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Plasmodium Falciparum-Like Parasites Infecting Wild Apes in Southern Cameroon Do Not Represent a Recurrent Source of Human Malaria

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Plasmodium Falciparum-Like Parasites Infecting Wild Apes in Southern Cameroon Do Not Represent a Recurrent Source of Human Malaria Plasmodium falciparum-like parasites infecting wild apes in southern Cameroon do not represent a recurrent source of human malaria Sesh A. Sundararamana,b, Weimin Liua, Brandon F. Keelec, Gerald H. Learna, Kyle Bittingerb, Fatima Mouachad, Steve Ahuka-Mundeked, Magnus Manskee, Scott Sherrill-Mixb, Yingying Lia, Jordan A. Malenkea, Eric Delaported, Christian Laurentd, Eitel Mpoudi Ngolef, Dominic P. Kwiatkowskie, George M. Shawa,b, Julian C. Raynere, Martine Peetersd, Paul M. Sharpg, Frederic D. Bushmanb, and Beatrice H. Hahna,b,1 Departments of aMedicine and bMicrobiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104; cThe AIDS and Cancer Virus Program, Science Applications International Corporation–Frederick, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD 21702; dUnité Mixte Internationale 233, Institut de Recherche pour le Développement and University of Montpellier 1, 34394 Montpellier, France; eSanger Institute Malaria Programme, The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; fCentre de Recherches pour les Maladies Emergents et Ré-émergents and Institut de Recherches Médicales et d’Etudes des Plantes Médicinales, BP 906, Yaoundé, Cameroon; and gInstitute of Evolutionary Biology and Centre for Immunity, Infection and Evolution, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom Contributed by Beatrice H. Hahn, March 18, 2013 (sent for review February 3, 2013) Wild-living chimpanzees and gorillas harbor a multitude of Plas- closely related to human P. falciparum and placed into a separate modium species, including six of the subgenus Laverania, one of Plasmodium subgenus, termed Laverania (4, 7, 9, 10). Of these six which served as the progenitor of Plasmodium falciparum. Despite Laverania species, Plasmodium reichenowi, Plasmodium gaboni, the magnitude of this reservoir, it is unknown whether apes rep- and Plasmodium billcollinsi were identified only in chimpanzees, resent a source of human infections. Here, we used Plasmodium whereas Plasmodium adleri, Plasmodium blacklocki,andPlasmo- species-specific PCR, single-genome amplification, and 454 se- dium praefalciparum were only found in gorillas. Moreover, quencing to screen humans from remote areas of southern Came- P. praefalciparum was shown to be the immediate precursor of roon for ape Laverania infections. Among 1,402 blood samples, we human P. falciparum (4). Because candidate Anopheles vectors MICROBIOLOGY found 1,000 to be Plasmodium mitochondrial DNA (mtDNA) posi- have been identified that may transmit both ape and human par- tive, all of which contained human parasites as determined by asites (11), the fact that a large fraction of wild-living apes is en- sequencing and/or restriction enzyme digestion. To exclude low- demically Plasmodium infected has raised concerns that they might abundance infections, we subjected 514 of these samples to 454 represent a source of recurring human infections (4, 5, 9, 12, 13). sequencing, targeting a region of the mtDNA genome that distin- In this study, we tested humans who live in remote rural areas Laverania of southern Cameroon for ape Plasmodium zoonoses. We spe- guishes ape from human species. Using algorithms spe- fi cifically developed to differentiate rare Plasmodium variants from ci cally screened for Laverania infections, because these are the 454-sequencing error, we identified single and mixed-species infec- most abundant and widespread in resident ape populations, and tions with P. falciparum, Plasmodium malariae, and/or Plasmodium because one of them, P. praefalciparum, has crossed the species ovale. However, none of the human samples contained ape Laver- barrier from gorillas to humans already once (4). Moreover, ape ania parasites, including the gorilla precursor of P. falciparum.To Laverania parasites have been studied extensively at the molec- ular level, with numerous mitochondrial, apicoplast, and nuclear characterize further the diversity of P. falciparum in Cameroon, sequences available for analyses. To detect zoonotic infections, we used single-genome amplification to amplify 3.4-kb mtDNA we (i) developed a Plasmodium species-specific diagnostic PCR, fragments from 229 infected humans. Phylogenetic analysis (ii) used ultra-deep sequencing to search for low-abundance ape identified 62 new variants, all of which clustered with extant parasites in mixed Plasmodium species infections, and (iii) used P. falciparum, providing further evidence that P. falciparum emerged single-genome amplification (SGA) to characterize the genetic following a single gorilla-to-human transmission. Thus, unlike Plas- modium knowlesi diversity of human P. falciparum in southern Cameroon. Our -infected macaques in southeast Asia, African apes study systematically searched for Plasmodium zoonoses in west harboring Laverania parasites do not seem to serve as a recurrent fi central Africa, thus providing