Microevolution of during Prolonged Infection of Single Hosts and within Families
Our understanding of basic evolutionary processes in bacteria is still very limited. For example, multiple recent dating estimates are based on a universal inter-species molecular clock rate, but that rate was calibrated using estimates of geological dates that are no longer accepted. We therefore estimated the short-term rates of mutation and recombination in Helicobacter pylori by sequencing an average of 39,300 bp in 78 gene fragments from 97 isolates. These isolates included 34 pairs of sequential samples, which were sampled at intervals of 0.25 to 10.2 years. They also included single isolates from 29 individuals (average age: 45 years) from 10 families. The accumulation of sequence diversity increased with time of separation in a clock-like manner in the sequential isolates. We used Approximate Bayesian Computation to estimate the rates of mutation, recombination, mean length of recombination tracts, and average diversity in those tracts. The estimates indicate that the short-term mutation rate is 1.4×10−6 (serial isolates) to 4.5×10−6 (family isolates) per nucleotide per year and that three times as many substitutions are introduced by recombination as by mutation. The long-term mutation rate over millennia is 5–17-fold lower, partly due to the removal of non-synonymous mutations due to purifying selection. Comparisons with the recent literature show that short-term mutation rates vary dramatically in different bacterial species and can span a range of several orders of magnitude.
Vyšlo v časopise:
Microevolution of during Prolonged Infection of Single Hosts and within Families. PLoS Genet 6(7): e32767. doi:10.1371/journal.pgen.1001036
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001036
Souhrn
Our understanding of basic evolutionary processes in bacteria is still very limited. For example, multiple recent dating estimates are based on a universal inter-species molecular clock rate, but that rate was calibrated using estimates of geological dates that are no longer accepted. We therefore estimated the short-term rates of mutation and recombination in Helicobacter pylori by sequencing an average of 39,300 bp in 78 gene fragments from 97 isolates. These isolates included 34 pairs of sequential samples, which were sampled at intervals of 0.25 to 10.2 years. They also included single isolates from 29 individuals (average age: 45 years) from 10 families. The accumulation of sequence diversity increased with time of separation in a clock-like manner in the sequential isolates. We used Approximate Bayesian Computation to estimate the rates of mutation, recombination, mean length of recombination tracts, and average diversity in those tracts. The estimates indicate that the short-term mutation rate is 1.4×10−6 (serial isolates) to 4.5×10−6 (family isolates) per nucleotide per year and that three times as many substitutions are introduced by recombination as by mutation. The long-term mutation rate over millennia is 5–17-fold lower, partly due to the removal of non-synonymous mutations due to purifying selection. Comparisons with the recent literature show that short-term mutation rates vary dramatically in different bacterial species and can span a range of several orders of magnitude.
Zdroje
1. AchtmanM
MorelliG
ZhuP
WirthT
DiehlI
2004 Microevolution and history of the plague bacillus, Yersinia pestis. Proc Natl Acad Sci (USA) 101 17837 17842
2. RoumagnacP
WeillF-X
DolecekC
BakerS
BrisseS
2006 Evolutionary history of Salmonella Typhi. Science 314 1301 1304
3. NübelU
RoumagnacP
FeldkampM
SongJH
KoKS
2008 Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci (USA) 105 14130 14135
4. SreevatsanS
PanX
StockbauerK
ConnellND
KreiswirthBN
1997 Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci (U S A) 94 9869 9874
5. PupoGM
LanR
ReevesPR
2000 Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics. Proc Natl Acad Sci (U S A) 97 10567 10572
6. LeopoldSR
MagriniV
HoltNJ
ShaikhN
MardisER
2009 A precise reconstruction of the emergence and constrained radiations of Escherichia coli O157 portrayed by backbone concatenomic analysis. Proc Natl Acad Sci (USA) 106 8713 8718
7. ParkhillJ
SebaihiaM
PrestonA
MurphyLD
ThomsonN
2003 Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nature Genet 35 32 40
8. WirthT
MorelliG
KusecekB
Van BelkumA
van der ScheeC
