On the Diversity of Malaria Parasites in African Apes and the Origin of from Bonobos
The origin of Plasmodium falciparum, the etiological agent of the most dangerous forms of human malaria, remains controversial. Although investigations of homologous parasites in African Apes are crucial to resolve this issue, studies have been restricted to a chimpanzee parasite related to P. falciparum, P. reichenowi, for which a single isolate was available until very recently. Using PCR amplification, we detected Plasmodium parasites in blood samples from 18 of 91 individuals of the genus Pan, including six chimpanzees (three Pan troglodytes troglodytes, three Pan t. schweinfurthii) and twelve bonobos (Pan paniscus). We obtained sequences of the parasites' mitochondrial genomes and/or from two nuclear genes from 14 samples. In addition to P. reichenowi, three other hitherto unknown lineages were found in the chimpanzees. One is related to P. vivax and two to P. falciparum that are likely to belong to distinct species. In the bonobos we found P. falciparum parasites whose mitochondrial genomes indicated that they were distinct from those present in humans, and another parasite lineage related to P. malariae. Phylogenetic analyses based on this diverse set of Plasmodium parasites in African Apes shed new light on the evolutionary history of P. falciparum. The data suggested that P. falciparum did not originate from P. reichenowi of chimpanzees (Pan troglodytes), but rather evolved in bonobos (Pan paniscus), from which it subsequently colonized humans by a host-switch. Finally, our data and that of others indicated that chimpanzees and bonobos maintain malaria parasites, to which humans are susceptible, a factor of some relevance to the renewed efforts to eradicate malaria.
Vyšlo v časopise:
On the Diversity of Malaria Parasites in African Apes and the Origin of from Bonobos. PLoS Pathog 6(2): e32767. doi:10.1371/journal.ppat.1000765
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000765
Souhrn
The origin of Plasmodium falciparum, the etiological agent of the most dangerous forms of human malaria, remains controversial. Although investigations of homologous parasites in African Apes are crucial to resolve this issue, studies have been restricted to a chimpanzee parasite related to P. falciparum, P. reichenowi, for which a single isolate was available until very recently. Using PCR amplification, we detected Plasmodium parasites in blood samples from 18 of 91 individuals of the genus Pan, including six chimpanzees (three Pan troglodytes troglodytes, three Pan t. schweinfurthii) and twelve bonobos (Pan paniscus). We obtained sequences of the parasites' mitochondrial genomes and/or from two nuclear genes from 14 samples. In addition to P. reichenowi, three other hitherto unknown lineages were found in the chimpanzees. One is related to P. vivax and two to P. falciparum that are likely to belong to distinct species. In the bonobos we found P. falciparum parasites whose mitochondrial genomes indicated that they were distinct from those present in humans, and another parasite lineage related to P. malariae. Phylogenetic analyses based on this diverse set of Plasmodium parasites in African Apes shed new light on the evolutionary history of P. falciparum. The data suggested that P. falciparum did not originate from P. reichenowi of chimpanzees (Pan troglodytes), but rather evolved in bonobos (Pan paniscus), from which it subsequently colonized humans by a host-switch. Finally, our data and that of others indicated that chimpanzees and bonobos maintain malaria parasites, to which humans are susceptible, a factor of some relevance to the renewed efforts to eradicate malaria.
Zdroje
1. EscalanteAA
AyalaFJ
1995 Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. Proc Natl Acad Sci USA 92 5793 5797
2. QariSH
ShiY-P
PieniazekNJ
CollinsWE
LalAA
1996 Phylogenetic relationship among the malaria parasites based on small subunit rRNA gene sequences: monophyletic nature of the human malaria parasite, Plasmodium falciparum. Mol Phylogenet Evol 6 157 165
3. EscalanteAA
BarrioE
AyalaFJ
1995 Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein gene. Mol Biol Evol 12 616 626
4. EscalanteAA
FreelandDE
CollinsWE
LalAA
1998 The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc Natl Acad Sci USA 95 8124 8129
5. EscalanteAA
CornejoOE
FreelandDE
PoeAC
DurregoE
2005 A monkey's tale: the origin of Plasmodium vivax as a human malaria parasite. Proc Natl Acad Sci USA 102 1980 1985
6. PerkinsSL
SchallJJ
2002 A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88 972 978
7. SnowRW
GuerraCA
NoorAM
Hla YinMint
HaySI
2005 The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434 214 217
8. ConwayDJ
FanelloC
LloydJM
Al-JouboriBMA-S
BalochAH
2000 Origin of Plasmodium falciparum malaria is traced by mitochondrial DNA. Mol Biochem Parasitol 111 163 171
9. JoyDA
FengX
MuJ
FuruyaT
ChotivanichKT
2003 Early origin and recent expansion of Plasmodium falciparum. Science 300 318 321
