The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host switching

Tobias Mourier; Denise Anete Madureira de Alvarenga; Abhinav Kaushik; Anielle de Pina-Costa; Olga Douvropoulou; Qingtian Guan; Francisco J. Guzmán-Vega; Sarah Forrester; Filipe Vieira Santos de Abreu; Cesare Bianco Júnior; Julio Cesar de Souza Junior; Silvia Bahadian Moreira; Zelinda Maria Braga Hirano; Alcides Pissinatti; Maria de Fátima Ferreira-da-Cruz; Ricardo Lourenço de Oliveira; Stefan T. Arold; Daniel C. Jeffares; Patrícia Brasil; Cristiana Ferreira Alves de Brito; Richard Culleton; Cláudio Tadeu Daniel-Ribeiro; Arnab Pain

doi:10.1186/s12915-021-01139-5

The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host switching

Tobias Mourier, Denise Anete Madureira de Alvarenga, Abhinav Kaushik, Anielle de Pina-Costa, Olga Douvropoulou, Qingtian Guan, Francisco J. Guzmán-Vega, Sarah Forrester, Filipe Vieira Santos de Abreu, Cesare Bianco Júnior, Julio Cesar de Souza Junior, Silvia Bahadian Moreira, Zelinda Maria Braga Hirano, Alcides Pissinatti, Maria de Fátima Ferreira-da-Cruz, Ricardo Lourenço de Oliveira, Stefan T. Arold, Daniel C. Jeffares, Patrícia Brasil, Cristiana Ferreira Alves de BritoRichard Culleton, Cláudio Tadeu Daniel-Ribeiro, Arnab Pain

Research output: Contribution to journal › Article › peer-review

20 Scopus citations

Abstract

Abstract Background Plasmodium simium, a malaria parasite of non-human primates (NHP), was recently shown to cause zoonotic infections in humans in Brazil. We sequenced the P. simium genome to investigate its evolutionary history and to identify any genetic adaptions that may underlie the ability of this parasite to switch between host species. Results Phylogenetic analyses based on whole genome sequences of P. simium from humans and NHPs reveals that P. simium is monophyletic within the broader diversity of South American Plasmodium vivax, suggesting P. simium first infected NHPs as a result of a host switch of P. vivax from humans. The P. simium isolates show the closest relationship to Mexican P. vivax isolates. Analysis of erythrocyte invasion genes reveals differences between P. vivax and P. simium, including large deletions in the Duffy-binding protein 1 (DBP1) and reticulocyte-binding protein 2a genes of P. simium. Analysis of P. simium isolated from NHPs and humans revealed a deletion of 38 amino acids in DBP1 present in all human-derived isolates, whereas NHP isolates were multi-allelic. Conclusions Analysis of the P. simium genome confirmed a close phylogenetic relationship between P. simium and P. vivax, and suggests a very recent American origin for P. simium. The presence of the DBP1 deletion in all human-derived isolates tested suggests that this deletion, in combination with other genetic changes in P. simium, may facilitate the invasion of human red blood cells and may explain, at least in part, the basis of the recent zoonotic infections.

Original language	English (US)
Journal	BMC Biology
Volume	19
Issue number	1
DOIs	https://doi.org/10.1186/s12915-021-01139-5
State	Published - Oct 1 2021

Bibliographical note

KAUST Repository Item: Exported on 2021-10-04
Acknowledged KAUST grant number(s): BAS/1/1056-01-01, BRF1020/01/01, OSR, URF/1/1976-25
Acknowledgements: The work was supported financially by the King Abdullah University of Science and Technology (KAUST) through the baseline fund BRF1020/01/01 to AP and BAS/1/1056-01-01 to STA, and the Award No. URF/1/1976-25 from the Office of Sponsored Research (OSR). The field work in the Atlantic Forest and laboratory analysis in Brazil received financial support from the Secretary for Health Surveillance of the Ministry of Health through the Global Fund (agreement IOC-005-Fio-13), Programa Nacional de Excelência (PRONEX) and contract 407873/2018-0 of the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Fapemig CBB-APQ-02620-15) and the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (Faperj), Brazil. CNPq supports CFAB, CTDR, MFFC, PB and RLO, with a research productivity fellowship. CTDR (CNE: E-26/202.921/2018), MFFC, PB and RLO are also supported by Faperj as Cientistas do nosso estado. AdP-C was supported by a postdoctoral fellowship from the Faperj and DAMA by a fellowship from the CGZV-SVS (Brazilian Ministry of Health) TED 49/2018 grant. SF was supported by a Wellcome Seed Award in Science to DCJ (208965/Z/17/Z).

