Bottlenecks and the Maintenance of Minor Genotypes during the Life Cycle of
African trypanosomes are digenetic parasites that undergo part of their developmental cycle in mammals and part in tsetse flies. We established a novel technique to monitor the population dynamics of Trypanosoma brucei throughout its life cycle while minimising the confounding factors of strain differences or variation in fitness. Clones derived from a single trypanosome were tagged with short synthetic DNA sequences in a non-transcribed region of the genome. Infections were initiated with mixtures of tagged parasites and a combination of polymerase chain reaction and deep sequencing were used to monitor the composition of populations throughout the life cycle. This revealed that a minimum of several hundred parasites survived transmission from a tsetse fly to a mouse, or vice versa, and contributed to the infection in the new host. In contrast, the parasites experienced a pronounced bottleneck during differentiation and migration from the midgut to the salivary glands of tsetse. In two cases a single tag accounted for ≥99% of the population in the glands, although minor tags could be also detected. Minor tags were transmitted to mice together with the dominant tag(s), persisted during a chronic infection, and survived transmission to a new insect host. An important outcome of the bottleneck within the tsetse is that rare variants can be amplified in individual flies and disseminated by them. This is compatible with the epidemic population structure of T. brucei, in which clonal expansion of a few genotypes in a region occurs against a background of frequent recombination between strains.
Vyšlo v časopise:
Bottlenecks and the Maintenance of Minor Genotypes during the Life Cycle of. PLoS Pathog 6(7): e32767. doi:10.1371/journal.ppat.1001023
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1001023
Souhrn
African trypanosomes are digenetic parasites that undergo part of their developmental cycle in mammals and part in tsetse flies. We established a novel technique to monitor the population dynamics of Trypanosoma brucei throughout its life cycle while minimising the confounding factors of strain differences or variation in fitness. Clones derived from a single trypanosome were tagged with short synthetic DNA sequences in a non-transcribed region of the genome. Infections were initiated with mixtures of tagged parasites and a combination of polymerase chain reaction and deep sequencing were used to monitor the composition of populations throughout the life cycle. This revealed that a minimum of several hundred parasites survived transmission from a tsetse fly to a mouse, or vice versa, and contributed to the infection in the new host. In contrast, the parasites experienced a pronounced bottleneck during differentiation and migration from the midgut to the salivary glands of tsetse. In two cases a single tag accounted for ≥99% of the population in the glands, although minor tags could be also detected. Minor tags were transmitted to mice together with the dominant tag(s), persisted during a chronic infection, and survived transmission to a new insect host. An important outcome of the bottleneck within the tsetse is that rare variants can be amplified in individual flies and disseminated by them. This is compatible with the epidemic population structure of T. brucei, in which clonal expansion of a few genotypes in a region occurs against a background of frequent recombination between strains.
Zdroje
1. BartonN
CharlesworthB
1984 Genetic Revolutions, Founder Effects, and Speciation. Annual Review of Ecology and Systematics 15 133.164
2. RichSM
LichtMC
HudsonRR
AyalaFJ
1998 Malaria's Eve: evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc Natl Acad Sci U S A 95 4425 4430
3. MackinnonMJ
BellA
ReadAF
2005 The effects of mosquito transmission and population bottlenecking on virulence, multiplication rate and rosetting in rodent malaria. Int J Parasitol 35 145 153
4. NeiM
MaruyamaT
ChakrabortyR
1975 The bottleneck effect and genetic variability in populations. Evolution 29 1 10
5. RoditiI
LehaneMJ
2008 Interactions between trypanosomes and tsetse flies. Curr Opin Microbiol 11 345 351
6. Van Den AbbeeleJ
ClaesY
van BockstaeleD
Le RayD
CoosemansM
1999 Tryanosoma brucei spp. development in the tsetse fly: characterization of the post-mesocyclic stages in the foregut and proboscis. Parasitology 118 469 478
7. MolooSK
KabataJM
SabwaCL
1994 A study on the maturation of procyclic Trypanosoma brucei brucei in Glossina morsitans centralis and G. brevipalpis. Med Vet Entomol 8 369 374
8. SharmaR
PeacockL
GluenzE
GullK
GibsonW
2008 Asymmetric cell division as a route to reduction in cell length and change in cell morphology in trypanosomes. Protist 159 137 151
9. BruceD
HamertonAE
BatemanHR
MackieFP
1911 Further researches on the development of Trypanosoma gambiense in Glossina palpalis. Proc Roy Soc B 83 513 527
10. HarmsenR
1973 The nature of the establishment barrier for Trypanosoma brucei in the gut of Glossina pallidipes. Trans R Soc Trop Med Hyg 67 364 373
11. PeacockL
FerrisV
BaileyM
