A Genomic Survey of Positive Selection in Provides Insights into the Evolution of Accidental Virulence
Certain environmental microorganisms can cause severe human infections, even in the absence of an obvious requirement for transition through an animal host for replication (“accidental virulence”). To understand this process, we compared eleven isolate genomes of Burkholderia pseudomallei (Bp), a tropical soil microbe and causative agent of the human and animal disease melioidosis. We found evidence for the existence of several new genes in the Bp reference genome, identifying 282 novel genes supported by at least two independent lines of supporting evidence (mRNA transcripts, database homologs, and presence of ribosomal binding sites) and 81 novel genes supported by all three lines. Within the Bp core genome, 211 genes exhibited significant levels of positive selection (4.5%), distributed across many cellular pathways including carbohydrate and secondary metabolism. Functional experiments revealed that certain positively selected genes might enhance mammalian virulence by interacting with host cellular pathways or utilizing host nutrients. Evolutionary modifications improving Bp environmental fitness may thus have indirectly facilitated the ability of Bp to colonize and survive in mammalian hosts. These findings improve our understanding of the pathogenesis of melioidosis, and establish Bp as a model system for studying the genetics of accidental virulence.
Vyšlo v časopise:
A Genomic Survey of Positive Selection in Provides Insights into the Evolution of Accidental Virulence. PLoS Pathog 6(4): e32767. doi:10.1371/journal.ppat.1000845
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000845
Souhrn
Certain environmental microorganisms can cause severe human infections, even in the absence of an obvious requirement for transition through an animal host for replication (“accidental virulence”). To understand this process, we compared eleven isolate genomes of Burkholderia pseudomallei (Bp), a tropical soil microbe and causative agent of the human and animal disease melioidosis. We found evidence for the existence of several new genes in the Bp reference genome, identifying 282 novel genes supported by at least two independent lines of supporting evidence (mRNA transcripts, database homologs, and presence of ribosomal binding sites) and 81 novel genes supported by all three lines. Within the Bp core genome, 211 genes exhibited significant levels of positive selection (4.5%), distributed across many cellular pathways including carbohydrate and secondary metabolism. Functional experiments revealed that certain positively selected genes might enhance mammalian virulence by interacting with host cellular pathways or utilizing host nutrients. Evolutionary modifications improving Bp environmental fitness may thus have indirectly facilitated the ability of Bp to colonize and survive in mammalian hosts. These findings improve our understanding of the pathogenesis of melioidosis, and establish Bp as a model system for studying the genetics of accidental virulence.
Zdroje
1. HoldenMT
TitballRW
PeacockSJ
Cerdeno-TarragaAM
AtkinsT
2004 Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci U S A 101 14240 14245
2. WiersingaWJ
van der PollT
WhiteNJ
DayNP
PeacockSJ
2006 Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 4 272 282
3. CurrieBJ
2008 Advances and remaining uncertainties in the epidemiology of Burkholderia pseudomallei and melioidosis. Trans R Soc Trop Med Hyg 102 225 227
4. CasadevallA
PirofskiLA
2007 Accidental virulence, cryptic pathogenesis, martians, lost hosts, and the pathogenicity of environmental microbes. Eukaryot Cell 6 2169 2174
5. U'Ren JM
HornstraH
PearsonT
SchuppJM
LeademB
2007 Fine-scale genetic diversity among Burkholderia pseudomallei soil isolates in northeast Thailand. Appl Environ Microbiol 73 6678 6681
6. TumapaS
Burkholderia pseudomallei genome plasticity associated with genomic island variation. BMC Genomics 9 190 (2008)
7. SimSH
YuY
LinCH
KaruturiRK
WuthiekanunV
2008 The core and accessory genomes of Burkholderia pseudomallei: implications for human melioidosis. PLoS Pathog 4 e1000178 doi:10.1371/journal.ppat.1000178
8. InglisTJ
RobertsonT
WoodsDE
DuttonN
ChangBJ
