Parallel Evolution of a Type IV Secretion System in Radiating Lineages of the Host-Restricted Bacterial Pathogen
Adaptive radiation is the rapid origination of multiple species from a single ancestor as the result of concurrent adaptation to disparate environments. This fundamental evolutionary process is considered to be responsible for the genesis of a great portion of the diversity of life. Bacteria have evolved enormous biological diversity by exploiting an exceptional range of environments, yet diversification of bacteria via adaptive radiation has been documented in a few cases only and the underlying molecular mechanisms are largely unknown. Here we show a compelling example of adaptive radiation in pathogenic bacteria and reveal their genetic basis. Our evolutionary genomic analyses of the α-proteobacterial genus Bartonella uncover two parallel adaptive radiations within these host-restricted mammalian pathogens. We identify a horizontally-acquired protein secretion system, which has evolved to target specific bacterial effector proteins into host cells as the evolutionary key innovation triggering these parallel adaptive radiations. We show that the functional versatility and adaptive potential of the VirB type IV secretion system (T4SS), and thereby translocated Bartonella effector proteins (Beps), evolved in parallel in the two lineages prior to their radiations. Independent chromosomal fixation of the virB operon and consecutive rounds of lineage-specific bep gene duplications followed by their functional diversification characterize these parallel evolutionary trajectories. Whereas most Beps maintained their ancestral domain constitution, strikingly, a novel type of effector protein emerged convergently in both lineages. This resulted in similar arrays of host cell-targeted effector proteins in the two lineages of Bartonella as the basis of their independent radiation. The parallel molecular evolution of the VirB/Bep system displays a striking example of a key innovation involved in independent adaptive processes and the emergence of bacterial pathogens. Furthermore, our study highlights the remarkable evolvability of T4SSs and their effector proteins, explaining their broad application in bacterial interactions with the environment.
Vyšlo v časopise:
Parallel Evolution of a Type IV Secretion System in Radiating Lineages of the Host-Restricted Bacterial Pathogen. PLoS Genet 7(2): e32767. doi:10.1371/journal.pgen.1001296
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001296
Souhrn
Adaptive radiation is the rapid origination of multiple species from a single ancestor as the result of concurrent adaptation to disparate environments. This fundamental evolutionary process is considered to be responsible for the genesis of a great portion of the diversity of life. Bacteria have evolved enormous biological diversity by exploiting an exceptional range of environments, yet diversification of bacteria via adaptive radiation has been documented in a few cases only and the underlying molecular mechanisms are largely unknown. Here we show a compelling example of adaptive radiation in pathogenic bacteria and reveal their genetic basis. Our evolutionary genomic analyses of the α-proteobacterial genus Bartonella uncover two parallel adaptive radiations within these host-restricted mammalian pathogens. We identify a horizontally-acquired protein secretion system, which has evolved to target specific bacterial effector proteins into host cells as the evolutionary key innovation triggering these parallel adaptive radiations. We show that the functional versatility and adaptive potential of the VirB type IV secretion system (T4SS), and thereby translocated Bartonella effector proteins (Beps), evolved in parallel in the two lineages prior to their radiations. Independent chromosomal fixation of the virB operon and consecutive rounds of lineage-specific bep gene duplications followed by their functional diversification characterize these parallel evolutionary trajectories. Whereas most Beps maintained their ancestral domain constitution, strikingly, a novel type of effector protein emerged convergently in both lineages. This resulted in similar arrays of host cell-targeted effector proteins in the two lineages of Bartonella as the basis of their independent radiation. The parallel molecular evolution of the VirB/Bep system displays a striking example of a key innovation involved in independent adaptive processes and the emergence of bacterial pathogens. Furthermore, our study highlights the remarkable evolvability of T4SSs and their effector proteins, explaining their broad application in bacterial interactions with the environment.
