A Timescale for Evolution, Population Expansion, and Spatial Spread of an Emerging Clone of Methicillin-Resistant
Due to the lack of fossil evidence, the timescales of bacterial evolution are largely unknown. The speed with which genetic change accumulates in populations of pathogenic bacteria, however, is a key parameter that is crucial for understanding the emergence of traits such as increased virulence or antibiotic resistance, together with the forces driving pathogen spread. Methicillin-resistant Staphylococcus aureus (MRSA) is a common cause of hospital-acquired infections. We have investigated an MRSA strain (ST225) that is highly prevalent in hospitals in Central Europe. By using mutation discovery at 269 genetic loci (118,804 basepairs) within an international isolate collection, we ascertained extremely low diversity among European ST225 isolates, indicating that a recent population bottleneck had preceded the expansion of this clone. In contrast, US isolates were more divergent, suggesting they represent the ancestral population. While diversity was low, however, our results demonstrate that the short-term evolutionary rate in this natural population of MRSA resulted in the accumulation of measurable DNA sequence variation within two decades, which we could exploit to reconstruct its recent demographic history and the spatiotemporal dynamics of spread. By applying Bayesian coalescent methods on DNA sequences serially sampled through time, we estimated that ST225 had diverged since approximately 1990 (1987 to 1994), and that expansion of the European clade began in 1995 (1991 to 1999), several years before the new clone was recognized. Demographic analysis based on DNA sequence variation indicated a sharp increase of bacterial population size from 2001 to 2004, which is concordant with the reported prevalence of this strain in several European countries. A detailed ancestry-based reconstruction of the spatiotemporal dispersal dynamics suggested a pattern of frequent transmission of the ST225 clone among hospitals within Central Europe. In addition, comparative genomics indicated complex bacteriophage dynamics.
Vyšlo v časopise:
A Timescale for Evolution, Population Expansion, and Spatial Spread of an Emerging Clone of Methicillin-Resistant. PLoS Pathog 6(4): e32767. doi:10.1371/journal.ppat.1000855
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000855
Souhrn
Due to the lack of fossil evidence, the timescales of bacterial evolution are largely unknown. The speed with which genetic change accumulates in populations of pathogenic bacteria, however, is a key parameter that is crucial for understanding the emergence of traits such as increased virulence or antibiotic resistance, together with the forces driving pathogen spread. Methicillin-resistant Staphylococcus aureus (MRSA) is a common cause of hospital-acquired infections. We have investigated an MRSA strain (ST225) that is highly prevalent in hospitals in Central Europe. By using mutation discovery at 269 genetic loci (118,804 basepairs) within an international isolate collection, we ascertained extremely low diversity among European ST225 isolates, indicating that a recent population bottleneck had preceded the expansion of this clone. In contrast, US isolates were more divergent, suggesting they represent the ancestral population. While diversity was low, however, our results demonstrate that the short-term evolutionary rate in this natural population of MRSA resulted in the accumulation of measurable DNA sequence variation within two decades, which we could exploit to reconstruct its recent demographic history and the spatiotemporal dynamics of spread. By applying Bayesian coalescent methods on DNA sequences serially sampled through time, we estimated that ST225 had diverged since approximately 1990 (1987 to 1994), and that expansion of the European clade began in 1995 (1991 to 1999), several years before the new clone was recognized. Demographic analysis based on DNA sequence variation indicated a sharp increase of bacterial population size from 2001 to 2004, which is concordant with the reported prevalence of this strain in several European countries. A detailed ancestry-based reconstruction of the spatiotemporal dispersal dynamics suggested a pattern of frequent transmission of the ST225 clone among hospitals within Central Europe. In addition, comparative genomics indicated complex bacteriophage dynamics.
