uropathogenic Escherichia coli CFT073 is adapted to acetatogenic growth but does not require acetate during murine urinary tract infection. Infect Immun 76 5760 5767
22. MoritzRL
WelchRA
2006 The Escherichia coli argW-dsdCXA genetic island is highly variable, and E. coli K1 strains commonly possess two copies of dsdCXA. J Clin Microbiol 44 4038 4048
23. PreumontA
SnoussiK
StroobantV
ColletJF
Van SchaftingenE
2008 Molecular identification of pseudouridine-metabolizing enzymes. J Biol Chem 283 25238 25246
24. AlteriCJ
SmithSN
MobleyHL
2009 Fitness of Escherichia coli during urinary tract infection requires gluconeogenesis and the TCA cycle. PLoS Pathog 5 e1000448
25. WarnerDM
LevySB
2009 Different effects of transcriptional regulators marA, soxS, and rob on susceptibility of Escherichia coli to cationic antimicrobial peptides (CAMPs): Rob-dependent CAMP induction of the marRAB operon. Microbiology doi:10.1099/mic.0.033415-0
26. BryzgunovaOE
SkvortsovaTE
KolesnikovaEV
StarikovAV
RykovaEY
2006 Isolation and comparative study of cell-free nucleic acids from human urine. Ann N Y Acad Sci 1075 334 340
27. HaganEC
MobleyHL
2007 Uropathogenic Escherichia coli outer membrane antigens expressed during urinary tract infection. Infect Immun 75 3941 3949
28. BettelheimKA
TaylorJ
1969 A study of Escherichia coli isolated from chronic urinary infection. J Med Microbiol 2 225 236
29. OlesenB
KolmosHJ
ØrskovF
ØrskovI
1998 Escherichia coli bacteraemia in patients with and without haematological malignancies: a study of strain characters and recurrent episodes. J Infect 36 93 100
30. BielaszewskaM
KockR
FriedrichAW
von EiffC
ZimmerhacklLB
2007 Shiga toxin-mediated hemolytic uremic syndrome: time to change the diagnostic paradigm? PLoS One 2 e1024
31. BarrickJE
YuDS
YoonSH
JeongH
OhTK
2009 Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461 1243 1247
32. JelsbakL
JohansenHK
FrostAL
ThogersenR
ThomsenLE
2007 Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients. Infect Immun 75 2214 2224
33. OhJD
Kling-BackhedH
GiannakisM
XuJ
FultonRS
2006 The complete genome sequence of a chronic atrophic gastritis Helicobacter pylori strain: evolution during disease progression. Proc Natl Acad Sci U S A 103 9999 10004
34. BjedovI
TenaillonO
GerardB
SouzaV
DenamurE
2003 Stress-induced mutagenesis in bacteria. Science 300 1404 1409
35. RosenbergSM
2001 Evolving responsively: adaptive mutation. Nat Rev Genet 2 504 515
36. GiraudA
ArousS
De PaepeM
Gaboriau-RouthiauV
BambouJC
2008 Dissecting the genetic components of adaptation of Escherichia coli to the mouse gut. PLoS Genet 4 e2
37. NovakM
PfeifferT
LenskiRE
SauerU
BonhoefferS
2006 Experimental tests for an evolutionary trade-off between growth rate and yield in E. coli. Am Nat 168 242 251
38. LundstedtAC
McCarthyS
GustafssonMC
GodalyG
JodalU
2007 A genetic basis of susceptibility to acute pyelonephritis. PLoS One 2 e825
39. FischerH
LutayN
RagnarsdóttirB
YadavM
JönssonK
2010 IRF3-dependent signalling, human polymorphism and innate resistance to kidney infection. in revision
40. RagnarsdóttirB
JönssonK
UrbanoA
Grönberg-HernandezJ
LutayN
2010 Toll-like receptor 4 promoter polymorphisms: Common TLR4 variants protect against severe urinary tract infection. PLoS One
41. BergstenG
SamuelssonM
WulltB
LeijonhufvudI
FischerH
2004 PapG-dependent adherence breaks mucosal inertia and triggers the innate host response. J Infect Dis 189 1734 1742
42. FrendeusB
GodalyG
HangL
KarpmanD
LundstedtAC
2000 Interleukin 8 receptor deficiency confers susceptibility to acute experimental pyelonephritis and may have a human counterpart. J Exp Med 192 881 890
43. RagnarsdottirB
FischerH
GodalyG
Gronberg-HernandezJ
GustafssonM
2008 TLR- and CXCR1-dependent innate immunity: insights into the genetics of urinary tract infections. Eur J Clin Invest 38 Suppl 2 12 20
44. BergstenG
WulltB
SvanborgC
2005 Escherichia coli, fimbriae, bacterial persistence and host response induction in the human urinary tract. Int J Med Microbiol 295 487 502
45. HaldaneJB
1949 Suggestions as to quantitative measurement of rates of evolution. Evolution 3 51 56
46. StadenR
BealKF
BonfieldJK
2000 The Staden package, 1998. Methods Mol Biol 132 115 130
47. TechM
MerklR
2003 YACOP: Enhanced gene prediction obtained by a combination of existing methods. In Silico Biol 3 441 451
48. OverbeekR
LarsenN
WalunasT
D'SouzaM
PuschG
2003 The ERGO genome analysis and discovery system. Nucleic Acids Res 31 164 171
49. CarverT
BerrimanM
TiveyA
PatelC
BohmeU
2008 Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 24 2672 2676
50. AltschulSF
MaddenTL
SchafferAA
ZhangJ
ZhangZ
1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389 3402
51. EisenMB
SpellmanPT
BrownPO
BotsteinD
1998 Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95 14863 14868
52. de LorenzoV
GiovanniniF
HerreroM
NeilandsJB
1988 Metal ion regulation of gene expression. Fur repressor-operator interaction at the promoter region of the aerobactin system of pColV-K30. J Mol Biol 203 875 884
53. JodalU
1987 The natural history of bacteriuria in childhood. Infect Dis Clin North Am 1 713 729
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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