Zdroje
1. SchluterD
2000 The ecology of adaptive radiation Oxford Oxford University Press viii, 288
2. GrantPR
GrantBR
2008 How and why species multiply : the radiation of Darwin's finches Princeton Princeton University Press xix, 218
3. SalzburgerW
2009 The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol Ecol 18 169 185
4. JohnsonZI
ZinserER
CoeA
McNultyNP
WoodwardEM
2006 Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311 1737 1740
5. RaineyPB
TravisanoM
1998 Adaptive radiation in a heterogeneous environment. Nature 394 69 72
6. SikorskiJ
NevoE
2005 Adaptation and incipient sympatric speciation of Bacillus simplex under microclimatic contrast at “Evolution Canyons” I and II, Israel. Proc Natl Acad Sci U S A 102 15924 15929
7. BrakefieldPM
RoskamJC
2006 Exploring evolutionary constraints is a task for an integrative evolutionary biology. Am Nat 168 Suppl 6 S4 13
8. DuponchelleF
ParadisE
RibbinkAJ
TurnerGF
2008 Parallel life history evolution in mouthbrooding cichlids from the African Great Lakes. Proc Natl Acad Sci U S A 105 15475 15480
9. KronforstMR
KapanDD
GilbertLE
2006 Parallel genetic architecture of parallel adaptive radiations in mimetic Heliconius butterflies. Genetics 174 535 539
10. LososJB
RicklefsRE
2009 Adaptation and diversification on islands. Nature 457 830 836
11. Harvey P.H.PMD
1991 The comparative method in evolutionary biology London/New York/Oxford Oxford University Press
12. DehioC
2005 Bartonella-host-cell interactions and vascular tumour formation. Nat Rev Microbiol 3 621 631
13. MarignacG
BarratF
ChomelB
Vayssier-TaussatM
GandoinC
2010 Murine model for Bartonella birtlesii infection: New aspects. Comp Immunol Microbiol Infect Dis 33 95 107
14. SchuleinR
SeubertA
GilleC
LanzC
HansmannY
2001 Invasion and persistent intracellular colonization of erythrocytes. A unique parasitic strategy of the emerging pathogen Bartonella. J Exp Med 193 1077 1086
15. ZhangP
ChomelBB
SchauMK
GooJS
DrozS
2004 A family of variably expressed outer-membrane proteins (Vomp) mediates adhesion and autoaggregation in Bartonella quintana. Proc Natl Acad Sci U S A 101 13630 13635
16. SaenzHL
EngelP
StoeckliMC
LanzC
RaddatzG
2007 Genomic analysis of Bartonella identifies type IV secretion systems as host adaptability factors. Nat Genet 39 1469 1476
17. SchuleinR
GuyeP
RhombergTA
SchmidMC
SchroderG
2005 A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc Natl Acad Sci U S A 102 856 861
18. SchmidMC
ScheideggerF
DehioM
Balmelle-DevauxN
SchuleinR
2006 A translocated bacterial protein protects vascular endothelial cells from apoptosis. PLoS Pathog 2 e115 doi:10.1371/journal.ppat.0020115
19. RhombergTA
TruttmannMC
GuyeP
EllnerY
DehioC
2009 A translocated protein of Bartonella henselae interferes with endocytic uptake of individual bacteria and triggers uptake of large bacterial aggregates via the invasome. Cell Microbiol 11 927 945
20. ScheideggerF
EllnerY
GuyeP
RhombergTA
WeberH
2009 Distinct activities of Bartonella henselae type IV secretion effector proteins modulate capillary-like sprout formation. Cell Microbiol 11 1088 1101
21. SelbachM
PaulFE
BrandtS
GuyeP
DaumkeO
2009 Host cell interactome of tyrosine-phosphorylated bacterial proteins. Cell Host Microbe 5 397 403
22. Vayssier-TaussatM
Le RhunD
DengHK
BivilleF
CescauS
2010 The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. PLoS Pathog 6 e1000946 doi:10.1371/journal.ppat.1000946