Zdroje
1. AchtmanM
WagnerM
2008 Microbial diversity and the genetic nature of microbial species. Nature Reviews Microbiology 6 431 440
2. Pérez-LosadaM
CrandallKA
ZenilmanJ
ViscidiRP
2007 Temporal trends in gonococcal population genetics in a high prevalence urban community. Infect Genet Evol 7 271 278
3. WilsonDJ
GabrielE
LeatherbarrowAJ
CheesbroughJ
GeeS
2009 Rapid evolution and the importance of recombination to the gastroenteric pathogen Campylobacter jejuni. Mol Biol Evol 26 385 397
4. FalushD
KraftC
TaylorNS
CorreaP
FoxJG
2001 Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc Natl Acad Sci U S A 98 15056 15061
5. GilbertMT
RambautA
WlasiukG
SpiraTJ
PitchenikAE
2007 The emergence of HIV/AIDS in the Americas and beyond. Proc Natl Acad Sci U S A 104 18566 18570
6. KleinE
SmithDL
LaxminarayanR
2007 Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999–2005. Emerg Infect Dis 13 1840 1846
7. WilliamsREO
1959 Epidemic staphylococci. Lancet 1 190 195
8. EnrightMC
RobinsonDA
RandleG
FeilEJ
GrundmannH
2002 The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A 99 7687 7692
9. HiramatsuK
CuiL
KurodaM
ItoT
2001 The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 9 486 493
10. CrisóstomoMI
WesthH
TomaszA
ChungM
OliveiraDC
2001 The evolution of methicillin resistance in Staphylococcus aureus: similarity of genetic backgrounds in historically early methicillin-susceptible and -resistant isolates and contemporary epidemic clones. Proc Natl Acad Sci U S A 98 9865 9870
11. NübelU
RoumagnacP
FeldkampM
SongJH
KoKS
2008 Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 105 14130 14135
12. ShuklaSK
StemperME
RamaswamySV
ConradtJM
ReichR
2004 Molecular characteristics of nosocomial and Native American community-associated methicillin-resistant Staphylococcus aureus clones from rural Wisconsin. J Clin Microbiol 42 3752 3757
13. MelterO
Aires de SousaM
UrbaskovaP
JakubuV
ZemlickovaH
2003 Update on the major clonal types of methicillin-resistant Staphylococcus aureus in the Czech Republic. J Clin Microbiol 41 4998 5005
14. WitteW
KlareI
NübelU
StrommengerB
WernerG
2008 Emergence and spread of antibiotic resistant Gram positive bacterial pathogens. International Journal of Medical Microbiology 298 365 377
15. JohnsonAP
PearsonA
DuckworthG
2005 Surveillance and epidemiology of MRSA bacteraemia in the UK. J Antimicrob Chemother 56 455 462
16. DauwalderO
LinaG
DurandG
BesM
MeugnierH
2008 Epidemiology of invasive methicillin-resistant Staphylococcus aureus clones collected in France in 2006 and 2007. J Clin Microbiol 46 3454 3458
17. ConceicaoM
Aires de SousaM
FüziM
TóthÁ
PásztiJ
2007 Replacement of methicilln-resistant Staphylococcus aureus clones in Hungary over time: a 10-year surveillance study. Clin Microbiol Infect 13 971 979
18. DeurenbergRH
VinkC
OudhuisGJ
MooijJE
DriessenC
2005 Different clonal complexes of methicillin-resistant Staphylococcus aureus are disseminated in the Euregio Meuse-Rhine regions. Antimicrob Agents Chemother 49 4263 4271
19. BartelsMD
BoyeK
LarsenAR
SkovR
WesthH
2007 Rapid increase of genetically diverse methicillin-resistant Staphylococcus aureus, Copenhagen, Denmark. Emerg Infect Dis 13 1533 1540
20. QiW
EnderM
O'BrienF
ImhofA
RuefC
2005 Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Zürich, Switzerland (2003): prevalence of type IV SCCmec and a new SCCmec element associated with isolates from intravenous drug users. J Clin Microbiol 43 5164 5170
21. FariaNA
OliveiraDC
WesthH
MonnetDL
LarsenAR
2005 Epidemiology of emerging methicillin-resistant Staphylococcus aureus (MRSA) in Denmark: a nationwide survey in a country with low prevalence of MRSA infection. J Clin Microbiol 43 1836 1842