ASJC Scopus subject areas

General Agricultural and Biological Sciences
General Biochemistry, Genetics and Molecular Biology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1186/s12915-021-01139-5

https://repository.kaust.edu.sa/bitstream/10754/664279/3/s12915-021-01139-5.pdf

Cite this

Mourier, T., de Alvarenga, D. A. M., Kaushik, A., de Pina-Costa, A., Douvropoulou, O., Guan, Q., Guzmán-Vega, F. J., Forrester, S., de Abreu, F. V. S., Júnior, C. B., de Souza Junior, J. C., Moreira, S. B., Hirano, Z. M. B., Pissinatti, A., Ferreira-da-Cruz, M. D. F., de Oliveira, R. L., Arold, S. T., Jeffares, D. C., Brasil, P., ... Pain, A. (2021). The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host switching. BMC Biology, 19(1). https://doi.org/10.1186/s12915-021-01139-5

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title = "The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host switching",

abstract = "Abstract Background Plasmodium simium, a malaria parasite of non-human primates (NHP), was recently shown to cause zoonotic infections in humans in Brazil. We sequenced the P. simium genome to investigate its evolutionary history and to identify any genetic adaptions that may underlie the ability of this parasite to switch between host species. Results Phylogenetic analyses based on whole genome sequences of P. simium from humans and NHPs reveals that P. simium is monophyletic within the broader diversity of South American Plasmodium vivax, suggesting P. simium first infected NHPs as a result of a host switch of P. vivax from humans. The P. simium isolates show the closest relationship to Mexican P. vivax isolates. Analysis of erythrocyte invasion genes reveals differences between P. vivax and P. simium, including large deletions in the Duffy-binding protein 1 (DBP1) and reticulocyte-binding protein 2a genes of P. simium. Analysis of P. simium isolated from NHPs and humans revealed a deletion of 38 amino acids in DBP1 present in all human-derived isolates, whereas NHP isolates were multi-allelic. Conclusions Analysis of the P. simium genome confirmed a close phylogenetic relationship between P. simium and P. vivax, and suggests a very recent American origin for P. simium. The presence of the DBP1 deletion in all human-derived isolates tested suggests that this deletion, in combination with other genetic changes in P. simium, may facilitate the invasion of human red blood cells and may explain, at least in part, the basis of the recent zoonotic infections.",

author = "Tobias Mourier and {de Alvarenga}, {Denise Anete Madureira} and Abhinav Kaushik and {de Pina-Costa}, Anielle and Olga Douvropoulou and Qingtian Guan and Guzm{\'a}n-Vega, {Francisco J.} and Sarah Forrester and {de Abreu}, {Filipe Vieira Santos} and J{\'u}nior, {Cesare Bianco} and {de Souza Junior}, {Julio Cesar} and Moreira, {Silvia Bahadian} and Hirano, {Zelinda Maria Braga} and Alcides Pissinatti and Ferreira-da-Cruz, {Maria de F{\'a}tima} and {de Oliveira}, {Ricardo Louren{\c c}o} and Arold, {Stefan T.} and Jeffares, {Daniel C.} and Patr{\'i}cia Brasil and {de Brito}, {Cristiana Ferreira Alves} and Richard Culleton and Daniel-Ribeiro, {Cl{\'a}udio Tadeu} and Arnab Pain",