2007 The rise and spread of a new pathogen: seroresistant Moraxella catarrhalis. Genome Research 17 1647 1656
9. HolmesEC
2008 Evolutionary history and phylogeography of human viruses. Annu Rev Microbiol 62 307 328
10. OchmanH
WilsonAC
1987 Evolution in bacteria: Evidence for a universal substitution rate in cellular genomes. J Mol Evol 26 74 86
11. SheridanPP
FreemanKH
BrenchleyJE
2003 Estimated minimal divergence times of the major bacterial and archaeal phyla. Geomicrobiology Journal 20 1 14
12. WirthT
FalushD
LanR
CollesF
MensaP
2006 Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60 1136 1151
13. BattistuzziFU
FeijaoA
HedgesSB
2004 A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol Biol 4 44
14. HoSY
LarsonG
2006 Molecular clocks: when times are a-changin'. Trends Genet 22 79 83
15. HoSY
ShapiroB
PhillipsMJ
CooperA
DrummondAJ
2007 Evidence for time dependency of molecular rate estimates. Syst Biol 56 515 522
16. RochaEP
SmithJM
HurstLD
HoldenMT
CooperJE
2006 Comparisons of dN/dS are time dependent for closely related bacterial genomes. J theor Biol 239 226 235
17. KryazhimskiyS
PlotkinJB
2008 The population genetics of dN/dS. PLoS Genet 4 e1000304 doi:10.1371/journal.pgen.1000304
18. OchmanH
ElwynS
MoranNA
1999 Calibrating bacterial evolution. Proc Natl Acad Sci (U S A) 96 12638 12643
19. AchtmanM
2008 Evolution, population structure and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol 62 53 70
20. 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
21. FengL
ReevesPR
LanR
RenY
GaoC
2008 A recalibrated molecular clock and independent origins for the cholera pandemic clones. PLoS ONE 3 e4053 doi:10.1371/journal.pone.0004053
22. HarrisSR
FeilEJ
HoldenMT
QuailMA
NickersonEK
2010 Evolution of MRSA during hospital transmission and intercontinental spread. Science 327 469 474
23. MenaA
SmithEE
BurnsJL
SpeertDP
MoskowitzSM
2008 Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J Bacteriol 190 7910 7917
24. SmithEE
BuckleyDG
WuZ
SaenphimmachakC
HoffmanLR
2006 Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci (USA) 103 8487 8492
25. 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 (USA) 104 9451 9456
26. WeissmanSJ
BeskhlebnayaV
ChesnokovaV
ChattopadhyayS
StammWE
2007 Differential stability and trade-off effects of pathoadaptive mutations in the Escherichia coli FimH adhesin. Infect Immun 75 3548 3555
27. ChattopadhyayS
WeissmanSJ
MininVN
RussoTA
DykhuizenDE
2009 High frequency of hotspot mutations in core genes of Escherichia coli due to short-term positive selection. Proc Natl Acad Sci (USA) 106 12412 12417
28. SuerbaumS
JosenhansC
2007 Helicobacter pylori evolution and phenotypic diversification in a changing host. Nat Rev Microbiol 5 441 452
29. MoodleyY
LinzB
YamaokaY
WindsorHM
BreurecS
2009 The peopling of the Pacific from a bacterial perspective. Science 323 527 530
30. LinzB
BallouxF
MoodleyY
ManicaA
LiuH
2007 An African origin for the intimate association between humans and Helicobacter pylori. Nature 445 915 918
31. 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 doi:10.1371/journal.pgen.0020120
32. WirthT
WangX
LinzB
NovickRP
LumJK
2004 Distinguishing human ethnic groups by means of sequences from Helicobacter pylori: lessons from Ladakh. Proc Natl Acad Sci (USA) 101 4746 4751
33. FalushD
WirthT
LinzB
PritchardJK
StephensM
2003 Traces of human migrations in Helicobacter pylori populations. Science 299 1582 1585
34. AchtmanM
AzumaT
BergDE
ItoY
MorelliG
1999 Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol Microbiol 32 459 470
35. BjorkholmB
SjolundM
FalkPG
BergOG
EngstrandL
2001 Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc Natl Acad Sci (USA) 98 14607 14612
36. KangJM
IovineNM
BlaserMJ
2006 A paradigm for direct stress-induced mutation in prokaryotes. FASEB J 20 2476 2485
37. LinZ
NeiM
MaH
2007 The origins and early evolution of DNA mismatch repair genes–multiple horizontal gene transfers and co-evolution. Nucleic Acids Res 35 7591 7603
38. KangJ
BlaserMJ
2006 Bacterial populations as perfect gases: genomic integrity and diversification tensions in Helicobacter pylori. Nat Rev Microbiol 4 826 836
39. SuerbaumS
Maynard SmithJ
BapumiaK
MorelliG
SmithNH
1998 Free recombination within Helicobacter pylori. Proc Natl Acad Sci (U S A) 95 12619 12624
40. MeinersmannRJ
Romero-GalloJ
BlaserMJ
2008 Rate heterogeneity in the evolution of Helicobacter pylori and the behavior of homoplastic sites. Infect Genet Evol 8 593 602
41. KulickS
MocciaC
DidelotX
FalushD
KraftC