22. HanssenAM
FossumA
MikalsenJ
HalvorsenDS
BukholmG
2005 Dissemination of communiy-acquired methicillin-resistant Staphylococcus aureus clones in northern Norway: sequence types 8 and 80 predeominate. J Clin Microbiol 43 2118 2124
23. KennedyAD
OttoM
BraughtonKR
WhitneyAR
ChenL
2008 Epidemic community-associated methicillin-resistant Staphylococcus aureus: recent clonal expansion and diversification. Proc Natl Acad Sci U S A 105 1327 1332
24. RochaEP
SmithJM
HurstLD
HoldenMT
CooperJE
2006 Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol 239 226 235
25. KryazhimskiyS
PlotkinJB
2008 The population genetics of dN/dS. PLoS Genetics 4 e1000304 doi:10.1371/journal.pgen.1000304
26. GoeringRV
MorrisonD
Al-DooriZ
EdwardsGFS
GemmellCG
2008 Usefulness of mec-associated direct repeat unit (dru) typing in the epidemiolological analysis of highly clonal methicillin-resistant Staphylococcus aureus in Scotland. Clin Microbiol Infect 14 964 969
27. OliveiraDC
WuSW
De LencastreH
2000 Genetic organization of the downstream region of the mecA element in methicillin-resistant Staphylococcus aureus isolates carrying different polymorphisms of this region. Antimicrob Agents Chemother 44 1906 1910
28. MwangiMM
WuSW
ZhouY
SieradzkiK
de LencastreH
2007 Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc Natl Acad Sci U S A 104 9451 9456
29. KatayamaY
ItoT
HiramatsuK
2000 A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 44 1549 1555
30. NotoMJ
FoxPM
ArcherGL
2008 Spontaneous deletion of the methicillin resistance determinant, mecA, partially compensates for the fitness cost associated with high-level vancomycin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 52 1221 1229
31. StrommengerB
BraulkeC
HeuckD
SchmidtC
PasemannB
2008 Spa-typing of Staphylococcus aureus as a frontline tool in epidemiological typing. J Clin Microbiol 46 574 581
32. DrummondAJ
PybusOG
RambautA
ForsbergR
RodrigoAG
2003 Measurably evolving populations. Trends Ecol Evol 18 481
33. DrummondAJ
HoSYW
PhillipsMJ
RambautA
2006 Relaxed phylogenetics and dating with confidence. PLoS Biol 4 e88 doi:10.1371/journal.pbio.0040088
34. LowderB
GuinaneCM
Ben ZakourNL
WeinertL
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
35. GuttmanDS
DykhuizenDE
1994 Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266 1380 1383
36. O'NeillAJ
CoveJH
ChopraI
2001 Mutation frequencies for resistance to fusidic acid and rifampicin in Staphylococcus aureus. J Antimicrob Chemother 47 647 650
37. Al MamunAAM
2007 Elevated expression of DNA polymerase II increases spontaneous mutagenesis in Escherichia coli. Mutat Res 625 29 39
38. O'NeillAJ
ChopraI
2002 Insertional inactivation of mutS in Staphylococcus aureus reveals potential for elevated mutation frequencies, although the prevalence of mutators in clinical isolates is low. J Antimicrob Chemother 50 161 169
39. HorstJ-P
WuT
MarinusMG
1999 Escherichia coli mutator genes. Trends Microbiol 7 29 36
40. HahnMW
RausherMD
CunninghamCW
2002 Distinguishing between selection and population expansion in an experimental lineage of bacteriophage T7. Genetics 161 11 20
41. HoSYW
PhillipsMJ
CooperA
DrummondAJ
2005 Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22 1561 1568
42. AchtmanM
ZurthK
MorelliG
TorreaG
GuiyouleA
1999 Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proceedings of the National Academy of Sciences of the United States of America 96 14043 14048
43. ZhangW
QiW
AlbertTJ
MotiwalaAS
AllandD
2006 Probing genomic diversity and evolution of Escherichia coli O157 by single nucleotide polymorphisms. Genome Res 16 757 767