2003 Flagellum-mediated adhesion by Burkholderia pseudomallei precedes invasion of Acanthamoeba astronyxis. Infect Immun 71 2280 2282
9. GanYH
ChuaKL
ChuaHH
LiuB
HiiCS
2002 Characterization of Burkholderia pseudomallei infection and identification of novel virulence factors using a Caenorhabditis elegans host system. Mol Microbiol 44 1185 1197
10. UlettGC
CurrieBJ
ClairTW
MayoM
KetheesanN
2001 Burkholderia pseudomallei virulence: definition, stability and association with clonality. Microbes Infect 3 621 631
11. FrigaardNU
MartinezA
MincerTJ
DeLongEF
2006 Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439 847 850
12. BensonG
1999 Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27 573 580
13. SiguierP
PerochonJ
LestradeL
MahillonJ
ChandlerM
2006 ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34 D32 36
14. MavromatisK
IvanovaN
BarryK
ShapiroH
GoltsmanE
2007 Use of simulated data sets to evaluate the fidelity of metagenomic processing methods. Nat Methods 4 495 500
15. ZhuH
HuGQ
YangYF
WangJ
SheZS
2007 MED: a new non-supervised gene prediction algorithm for bacterial and archaeal genomes. BMC Bioinformatics 8 97
16. BertoneP
StolcV
RoyceTE
RozowskyJS
UrbanAE
2004 Global identification of human transcribed sequences with genome tiling arrays. Science 306 2242 2246
17. GardnerPP
DaubJ
TateJG
NawrockiEP
KolbeDL
2009 Rfam: updates to the RNA families database. Nucleic Acids Res 37 D136 140
18. LoftusB
AndersonI
DaviesR
AlsmarkUC
SamuelsonJ
2005 The genome of the protist parasite Entamoeba histolytica. Nature 433 865 868
19. KalmanS
MitchellW
MaratheR
LammelC
FanJ
1999 Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat Genet 21 385 389
20. LoweTM
EddySR
1997 tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25 955 964
21. LarkinMA
BlackshieldsG
BrownNP
ChennaR
McGettiganPA
2007 Clustal W and Clustal X version 2.0. Bioinformatics 23 2947 2948
22. SuzekBE
ErmolaevaMD
SchreiberM
SalzbergSL
2001 A probabilistic method for identifying start codons in bacterial genomes. Bioinformatics 17 1123 1130
23. SmithMG
GianoulisTA
PukatzkiS
MekalanosJJ
OrnstonLN
2007 New insights into Acinetobacter baumannii pathogenesis revealed by high-density pyrosequencing and transposon mutagenesis. Genes Dev 21 601 614
24. DelcherAL
BratkeKA
PowersEC
SalzbergSL
2007 Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23 673 679
25. WooPC
LeungPK
TsoiHW
YuenKY
2001 Cloning and characterisation of malE in Burkholderia pseudomallei. J Med Microbiol 50 330 338
26. WinstanleyC
HalesBA
HartCA
1999 Evidence for the presence in Burkholderia pseudomallei of a type III secretion system-associated gene cluster. J Med Microbiol 48 649 656
27. KyteJ
DoolittleRF
1982 A simple method for displaying the hydropathic character of a protein. J Mol Biol 157 105 132
28. KrauseL
McHardyAC
NattkemperTW
PuhlerA
StoyeJ
2007 GISMO–gene identification using a support vector machine for ORF classification. Nucleic Acids Res 35 540 549
29. SerresMH
GopalS
NahumLA
LiangP
GaasterlandT
2001 A functional update of the Escherichia coli K-12 genome. Genome Biol 2 RESEARCH0035
30. LefebureT
StanhopeMJ
2007 Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition. Genome Biol 8 R71
31. 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
32. NiermanWC
DeShazerD
KimHS
TettelinH
NelsonKE
2004 Structural flexibility in the Burkholderia mallei genome. Proc Natl Acad Sci U S A 101 14246 14251
33. KimHS
SchellMA
YuY
UlrichRL
SarriaSH
2005 Bacterial genome adaptation to niches: divergence of the potential virulence genes in three Burkholderia species of different survival strategies. BMC Genomics 6 174
34. YuY
KimHS
ChuaHH
LinCH
SimSH
2006 Genomic patterns of pathogen evolution revealed by comparison of Burkholderia pseudomallei, the causative agent of melioidosis, to avirulent Burkholderia thailandensis. BMC Microbiol 6 46
35. PearsonT
GiffardP
Beckstrom-SternbergS
AuerbachR
HornstraH
2009 Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer. BMC Biol 7 78
36. TuanyokA
AuerbachRK
BrettinTS
BruceDC
MunkAC
2007 A horizontal gene transfer event defines two distinct groups within Burkholderia pseudomallei that have dissimilar geographic distributions. J Bacteriol 189 9044 9049
37. ChenSL
HungCS
XuJ
ReigstadCS
MagriniV
2006 Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc Natl Acad Sci U S A 103 5977 5982
38. AnisimovaM
BielawskiJP
YangZ