GibsonW
2007 Dynamics of infection and competition between two strains of Trypanosoma brucei brucei in the tsetse fly observed using fluorescent markers. Kinetoplastid Biol Dis 6 4
12. GibsonW
PeacockL
FerrisV
WilliamsK
BaileyM
2008 The use of yellow fluorescent hybrids to indicate mating in Trypanosoma brucei. Parasit Vectors 1 4
13. VickermanK
1985 Developmental cycles and biology of pathogenic trypanosomes. Br Med Bull 41 105 114
14. FairbairnH
BurttE
1946 The infectivity to man of a strain of Trypanosoma rhodesiense transmitted cyclically by Glossina morsitans through sheep and antelope: evidence that man requires a minimum infective dose of metacyclic trypanosomes. Annals of Tropical Medicine and Parasitology 40 270 313
15. BrunR
JenniL
1987 Human serum resistance of metacyclic forms of Trypanosoma brucei brucei, T. brucei rhodesiense and T. brucei gambiense. Parasitol Res 73 218 223
16. VickermanK
TetleyL
HendryKA
TurnerCM
1988 Biology of African trypanosomes in the tsetse fly. Biol Cell 64 109 119
17. MaudlinI
WelburnSC
1989 A single trypanosome is sufficient to infect a tsetse fly. Ann Trop Med Parasitol 83 431 433
18. ThuitaJK
KagiraJM
MwangangiD
MatovuE
TurnerCM
2008 Trypanosoma brucei rhodesiense Transmitted by a Single Tsetse Fly Bite in Vervet Monkeys as a Model of Human African Trypanosomiasis. PLoS Negl Trop Dis 2 e238
19. GingrichJB
WardRA
MackenLM
EsserKM
1981 Some phenomena associated with the development of Trypanosoma brucei rhodesiense infections in the tsetse fly, Glossina morsitans. Am J Trop Med Hyg 30 570 574
20. EbertD
1998 Experimental evolution of parasites. Science 282 1432 1435
21. RueppS
FurgerA
KurathU
RenggliCK
HemphillA
1997 Survival of Trypanosoma brucei in the tsetse fly is enhanced by the expression of specific forms of procyclin. J Cell Biol 137 1369 1379
22. VassellaE
OberleM
UrwylerS
RenggliCK
StuderE
2009 Major surface glycoproteins of insect forms of Trypanosoma brucei are not essential for cyclical transmission by tsetse. PLoS One 4 e4493
23. SimpsonEH
1949 Measurement of diversity. Nature 163 688
24. AitchesonN
TalbotS
ShapiroJ
HughesK
AdkinC
2005 VSG switching in Trypanosoma brucei: antigenic variation analysed using RNAi in the absence of immune selection. Mol Microbiol 57 1608 1622
25. MorrisonLJ
MajiwaP
ReadAF
BarryJD
2005 Probabilistic order in antigenic variation of Trypanosoma brucei. Int J Parasitol
26. LythgoeKA
MorrisonLJ
ReadAF
BarryJD
2007 Parasite-intrinsic factors can explain ordered progression of trypanosome antigenic variation. Proc Natl Acad Sci U S A 104 8095 8100
27. CapbernA
GiroudC
BaltzT
MatternP
1977 Trypanosoma equiperdum: antigenic variations in experimental trypanosomiasis of rabbits. Exp Parasitol 42 6 13
28. WoottonJC
FengX
FerdigMT
CooperRA
MuJ
2002 Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 418 320 323
29. de RoodeJC
CulletonR
BellAS
ReadAF
2004 Competitive release of drug resistance following drug treatment of mixed Plasmodium chabaudi infections. Malar J 3 33
30. MacLeodA
TweedieA
WelburnSC
MaudlinI
TurnerCM
2000 Minisatellite marker analysis of Trypanosoma brucei: reconciliation of clonal, panmictic, and epidemic population genetic structures. Proc Natl Acad Sci U S A 97 13442 13447
31. StevensJR
Mathieu DaudeF
McNamaraJJ
MizenVH
NzilaA
1994 Mixed populations of Trypanosoma brucei in wild Glossina palpalis palpalis. Trop Med Parasitol 45 313 318
32. MacLeodA
TurnerCM
TaitA
1999 A high level of mixed Trypanosoma brucei infections in tsetse flies detected by three hypervariable minisatellites. Mol Biochem Parasitol 102 237 248
33. BalmerO
CacconeA
2008 Multiple-strain infections of Trypanosoma brucei across Africa. Acta Trop 107 275 279
34. BalmerO
StearnsSC
SchotzauA
BrunR
2009 Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 90 3367 3378
35. TaitA
1980 Evidence for diploidy and mating in trypanosomes. Nature 287 536 538
36. JenniL
MartiS
SchweizerJ
BetschartB
Le PageRW
1986 Hybrid formation between African trypanosomes during cyclical transmission. Nature 322 173 175
37. Le RayD
BarryJD
EastonC
VickermanK
1977 First tsetse fly transmission of the “AnTat” serodeme of Trypanosoma brucei. Ann Soc Belg Med Trop 57 369 381
38. BrunR
SchoenenbergerM
1979 Cultivation and in vitro cloning of procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Tropica 36 289 292
39. BrunR
SchoenenbergerM
1981 Stimulating effect of citrate and cis-aconitate on the transformation of Trypanosoma brucei bloodstream forms to procyclic forms in vitro. Z Parasitenkd 66 17 24
40. VassellaE
Den AbbeeleJV
BütikoferP
RenggliCK
FurgerA
2000 A major surface glycoprotein of Trypanosoma brucei is expressed transiently during development and can be regulated post- transcriptionally by glycerol or hypoxia. Genes Dev 14 615 626
41. ThomasRK
NickersonE
SimonsJF
JannePA
TengsT
2006 Sensitive mutation detection in heterogeneous cancer specimens by massively parallel picoliter reactor sequencing. Nat Med 12 852 855
42. MarguliesM
EgholmM
AltmanWE
AttiyaS
BaderJS
2005 Genome sequencing in microfabricated high-density picolitre reactors. Nature 437 376 380
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