44. HolmesEC
2008 Evolutionary history and phylogeography of human viruses. Annu Rev Microbiol 62 307 328
45. JombartT
EggoRM
DoddPJ
BallouxF
2009 Spatiotemporal dynamics in the early stages of the 2009 A/H1N1 influenza pandemic. PLoS Curr Influenza: RRN1026. Available: http://knol.google.com/k/thibaut-jombart/spatiotemporal-dynamics-in-the-early/11igg07td5uji/1
46. AlbrichWC
HarbarthS
2008 Health-care workers: source, vector, or victim of MRSA? The Lancet 8 289 301
47. WitteW
StrommengerB
CunyC
HeuckD
NübelU
2007 Methicillin-resistant Staphylococcus aureus containing the Panton-Valentine leukocidin gene in Germany in 2005 and 2006. J Antimicrob Chemother 60 1258 1263
48. BootsmaMCJ
DiekmannO
BontenMJM
2006 Controlling methicillin-resistant Staphylococcus aureus: quantifying the effects of interventions and rapid diagnostic testing. Proc Natl Acad Sci U S A 103 5620 5625
49. KurodaM
OhtaT
UchiyamaI
BabaT
YuzawaH
2001 Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357 1225 1240
50. Truong-BolducQC
HooperDC
2007 The transcriptional regulators NorG and MgrA modulate resistance to both quinolones and β-lactams in Staphylococcus aureus. J Bacteriol 189 2996 3005
51. BaeT
BabaT
HiramatsuK
SchneewindO
2006 Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol Microbiol 62 1035 1047
52. MoxonER
JansenVA
2005 Phage variation: understanding the behaviour of an accidental pathogen. Trends Microbiol 13 563 565
53. MaidenMC
2008 Population genomics: diversity and virulence in the Neisseria. Current Opinion in Microbiology 11 467 471
54. ParkhillJ
2008 Time to remove the model organism blinkers. Trends Microbiol 16 510 511
55. KurtK
AlderbornA
NilssonM
StrommengerB
WitteW
2009 Multiplexed genotyping of methicillin-resistant Staphylococcus aureus isolates by use of padlock probes and tag microarrays. J Clin Microbiol 47 577 585
56. BakerS
HoltK
van de VosseE
RoumagnacP
WhiteheadS
2008 High-throughput genotyping of Salmonella Typhi allows geographical assignment of haplotypes and pathotypes within an urban district of Jakarta, Indonesia. J Clin Microbiol
57. KeimP
Van ErtMN
PearsonT
VoglerAJ
HuynhLY
2004 Anthrax molecular epidemiology and forensics: using the appropriate marker for different evolutionary scales. Infect Genet Evol 4 205 213
58. Anonymous 2004 DIN 58940. Medical microbiology – susceptibility testing of pathogens to antimicrobial agents. Part 8 – microdilution. DIN-Taschenbuch 222: medizinische Mikrobiologie und Immunologie – diagnostische Verfahren Berlin, Germany Deutsches Institut für Normung, Beuth-Verlag
59. AzizRK
BartelsD
BestAA
DeJonghM
DiszT
2008 The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9 75
60. RutherfordK
ParkhillJ
CrookJ
HorsnellT
RiceP
2000 Artemis: sequence visualization and annotation. Bioinformatics 16 944 945
61. FelsensteinJ
1981 Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17 368 376
62. DrummondAJ
RambautA
2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7 214
63. R Development Core Team 2009 R: a language and environment for statistical computing Vienna, Austria R Foundation for Statistical Computing
64. ParadisE
ClaudeJ
StrimmerK
2004 APE: Analysis of phylogenetics and evolution in R language. Bioinformatics 20 289 290
65. JombartT
2008 adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24 1403 1405
66. GastmeierP
GeffersC
2008 [Nosocomial infections in Germany. What are the numbers, based on the estimates for 2006?]. Dtsch Med Wochenschr 133 1111 1115
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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