10. 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 USA 95 4425 4430
11. VolkmanSK
BarryAE
LyonsEJ
NielsenKM
ThomasSM
2001 Recent origin of Plasmodium falciparum from a single progenitor. Science 293 482 484
12. RichSM
LeendertzFH
XuG
LebretonM
DjokoCF
2009 The origin of malignant malaria. Proc Natl Acad Sci USA
13. CoatneyGR
CollinsWE
WarrenM
ContacosPG
1971 The primate malarias. Washington DC U.S. Government Printing Office 1 366
14. GarnhamPCC
1966 Malaria parasites and other haemosporidia. Oxford Blackwell Scientific Publications 1 1114
15. DubbeldMA
KockenCHM
ThomasAW
1998 Merozoite surface protein 2 of Plasmodium reichenowi is a unique mosaic of Plasmodium falciparum allelic forms and species-specific elements. Mol Biochem Parasitol 92 187 192
16. TanabeK
SakihamaN
HattoriT
Ranford-CartwrightLC
GoldmanIF
2004 Genetic distance in housekeeping genes between Plasmodium falciparum and Plasmodium reichenowi and within P. falciparum. J Mol Evol 59 687 694
17. OllomoB
DurandP
PrugnolleF
DouzeryE
ArnathauC
2009 A new malaria agent in African hominids. PLoS Pathog 5 e1000446 doi:10.1371/journal.ppat.1000446
18. SnounouG
SinghB
2002 Nested PCR analysis of Plasmodium parasites. Methods Mol Med 72 189 203
19. DuvalL
NerrienetE
RoussetD
Sadeuh MbaSA
HouzeS
2009 Chimpanzee malaria parasites related to Plasmodium ovale in Africa. PLoS ONE 4 e5520 doi:10.1371/journal.pone.0005520
20. RubioJM
BenitoA
RocheJ
BerzosaPJ
GarcíaML
1999 Semi-nested, multiplex polymerase chain reaction for detection of human malaria parasites and evidence of Plasmodium vivax infection in Equatorial Guinea. Am J Trop Med Hyg 60 183 187
21. RyanJR
StouteJA
AmonJ
DuntonRF
MtalibR
2006 Evidence for transmission of Plasmodium vivax among a Duffy antigen negative population in Western Kenya. Am J Trop Med Hyg 75 575 581
22. BedfordT
HartlDL
2008 Overdispersion of the molecular clock: temporal variation of gene-specific substitution rates in Drosophila. Mol Biol Evol 25 1631 1638
23. KumarS
FilipskiA
SwarnaV
WalkerA
HedgesSB
2005 Placing confidence limits on the molecular age of the human-chimpanzee divergence. Proc Natl Acad Sci USA 102 18842 18847
24. DrummondAJ
RambautA
2003 BEAST version 1.3 (http://evolve.zoo.ox.ac.uk/Evolve/Software.html)
25. MuJ
JoyDA
DuanJ
HuangY
CarltonJM-R
2005 Host switch leads to emergence of Plasmodium vivax malaria in humans. Mol Biol Evol 22 1686 1693
26. HedgesSB
KumarS
editors
2009 The timetree of life. New York Oxford University Press i-555
27. BecquetC
PattersonN
StoneAC
PrzeworskiM
ReichD
2007 Genetic structure of chimpanzee populations. PLoS Genet 3 e66 doi:10.1371/journal.pgen.0030066
28. CaswellJL
MallickS
RichterDJ
NeubauerJ
SchirmerC
2008 Analysis of chimpanzee history based on genome sequence alignments. PLoS Genet 4 e1000057 doi:10.1371/journal.pgen.1000057
29. YuN
Jensen-SeamanMI
ChemnickL
KiddJR
DeinardAS
2003 Low nucleotide diversity in chimpanzees and bonobos. Genetics 164 1511 1518
30. MobulaL
LilleyB
TshefuAK
RosenthalPJ
2009 Resistance-mediating polymorphisms in Plasmodium falciparum infections in Kinshasa, Democratic Republic of the Congo. Am J Trop Med Hyg 80 555 558
31. VerrelliBC
TishkoffSA
StoneAC
TouchmanJW
2006 Contrasting histories of G6PD molecular evolution and malarial resistance in humans and chimpanzees. Mol Biol Evol 23 1592 1601
32. SinghB
Kim SungL
MatusopA
RadhakrishnanA
ShamsulSSG
2004 A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet 363 1017 1024
33. Cox-SinghJ
DavisTME
LeeK-S
ShamsulSSG
MatusopA
2008 Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin Infect Dis 46 165 171
34. TamuraK
1992 Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol 9 678 687
35. TamuraK
DudleyJ
NeiM
KumarS
2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599
36. YangZ
2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24 1586 15891
37. PosadaD
CrandallKA
2001 Selecting the best-fit model of nucleotide substitution. Syst Biol 50 580 601
38. HuelsenbeckJP
RonquistF
2001 MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17 754 755
39. JongwutiwesS
PutaporntipC
FriedmanRM
HughesAL
2002 The extent of nucleotide polymorphism is highly variable across a 3-kb region on Plasmodium falciparum chromosome 2. Mol Biol Evol 19 1585 1590
40. DrummondAJ
HoSY
PhillipsMJ
RambautA
2006 Relaxed phylogenetics and dating with confidence. PLoS Biol 4 e88 doi:10.1371/journal.pbio.0040088
41. RambautA
DrummondAJ
2003 Tracer version 1.4 (http://beast.bio.ed.ac.uk/Tracer)
42. BandeltHJ
ForsterP
RohlA
1999 Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16 37 48
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 2
- 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
- Caspase-1 Activation via Rho GTPases: A Common Theme in Mucosal Infections?
- Kaposi's Sarcoma Associated Herpes Virus (KSHV) Induced COX-2: A Key Factor in Latency, Inflammation, Angiogenesis, Cell Survival and Invasion
- IL-1β Processing in Host Defense: Beyond the Inflammasomes
- Reverse Genetics in Predicts ARF Cycling Is Essential for Drug Resistance and Virulence