insight into the host range of hu- source of human malaria, a nding of import to ongoing control and man and great ape parasites. eradication measures. Results diagnostic Laverania PCR | great apes | nextgen sequencing | Genetic Analysis of Human Plasmodium Infections in Rural Cameroon. Plasmodium coinfections | Plasmodium diversity Cameroon is an area of high malaria endemicity, with nearly 100% of clinical cases believed to be caused by P. falciparum (1). alaria is one of the most devastating infectious diseases of Mhumans worldwide, with hundreds of millions of cases of clinical illness and over 650,000 deaths occurring annually (1). Author contributions: S.A.S., W.L., F.D.B., and B.H.H. designed the study; S.A.S., W.L., G.H.L., Given this enormous health burden, efforts to control and poten- K.B., F.M., S.A.-M., Y.L., and J.A.M. performed research; K.B., M.M., S.S.-M., E.D., C.L., E.M.N., tially eradicate this disease have become an urgent public health D.P.K., and J.C.R. contributed new reagents/analytic tools; S.A.S., W.L., B.F.K., G.H.L., K.B., priority (2, 3). Effective control and elimination measures require F.M., S.A.-M., Y.L., and J.A.M. analyzed data; and S.A.S., W.L., G.M.S., J.C.R., M.P., P.M.S., F.D.B., and B.H.H. wrote the paper. a clear understanding of parasite, vector, human, and environ- fl mental factors that sustain malaria transmission. This includes a The authors declare no con ict of interest. systematic evaluation of potential zoonotic reservoirs and the risk Data deposition: All newly derived Plasmodium sequences have been deposited in the GenBank database (accession nos. KC175306–KC175322 and KC203521–KC203587). The that they may pose for humans. Recently, close genetic relatives of 454 pyrosequencing read data have been deposited in the National Center for Biotech- the human malaria parasites Plasmodium falciparum, Plasmodium nology Information Sequence Read Archive (SRA), www.ncbi.nlm.nih.gov/sra (accession ovale, Plasmodium malariae,andPlasmodium vivax have been no. SRP019191). identified in wild-living apes in sub-Saharan Africa (4–8). These 1To whom correspondence should be addressed. E-mail: [email protected]. fi parasites were tentatively classi ed on the basis of their sequence This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. relationships into a number of different species, six of which were 1073/pnas.1305201110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1305201110 PNAS Early Edition | 1of6 Downloaded by guest on September 30, 2021 However, few of these infections have been molecularly char- acterized and the extent of parasite diversity, both at the in- S N V traspecies and interspecies level, is largely unknown. Studying 1 0 3.3 kb the epidemiology and natural history of HIV type 1 (HIV-1) 0 SG 0 A 5 infections in Cameroon, we previously collected large numbers 1 0 C 0 of buffy coat samples, which represent thin layers of leukocytes O 0 X I I on the surface of sedimented erythrocytes (14). These samples I also contain Plasmodium DNA, because parasite-infected red blood cells concentrate immediately below the buffy coat layer Plasmodium mtDNA and are thus harvested together with the leukocytes (15). To 5967 bp characterize the Plasmodium species that commonly infect humans in rural Cameroon, we selected samples from 318 c y 4 C t b inhabitants of seven remote villages (Fig. 1 and SI Appendix, 0 Y 0 T B 0 x Table S1). These study sites were chosen because of the high a v B GA vi s b S . 0 Laverania prevalence rates in chimpanzee and gorilla pop- r 3.4 k P 0 l 0 2 ulations in adjacent forest regions (Fig. 1A). All sampled indi- 45 S 4 N viduals lived in close proximity to ape habitats (Fig. 1B) and V I 4 COX SN included forest dwellers, hunters, members of local pygmy tribes, V3 SN and individuals who worked at logging concessions. Because V2 3000 many of these subjects spent numerous hours and days in the forest, we reasoned that at least some of them were exposed to Fig. 2. Schematic representation of the Plasmodium mitochondrial ge- ape Plasmodium-infected Anopheles mosquitoes. To examine nome. DNA fragments amplified for diagnostic purposes (cytb, BsrI, P. vivax), whether such exposures had resulted in parasite transmission, we 454 sequencing (454), and SGA (mtDNA-3.3 kb; mtDNA-3.4 kb) are shown in screened buffy coat DNA for ape parasites by diagnostic PCR. relation to cytochrome b (cytb), cytochrome c oxidase subunit I (coxI), and cytochrome c oxidase subunit III (coxIII) coding regions, respectively. The Using primers previously shown to amplify ape Laverania para- – fi positions of four SNVs (SNV1 SNV4), which distinguish human P. falciparum sites with high sensitivity and speci city (4), we targeted a 939-bp from ape Laverania parasites, are shown in red. region spanning most of the cytochrome b (cytb) gene of the Plasmodium mitochondrial DNA (mtDNA) genome (Fig. 2). fi This analysis identi ed 194 of the 318 blood samples to be PCR Table S1). From this experiment, we concluded that zoonotic positive (61%), all of which contained human parasites as de- Laverania infections, if they indeed occurred, were rare and un- termined by direct sequencing: 181 samples contained P.
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