2008 Mosaic DNA imports with interspersions of recipient sequence after natural transformation of Helicobacter pylori. PLoS ONE 3 e3797 doi:10.1371/journal.pone.0003797
42. LinEA
ZhangXS
LevineSM
GillSR
FalushD
2009 Natural transformation of Helicobacter pylori involves the integration of short DNA fragments interrupted by gaps of variable size. PLoS Pathog 5 e1000337 doi:10.1371/journal.ppat.1000337
43. TaylorNS
FoxJG
AkopyantsNS
BergDE
ThompsonN
1995 Long-term colonization with single and multiple strains of Helicobacter pylori assessed by DNA fingerprinting. J Clin Microbiol 33 918 923
44. BergDE
GilmanRH
Lelwala-GurugeJ
SrivastavaK
ValdezY
1997 Helicobacter pylori populations in Peruvian patients. Clin Infect Dis 25 996 1002
45. KersulyteD
ChalkauskasH
BergDE
1999 Emergence of recombinant strains of Helicobacter pylori during human infection. Mol Microbiol 31 31 43
46. RaymondJ
ThibergJM
ChevalierC
KalachN
BergeretM
2004 Genetic and transmission analysis of Helicobacter pylori strains within a family. Emerg Infect Dis 10 1816 1821
47. SchwarzS
MorelliG
KusecekB
ManicaA
BallouxF
2008 Horizontal versus familial transmission of Helicobacter pylori. PLoS Pathog 4 e1000180 doi:10.1371/journal.ppat.1000180
48. TalaricoS
GoldBD
FeroJ
ThompsonDT
GuarnerJ
2009 Pediatric Helicobacter pylori isolates display distinct gene coding capacities and virulence gene marker profiles. J Clin Microbiol 47 1680 1688
49. 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
50. KuipersEJ
IsraelDA
KustersJG
GerritsMM
WeelJ
2000 Quasispecies development of Helicobacter pylori observed in paired isolates obtained years apart from the same host. J Infect Dis 181 273 282
51. DidelotX
FalushD
2007 Inference of bacterial microevolution using multilocus sequence data. Genetics 175 1251 1266
52. BeaumontMA
ZhangWY
BaldingDJ
2002 Approximate Bayesian computation in population genetics. Genetics 162 2025 2035
53. PritchardJK
SeielstadMT
Perez-LezaunA
FeldmanMW
1999 Population growth of human Y chromosomes: a study of Y chromosome microsatellites. Mol Biol Evol 16 1791 1798
54. TavareS
MarshallCR
WillO
SoligoC
MartinRD
2002 Using the fossil record to estimate the age of the last common ancestor of extant primates. Nature 416 726 729
55. VoightBF
AdamsAM
FrisseLA
QianY
HudsonRR
2005 Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc Natl Acad Sci (USA) 102 18508 18513
56. MarjoramP
MolitorJ
PlagnolV
TavareS
2003 Markov chain Monte Carlo without likelihoods. Proc Natl Acad Sci (USA) 100 15324 15328
57. GelmanA
MengXL
SternH
1996 Posterior predictive assessment of model fitness via realized discrepancies. Statistica Sinica 6 733 760
58. IngvarssonPK
2008 Multilocus patterns of nucleotide polymorphism and the demographic history of Populus tremula. Genetics 180 329 340
59. ThorntonK
AndolfattoP
2006 Approximate Bayesian inference reveals evidence for a recent, severe bottleneck in a Netherlands population of Drosophila melanogaster. Genetics 172 1607 1619
60. HolmesEC
2010 The comparative genomics of viral emergence. Proc Natl Acad Sci (USA) 107 Supplement 1 1742 1746
61. JolleyKA
ChanMS
MaidenMC
2004 mlstdbNet - distributed multi-locus sequence typing (MLST) databases. BMC Bioinformatics 5 86
62. PetersonGI
MaselJ
2009 Quantitative prediction of molecular clock and Ka/Ks at short timescales. Mol Biol Evol 26 2595 2603
63. TombJF
WhiteO
KerlavageAR
ClaytonRA
SuttonGG
1997 The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388 539 547
64. TomitaniA
KnollAH
CavanaughCM
OhnoT
2006 The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives. Proc Natl Acad Sci (USA) 103 5442 5447
65. ButterfieldNJ
2000 Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26 386 404
66. HollandHD
2002 Volcanic gases, black smokers, and the Great Oxidation Event. Geochimica et Cosmochimica Acta 66 3811 3826
67. JavauxEJ
KnollAH
WalterMR
2001 Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412 66 69
68. Date-a-Clade service for the molecular tree of life 2009 Age of crown Bilateria. http://www.fossilrecord.net/dateaclade/clade_crown_Bilateria.html
69. Date-a-Clade service for the molecular tree of life 2009 Age of mammals. http://www.fossilrecord.net/dateaclade/clade-platypus-elephant.html
70. Tree of Life web project 2009 Age of legumes. http://tolweb.org/Fabaceae/21093
71. MoranNA
McLaughlinHJ
SorekR
2009 The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323 379 382
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