23. SeubertA
HiestandR
de la CruzF
DehioC
2003 A bacterial conjugation machinery recruited for pathogenesis. Mol Microbiol 49 1253 1266
24. NystedtB
FrankAC
ThollessonM
AnderssonSG
2008 Diversifying selection and concerted evolution of a type IV secretion system in Bartonella. Mol Biol Evol 25 287 300
25. YarbroughML
LiY
KinchLN
GrishinNV
BallHL
2009 AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323 269 272
26. YarbroughML
OrthK
2009 AMPylation is a new post-translational modiFICation. Nat Chem Biol 5 378 379
27. AlsmarkCM
FrankAC
KarlbergEO
LegaultBA
ArdellDH
2004 The louse-borne human pathogen Bartonella quintana is a genomic derivative of the zoonotic agent Bartonella henselae. Proc Natl Acad Sci U S A 101 9716 9721
28. BerglundEC
FrankAC
CalteauA
Vinnere PetterssonO
GranbergF
2009 Run-off replication of host-adaptability genes is associated with gene transfer agents in the genome of mouse-infecting Bartonella grahamii. PLoS Genet 5 e1000546 doi:10.1371/journal.pgen.1000546
29. EremeevaME
GernsHL
LydySL
GooJS
RyanET
2007 Bacteremia, fever, and splenomegaly caused by a newly recognized Bartonella species. N Engl J Med 356 2381 2387
30. InoueK
MaruyamaS
KabeyaH
HagiyaK
IzumiY
2009 Exotic small mammals as potential reservoirs of zoonotic Bartonella spp. Emerg Infect Dis 15 526 532
31. LinJW
ChenCY
ChenWC
ChomelBB
ChangCC
2008 Isolation of Bartonella species from rodents in Taiwan including a strain closely related to ‘Bartonella rochalimae’ from Rattus norvegicus. J Med Microbiol 57 1496 1501
32. HennJB
GabrielMW
KastenRW
BrownRN
KoehlerJE
2009 Infective endocarditis in a dog and the phylogenetic relationship of the associated “Bartonella rochalimae” strain with isolates from dogs, gray foxes, and a human. J Clin Microbiol 47 787 790
33. KordickDL
HilyardEJ
HadfieldTL
WilsonKH
SteigerwaltAG
1997 Bartonella clarridgeiae, a newly recognized zoonotic pathogen causing inoculation papules, fever, and lymphadenopathy (cat scratch disease). J Clin Microbiol 35 1813 1818
34. HellerR
ArtoisM
XemarV
De BrielD
GehinH
1997 Prevalence of Bartonella henselae and Bartonella clarridgeiae in stray cats. J Clin Microbiol 35 1327 1331
35. Kosakovsky PondSL
PosadaD
GravenorMB
WoelkCH
FrostSD
2006 GARD: a genetic algorithm for recombination detection. Bioinformatics 22 3096 3098
36. Bininda-EmondsOR
2005 Supertree construction in the genomic age. Methods Enzymol 395 745 757
37. IhlerGM
1996 Bartonella bacilliformis: dangerous pathogen slowly emerging from deep background. FEMS Microbiol Lett 144 1 11
38. ChomelBB
BoulouisHJ
BreitschwerdtEB
KastenRW
Vayssier-TaussatM
2009 Ecological fitness and strategies of adaptation of Bartonella species to their hosts and vectors. Vet Res 40 29
39. ChomelBB
HennJB
KastenRW
NietoNC
FoleyJ
2009 Dogs are more permissive than cats or guinea pigs to experimental infection with a human isolate of Bartonella rochalimae. Vet Res 40 27
40. KosoyMY
SaitoEK
GreenD
MarstonEL
JonesDC
2000 Experimental evidence of host specificity of Bartonella infection in rodents. Comp Immunol Microbiol Infect Dis 23 221 238
41. BerglundEC
EllegaardK
GranbergF
XieZ
MaruyamaS
2010 Rapid diversification by recombination in Bartonella grahamii from wild rodents in Asia contrasts with low levels of genomic divergence in Northern Europe and America. Mol Ecol 19 2241 2255
42. YangZ
NielsenR
2002 Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19 908 917
