Mitochondrial genome of Plasmodium vivax/simium detected in an endemic region for malaria in the Atlantic Forest of Esp��rito Santo state, Brazil: do mosquitoes, simians and humans harbour the same parasite?

Julyana Cerqueira Buery, Priscila Thihara Rodrigues, L��cia Natal, La��s Camoese Salla, Ana Carolina Loss, Creuza Rachel Vicente, Helder Ricas Rezende, Ana Maria Ribeiro de Castro Duarte, Blima Fux, Rosely Dos Santos Malafronte, Alo��sio Falqueto, Crispim Cerutti
Author Information
  1. Julyana Cerqueira Buery: Tropical Medicine Unit, Federal University of Esp��rito Santo, Vit��ria, Avenida Marechal Campos, 1468-Maru��pe, Vit��ria, Esp��rito Santo, 29043-900, Brazil.
  2. Priscila Thihara Rodrigues: Department of Parasitology, University of S��o Paulo, Avenida Professor Lineu Prestes, 1374, Cidade Universit��ria, S��o Paulo, 05508-900, Brazil.
  3. L��cia Natal: Tropical Medicine Institute, University of S��o Paulo, Avenida Doutor En��as Carvalho de Aguiar, 470, Cerqueira Cesar, S��o Paulo, 05403-000, Brazil.
  4. La��s Camoese Salla: Department of Parasitology, University of S��o Paulo, Avenida Professor Lineu Prestes, 1374, Cidade Universit��ria, S��o Paulo, 05508-900, Brazil.
  5. Ana Carolina Loss: Laboratory of Mastozoology and Biogeography, Federal University of Esp��rito Santo, Avenida Fernando Ferrari, 514, Goiabeiras, Vit��ria, Esp��rito Santo, 29075-910, Brazil.
  6. Creuza Rachel Vicente: Tropical Medicine Unit, Federal University of Esp��rito Santo, Vit��ria, Avenida Marechal Campos, 1468-Maru��pe, Vit��ria, Esp��rito Santo, 29043-900, Brazil.
  7. Helder Ricas Rezende: Nucleus of Entomology and Malacology of Esp��rito Santo, Health Department of Esp��rito Santo State, Rua Pedro Zangrandi, 320, Jardim Limoeiro, Serra, Esp��rito Santo, 29164-020, Brazil.
  8. Ana Maria Ribeiro de Castro Duarte: Superintendency for the Control of Endemies (SUCEN), State Secretary of Health of S��o Paulo, Rua Paula Souza 166, Luz, S��o Paulo, 01027-000, Brazil.
  9. Blima Fux: Tropical Medicine Unit, Federal University of Esp��rito Santo, Vit��ria, Avenida Marechal Campos, 1468-Maru��pe, Vit��ria, Esp��rito Santo, 29043-900, Brazil.
  10. Rosely Dos Santos Malafronte: Tropical Medicine Institute, University of S��o Paulo, Avenida Doutor En��as Carvalho de Aguiar, 470, Cerqueira Cesar, S��o Paulo, 05403-000, Brazil.
  11. Alo��sio Falqueto: Tropical Medicine Unit, Federal University of Esp��rito Santo, Vit��ria, Avenida Marechal Campos, 1468-Maru��pe, Vit��ria, Esp��rito Santo, 29043-900, Brazil.
  12. Crispim Cerutti: Tropical Medicine Unit, Federal University of Esp��rito Santo, Vit��ria, Avenida Marechal Campos, 1468-Maru��pe, Vit��ria, Esp��rito Santo, 29043-900, Brazil. fil.cris@terra.com.br.

Abstract

BACKGROUND: The transmission of malaria in the extra-Amazonian regions of Brazil, although interrupted in the 1960s, has persisted to the present time in some areas of dense Atlantic Forest, with reports of cases characterized by particular transmission cycles and clinical presentations. Bromeliad-malaria, as it is named, is particularly frequent in the state of Esp��rito Santo, with Plasmodium vivax being the parasite commonly recognized as the aetiologic agent of human infections. With regard to the spatial and temporal distances between cases reported in this region, the transmission cycle does not fit the traditional malaria cycle. The existence of a zoonosis, with infected simians participating in the epidemiology, is therefore hypothesized. In the present study, transmission of Bromeliad-malaria in Esp��rito Santo is investigated, based on the complete mitochondrial genome of DNA extracted from isolates of Plasmodium species, which had infected humans, a simian from the genus Allouata, and Anopheles mosquitoes. Plasmodium vivax/simium was identified in the samples by both nested PCR and real-time PCR. After amplification, the mitochondrial genome was completely sequenced and compared with a haplotype network which included all sequences of P. vivax/simium mitochondrial genomes sampled from humans and simians from all regions in Brazil.
RESULTS: The haplotype network indicates that humans and simians from the Atlantic Forest become infected by the same haplotype, but some isolates from humans are not identical to the simian isolate. In addition, the plasmodial DNA extracted from mosquitoes revealed sequences different from those obtained from simians, but similar to two isolates from humans.
CONCLUSIONS: These findings strengthen support for the hypothesis that in the Atlantic Forest, and especially in the state with the highest frequency of Bromeliad-malaria in Brazil, parasites with similar molecular backgrounds are shared by humans and simians. The recognized identity between P. vivax and P. simium at the species level, the sharing of haplotypes, and the participation of the same vector in transmitting the infection to both host species indicate interspecies transference of the parasites. However, the intensity, frequency and direction of this transfer remain to be clarified.