2001 Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol 18 1585 1592
39. YangZ
2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24 1586 1591
40. KorberB
2000 HIV Signature and Sequence Variation Analysis. Dordrecht, Netherlands Kluwer Academic Publishers 55 72 Computational Analysis of HIV Molecular Sequences, Chapter 4 Allen G. Rodrigo and Gerald H. Learn, eds
41. SawyerS
1989 Statistical tests for detecting gene conversion. Mol Biol Evol 6 526 538
42. BruenTC
PhilippeH
BryantD
2006 A simple and robust statistical test for detecting the presence of recombination. Genetics 172 2665 2681
43. DidelotX
FalushD
2007 Inference of bacterial microevolution using multilocus sequence data. Genetics 175 1251 1266
44. CraigL
PiqueME
TainerJA
2004 Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2 363 378
45. Essex-LoprestiAE
BoddeyJA
ThomasR
SmithMP
HartleyMG
2005 A type IV pilin, PilA, Contributes To Adherence of Burkholderia pseudomallei and virulence in vivo. Infect Immun 73 1260 1264
46. LiuB
KooGC
YapEH
ChuaKL
GanYH
2002 Model of differential susceptibility to mucosal Burkholderia pseudomallei infection. Infect Immun 70 504 511
47. AktoriesK
BarbieriJT
2005 Bacterial cytotoxins: targeting eukaryotic switches. Nat Rev Microbiol 3 397 410
48. HallA
1998 Rho GTPases and the actin cytoskeleton. Science 279 509 514
49. StevensMP
FriebelA
TaylorLA
WoodMW
BrownPJ
2003 A Burkholderia pseudomallei type III secreted protein, BopE, facilitates bacterial invasion of epithelial cells and exhibits guanine nucleotide exchange factor activity. J Bacteriol 185 4992 4996
50. De BuckE
LammertynE
AnneJ
2008 The importance of the twin-arginine translocation pathway for bacterial virulence. Trends Microbiol 16 442 453
51. HuxtableRJ
1992 Physiological actions of taurine. Physiol Rev 72 101 163
52. SaitouN
NeiM
1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 406 425
53. PerriereG
GouyM
1996 WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78 364 369
54. EichhornE
van der PloegJR
KerteszMA
LeisingerT
1997 Characterization of alpha-ketoglutarate-dependent taurine dioxygenase from Escherichia coli. J Biol Chem 272 23031 23036
55. van der PloegJR
WeissMA
SallerE
NashimotoH
SaitoN
1996 Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source. J Bacteriol 178 5438 5446
56. ChuaKL
ChanYY
GanYH
2003 Flagella are virulence determinants of Burkholderia pseudomallei. Infect Immun 71 1622 1629
57. TuanyokA
KimHS
NiermanWC
YuY
DunbarJ
2005 Genome-wide expression analysis of iron regulation in Burkholderia pseudomallei and Burkholderia mallei using DNA microarrays. FEMS Microbiol Lett 252 327 335
58. BrownSA
PalmerKL
WhiteleyM
2008 Revisiting the host as a growth medium. Nat Rev Microbiol 6 657 666
59. SpragueLD
NeubauerH
2004 Melioidosis in animals: a review on epizootiology, diagnosis and clinical presentation. J Vet Med B Infect Dis Vet Public Health 51 305 320
60. PeacockSJ
SchweizerHP
DanceDA
SmithTL
GeeJE
2008 Management of accidental laboratory exposure to Burkholderia pseudomallei and B. mallei. Emerg Infect Dis 14 e2
61. DarlingAE
TreangenTJ
MesseguerX
PernaNT
2007 Analyzing patterns of microbial evolution using the mauve genome alignment system. Methods Mol Biol 396 135 152
62. ChenF
MackeyAJ
StoeckertCJJr
RoosDS
2006 OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res 34 D363 368
63. AltschulSF
GishW
MillerW
MyersEW
LipmanDJ
1990 Basic local alignment search tool. J Mol Biol 215 403 410
64. SuyamaM
TorrentsD
BorkP
2006 PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34 W609 612
65. WongWS
YangZ
GoldmanN
NielsenR
2004 Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168 1041 1051
66. BoddeyJA
FleggCP
DayCJ
BeachamIR
PeakIR
2006 Temperature-regulated microcolony formation by Burkholderia pseudomallei requires pilA and enhances association with cultured human cells. Infect Immun 74 5374 5381
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 4
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- The Effect of Vaccination on the Evolution and Population Dynamics of Avian Paramyxovirus-1
- Reconstitution of SARS-Coronavirus mRNA Cap Methylation
- Deficiencies in Jasmonate-Mediated Plant Defense Reveal Quantitative Variation in Pathogenesis
- A Timescale for Evolution, Population Expansion, and Spatial Spread of an Emerging Clone of Methicillin-Resistant