43. CarrollJA
ColemanSA
SmithermanLS
MinnickMF
2000 Hemin-binding surface protein from Bartonella quintana. Infect Immun 68 6750 6757
44. DehioC
2004 Molecular and cellular basis of Bartonella pathogenesis. Annu Rev Microbiol 58 365 390
45. MinnickMF
SappingtonKN
SmithermanLS
AnderssonSG
KarlbergO
2003 Five-member gene family of Bartonella quintana. Infect Immun 71 814 821
46. McCannHC
GuttmanDS
2008 Evolution of the type III secretion system and its effectors in plant-microbe interactions. New Phytol 177 33 47
47. MaW
DongFF
StavrinidesJ
GuttmanDS
2006 Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLoS Genet 2 e209 doi:10.1371/journal.pgen.0020209
48. FrankAC
AlsmarkCM
ThollessonM
AnderssonSG
2005 Functional divergence and horizontal transfer of type IV secretion systems. Mol Biol Evol 22 1325 1336
49. OguraY
OokaT
IguchiA
TohH
AsadulghaniM
2009 Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli. Proc Natl Acad Sci U S A 106 17939 17944
50. SandegrenL
AnderssonDI
2009 Bacterial gene amplification: implications for the evolution of antibiotic resistance. Nat Rev Microbiol 7 578 588
51. KinchLN
YarbroughML
OrthK
GrishinNV
2009 Fido, a novel AMPylation domain common to fic, doc, and AvrB. PLoS ONE 4 e5818 doi:10.1371/journal.pone.0005818
52. BlomN
GammeltoftS
BrunakS
1999 Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294 1351 1362
53. HuangHD
LeeTY
TzengSW
HorngJT
2005 KinasePhos: a web tool for identifying protein kinase-specific phosphorylation sites. Nucleic Acids Res 33 W226 229
54. ObenauerJC
CantleyLC
YaffeMB
2003 Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31 3635 3641
55. DehioC
LanzC
PohlR
BehrensP
BermondD
2001 Bartonella schoenbuchii sp. nov., isolated from the blood of wild roe deer. Int J Syst Evol Microbiol 51 1557 1565
56. MarguliesM
EgholmM
AltmanWE
AttiyaS
BaderJS
2005 Genome sequencing in microfabricated high-density picolitre reactors. Nature 437 376 380
57. BocsS
CruveillerS
VallenetD
NuelG
MedigueC
2003 AMIGene: Annotation of MIcrobial Genes. Nucleic Acids Res 31 3723 3726
58. VallenetD
LabarreL
RouyZ
BarbeV
BocsS
2006 MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res 34 53 65
59. ThompsonJD
HigginsDG
GibsonTJ
1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 4673 4680
60. TamuraK
DudleyJ
NeiM
KumarS
2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599
61. WilgenbuschJC
SwoffordD
2003 Inferring evolutionary trees with PAUP*. Curr Protoc Bioinformatics Chapter 6 Unit 6.4.1 6.4.28
62. HuelsenbeckJP
RonquistF
2001 MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17 754 755
63. PosadaD
2003 Using MODELTEST and PAUP* to select a model of nucleotide substitution. Curr Protoc Bioinformatics Chapter 6 Unit 6.5.1 6.5.14
64. NylanderJAA
2004 MrModeltest v2 Program distributed by the author
65. YangZ
2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24 1586 1591
66. PondSL
FrostSD
MuseSV
2005 HyPhy: hypothesis testing using phylogenies. Bioinformatics 21 676 679
67. EngelP
DehioC
2009 Genomics of Host-Restricted Pathogens of the Genus Bartonella. Genome Dyn 6 158 169
68. ArvandM
RaoultD
FeilEJ
2010 Multi-locus sequence typing of a geographically and temporally diverse sample of the highly clonal human pathogen Bartonella quintana. PLoS ONE 5 e9765 doi:10.1371/journal.pone.0009765
69. BaiY
KosoyMY
CullyJF
BalaT
RayC