Keywords

References

  1. Am J Trop Med Hyg. 1946 Jan;26:47-66 [PMID: 21018584]
  2. Mem Inst Oswaldo Cruz. 2006 May;101(3):229-37 [PMID: 16862314]
  3. Infect Genet Evol. 2011 Jan;11(1):209-21 [PMID: 20849978]
  4. J Med Primatol. 2011 Dec;40(6):392-400 [PMID: 21933192]
  5. PLoS Pathog. 2011 Apr;7(4):e1002015 [PMID: 21490952]
  6. Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8124-9 [PMID: 9653151]
  7. Parasitology. 2000 Jan;120 ( Pt 1):11-21 [PMID: 10726261]
  8. Mem Inst Oswaldo Cruz. 1992;87 Suppl 3:1-20 [PMID: 1343676]
  9. J Biol Chem. 1988 Apr 25;263(12):5495-8 [PMID: 3128542]
  10. Mol Biol Evol. 1999 Jan;16(1):37-48 [PMID: 10331250]
  11. Acta Trop. 2006 Nov;100(1-2):54-62 [PMID: 17126279]
  12. Expert Rev Anti Infect Ther. 2013 Jun;11(6):623-39 [PMID: 23750733]
  13. Am J Trop Med Hyg. 1989 Oct;41(4):379-85 [PMID: 2508499]
  14. Mem Inst Oswaldo Cruz. 2014 Aug;109(5):618-33 [PMID: 25185003]
  15. Trop Med Int Health. 2002 Mar;7(3):231-9 [PMID: 11903985]
  16. Am J Trop Med Hyg. 2014 Jun;90(6):1102-8 [PMID: 24639297]
  17. Acta Trop. 2008 Aug;107(2):179-85 [PMID: 18620330]
  18. Malar J. 2007 Mar 19;6:33 [PMID: 17371598]
  19. Mol Biochem Parasitol. 1993 Jan;57(1):177-80 [PMID: 8426613]
  20. Am J Trop Med Hyg. 1999 Feb;60(2):183-7 [PMID: 10072133]
  21. Rev Inst Med Trop Sao Paulo. 1969 Mar-Apr;11(2):71-86 [PMID: 4389239]
  22. J Med Entomol. 2013 May;50(3):598-602 [PMID: 23802455]
  23. Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15523-8 [PMID: 16227436]
  24. Proc Natl Acad Sci U S A. 2004 Oct 5;101(40):14455-60 [PMID: 15328406]
  25. Mem Inst Oswaldo Cruz. 1997 Mar-Apr;92(2):235-43 [PMID: 9332584]
  26. Mem Inst Oswaldo Cruz. 2018 Feb;113(2):111-118 [PMID: 29236924]
  27. Malar J. 2013 Jun 03;12:180 [PMID: 23731624]
  28. Neotrop Entomol. 2009 Mar-Apr;38(2):272-80 [PMID: 19488519]
  29. J Med Primatol. 2006 Apr;35(2):87-96 [PMID: 16556295]
  30. PLoS One. 2015 Jun 24;10(6):e0131339 [PMID: 26107662]
  31. Acta Trop. 2002 Apr;82(1):11-23 [PMID: 11904099]

MeSH Term

Alouatta
Animals
Anopheles
Brazil
Genome, Mitochondrial
Genome, Protozoan
Humans
Malaria, Vivax
Monkey Diseases
Plasmodium vivax
Real-Time Polymerase Chain Reaction

Word Cloud

Created with Highcharts 10.0.0humanssimianstransmissionAtlanticForestPlasmodiummitochondrialDNAmalariaBrazilstateEsp��ritoSantoinfectedgenomeisolatesspeciesmosquitoesvivax/simiumhaplotypePregionspresentcasesvivaxrecognizedregioncyclebromeliad-malariaextractedsimianPCRnetworksequencessimilarfrequencyparasitesBACKGROUND:extra-Amazonianalthoughinterrupted1960spersistedtimeareasdensereportscharacterizedparticularcyclesclinicalpresentationsBromeliad-malarianamedparticularlyfrequentparasitecommonlyaetiologicagenthumaninfectionsregardspatialtemporaldistancesreportedfittraditionalexistencezoonosisparticipatingepidemiologythereforehypothesizedstudyinvestigatedbasedcompletegenusAllouataAnophelesidentifiedsamplesnestedreal-timeamplificationcompletelysequencedcomparedincludedgenomessampledRESULTS:indicatesbecomeidenticalisolateadditionplasmodialrevealeddifferentobtainedtwoCONCLUSIONS:findingsstrengthensupporthypothesisespeciallyhighestmolecularbackgroundssharedidentitysimiumlevelsharinghaplotypesparticipationvectortransmittinginfectionhostindicateinterspeciestransferenceHoweverintensitydirectiontransferremainclarifiedMitochondrialdetectedendemicBrazil:harbourparasite?AnophelesEpidemiologyMalariaReal-timepolymerasechainreactionSequenceanalysesZoonoses

Similar Articles

Cited By (21)