2007 Acquisition of nonspecific Bartonella strains by the northern grasshopper mouse (Onychomys leucogaster). FEMS Microbiol Ecol 61 438 448
70. BaiY
KosoyMY
LerdthusneeK
PeruskiLF
RichardsonJH
2009 Prevalence and genetic heterogeneity of Bartonella strains cultured from rodents from 17 provinces in Thailand. Am J Trop Med Hyg 81 811 816
71. BemisDA
KaniaSA
2007 Isolation of Bartonella sp. from sheep blood. Emerg Infect Dis 13 1565 1567
72. BerglundEC
EhrenborgC
Vinnere PetterssonO
GranbergF
NaslundK
2010 Genome dynamics of Bartonella grahamii in micro-populations of woodland rodents. BMC Genomics 11 152
73. BermondD
BoulouisHJ
HellerR
Van LaereG
MonteilH
2002 Bartonella bovis Bermond et al. sp. nov. and Bartonella capreoli sp. nov., isolated from European ruminants. Int J Syst Evol Microbiol 52 383 390
74. BermondD
HellerR
BarratF
DelacourG
DehioC
2000 Bartonella birtlesii sp. nov., isolated from small mammals (Apodemus spp.). Int J Syst Evol Microbiol 50 1973 1979
75. BirtlesRJ
HarrisonTG
SaundersNA
MolyneuxDH
1995 Proposals to unify the genera Grahamella and Bartonella, with descriptions of Bartonella talpae comb. nov., Bartonella peromysci comb. nov., and three new species, Bartonella grahamii sp. nov., Bartonella taylorii sp. nov., and Bartonella doshiae sp. nov. Int J Syst Bacteriol 45 1 8
76. BirtlesRJ
HazelSM
BennettM
BownK
RaoultD
2001 Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiol Infect 126 323 329
77. BirtlesRJ
RaoultD
1996 Comparison of partial citrate synthase gene (gltA) sequences for phylogenetic analysis of Bartonella species. Int J Syst Bacteriol 46 891 897
78. CelebiB
CarhanA
KilicS
BaburC
2010 Detection and Genetic Diversity of Bartonella vinsonii Subsp. berkhoffii Strains Isolated from Dogs in Ankara, Turkey. J Vet Med Sci 72 969 73
79. ChamberlinJ
LaughlinLW
RomeroS
SolorzanoN
GordonS
2002 Epidemiology of endemic Bartonella bacilliformis: a prospective cohort study in a Peruvian mountain valley community. J Infect Dis 186 983 990
80. ChangCC
ChomelBB
KastenRW
HellerRM
UenoH
2000 Bartonella spp. isolated from wild and domestic ruminants in North America. Emerg Infect Dis 6 306 311
81. ClarridgeJE3rd
RaichTJ
PirwaniD
SimonB
TsaiL
1995 Strategy to detect and identify Bartonella species in routine clinical laboratory yields Bartonella henselae from human immunodeficiency virus-positive patient and unique Bartonella strain from his cat. J Clin Microbiol 33 2107 2113
82. DillonB
ValenzuelaJ
DonR
BlanckenbergD
WigneyDI
2002 Limited diversity among human isolates of Bartonella henselae. J Clin Microbiol 40 4691 4699
83. EllisBA
RegneryRL
BeatiL
BacellarF
RoodM
1999 Rats of the genus Rattus are reservoir hosts for pathogenic Bartonella species: an Old World origin for a New World disease? J Infect Dis 180 220 224
84. GundiVA
DavoustB
KhamisA
BoniM
RaoultD
2004 Isolation of Bartonella rattimassiliensis sp. nov. and Bartonella phoceensis sp. nov. from European Rattus norvegicus. J Clin Microbiol 42 3816 3818
85. GurfieldAN
BoulouisHJ
ChomelBB
KastenRW
HellerR
2001 Epidemiology of Bartonella infection in domestic cats in France. Vet Microbiol 80 185 198
86. HarrusS
Bar-GalGK
GolanA
Elazari-VolcaniR
KosoyMY
2009 Isolation and genetic characterization of a Bartonella strain closely related to Bartonella tribocorum and Bartonella elizabethae in Israeli commensal rats. Am J Trop Med Hyg 81 55 58
87. HellerR
RiegelP
HansmannY
DelacourG
BermondD
1998 Bartonella tribocorum sp. nov., a new Bartonella species isolated from the blood of wild rats. Int J Syst Bacteriol 48 Pt 4 1333 1339
88. HennJB
ChomelBB
BoulouisHJ
KastenRW
MurrayWJ
2009 Bartonella rochalimae in raccoons, coyotes, and red foxes. Emerg Infect Dis 15 1984 1987
89. HofmeisterEK
KolbertCP
AbdulkarimAS
MageraJM
HopkinsMK
1998 Cosegregation of a novel Bartonella species with Borrelia burgdorferi and Babesia microti in Peromyscus leucopus. J Infect Dis 177 409 416
90. HolmbergM
MillsJN
McGillS
BenjaminG
EllisBA
2003 Bartonella infection in sylvatic small mammals of central Sweden. Epidemiol Infect 130 149 157
91. InoueK
KabeyaH
KosoyMY
BaiY
SmirnovG
2009 Evolutional and geographical relationships of Bartonella grahamii isolates from wild rodents by multi-locus sequencing analysis. Microb Ecol 57 534 541
92. InoueK
MaruyamaS
KabeyaH
YamadaN
OhashiN
2008 Prevalence and genetic diversity of Bartonella species isolated from wild rodents in Japan. Appl Environ Microbiol 74 5086 5092
93. JardineC
AppleyardG
KosoyMY
McCollD
Chirino-TrejoM
2005 Rodent-associated Bartonella in Saskatchewan, Canada. Vector Borne Zoonotic Dis 5 402 409
94. KosoyM
MurrayM
GilmoreRDJr
BaiY
GageKL
2003 Bartonella strains from ground squirrels are identical to Bartonella washoensis isolated from a human patient. J Clin Microbiol 41 645 650
95. KosoyMY
RegneryRL
TzianabosT
MarstonEL
JonesDC
1997 Distribution, diversity, and host specificity of Bartonella in rodents from the Southeastern United States. Am J Trop Med Hyg 57 578 588
96. LiDM
MengFX
SongXP
QinZJ
YangXR
2006 [Study on Bartonella vinsonii berkhoffii isolated from blood of native dogs in China]. Zhonghua Liu Xing Bing Xue Za Zhi 27 333 338
97. LydySL
EremeevaME
AsnisD
PaddockCD
NicholsonWL
2008 Isolation and characterization of Bartonella bacilliformis from an expatriate Ecuadorian. J Clin Microbiol 46 627 637
98. MaillardR
RiegelP
BarratF
BouillinC
ThibaultD
2004 Bartonella chomelii sp. nov., isolated from French domestic cattle (Bos taurus). Int J Syst Evol Microbiol 54 215 220
99. MarquezFJ
2010 Molecular Detection of Bartonella alsatica in European Wild Rabbits (Oryctolagus cuniculus) in Andalusia (Spain). Vector Borne Zoonotic Dis 10 731 4
100. MarstonEL
FinkelB
RegneryRL
WinotoIL
GrahamRR
1999 Prevalence of Bartonella henselae and Bartonella clarridgeiae in an urban Indonesian cat population. Clin Diagn Lab Immunol 6 41 44
101. PretoriusAM
BeatiL
BirtlesRJ
2004 Diversity of bartonellae associated with small mammals inhabiting Free State province, South Africa. Int J Syst Evol Microbiol 54 1959 1967
102. RolainJM
FournierPE
RaoultD
BonerandiJJ
2003 First isolation and detection by immunofluorescence assay of Bartonella koehlerae in erythrocytes from a French cat. J Clin Microbiol 41 4001 4002
103. TeaA
Alexiou-DanielS
PapoutsiA
PapaA
AntoniadisA
2004 Bartonella species isolated from rodents, Greece. Emerg Infect Dis 10 963 964
104. YingB
KosoyMY
MaupinGO
TsuchiyaKR
GageKL
2002 Genetic and ecologic characteristics of Bartonella communities in rodents in southern China. Am J Trop Med Hyg 66 622 627
105. ZeaiterZ
FournierPE
OgataH
RaoultD
2002 Phylogenetic classification of Bartonella species by comparing groEL sequences. Int J Syst Evol Microbiol 52 165 171
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 2
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na 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