note = "KAUST Repository Item: Exported on 2021-10-04 Acknowledged KAUST grant number(s): BAS/1/1056-01-01, BRF1020/01/01, OSR, URF/1/1976-25 Acknowledgements: The work was supported financially by the King Abdullah University of Science and Technology (KAUST) through the baseline fund BRF1020/01/01 to AP and BAS/1/1056-01-01 to STA, and the Award No. URF/1/1976-25 from the Office of Sponsored Research (OSR). The field work in the Atlantic Forest and laboratory analysis in Brazil received financial support from the Secretary for Health Surveillance of the Ministry of Health through the Global Fund (agreement IOC-005-Fio-13), Programa Nacional de Excel{\^e}ncia (PRONEX) and contract 407873/2018-0 of the Conselho Nacional de Desenvolvimento Cient{\'i}fico e Tecnol{\'o}gico (CNPq), the Funda{\c c}{\~a}o de Amparo {\`a} Pesquisa do Estado de Minas Gerais (Fapemig CBB-APQ-02620-15) and the Funda{\c c}{\~a}o Carlos Chagas Filho de Amparo {\`a} Pesquisa do Estado do Rio de Janeiro (Faperj), Brazil. CNPq supports CFAB, CTDR, MFFC, PB and RLO, with a research productivity fellowship. CTDR (CNE: E-26/202.921/2018), MFFC, PB and RLO are also supported by Faperj as Cientistas do nosso estado. AdP-C was supported by a postdoctoral fellowship from the Faperj and DAMA by a fellowship from the CGZV-SVS (Brazilian Ministry of Health) TED 49/2018 grant. SF was supported by a Wellcome Seed Award in Science to DCJ (208965/Z/17/Z).",

year = "2021",

month = oct,

day = "1",

doi = "10.1186/s12915-021-01139-5",

language = "English (US)",

volume = "19",

journal = "BMC Biology",

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Mourier, T, de Alvarenga, DAM, Kaushik, A, de Pina-Costa, A, Douvropoulou, O, Guan, Q, Guzmán-Vega, FJ, Forrester, S, de Abreu, FVS, Júnior, CB, de Souza Junior, JC, Moreira, SB, Hirano, ZMB, Pissinatti, A, Ferreira-da-Cruz, MDF, de Oliveira, RL, Arold, ST, Jeffares, DC, Brasil, P, de Brito, CFA, Culleton, R, Daniel-Ribeiro, CT & Pain, A 2021, 'The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host switching', BMC Biology, vol. 19, no. 1. https://doi.org/10.1186/s12915-021-01139-5

TY - JOUR

T1 - The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host switching

AU - Mourier, Tobias

AU - de Alvarenga, Denise Anete Madureira

AU - Kaushik, Abhinav

AU - de Pina-Costa, Anielle

AU - Douvropoulou, Olga

AU - Guan, Qingtian

AU - Guzmán-Vega, Francisco J.

AU - Forrester, Sarah

AU - de Abreu, Filipe Vieira Santos

AU - Júnior, Cesare Bianco

AU - de Souza Junior, Julio Cesar

AU - Moreira, Silvia Bahadian

AU - Hirano, Zelinda Maria Braga

AU - Pissinatti, Alcides

AU - Ferreira-da-Cruz, Maria de Fátima

AU - de Oliveira, Ricardo Lourenço

AU - Arold, Stefan T.

AU - Jeffares, Daniel C.

AU - Brasil, Patrícia

AU - de Brito, Cristiana Ferreira Alves

AU - Culleton, Richard

AU - Daniel-Ribeiro, Cláudio Tadeu

AU - Pain, Arnab

N1 - KAUST Repository Item: Exported on 2021-10-04 Acknowledged KAUST grant number(s): BAS/1/1056-01-01, BRF1020/01/01, OSR, URF/1/1976-25 Acknowledgements: The work was supported financially by the King Abdullah University of Science and Technology (KAUST) through the baseline fund BRF1020/01/01 to AP and BAS/1/1056-01-01 to STA, and the Award No. URF/1/1976-25 from the Office of Sponsored Research (OSR). The field work in the Atlantic Forest and laboratory analysis in Brazil received financial support from the Secretary for Health Surveillance of the Ministry of Health through the Global Fund (agreement IOC-005-Fio-13), Programa Nacional de Excelência (PRONEX) and contract 407873/2018-0 of the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Fapemig CBB-APQ-02620-15) and the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (Faperj), Brazil. CNPq supports CFAB, CTDR, MFFC, PB and RLO, with a research productivity fellowship. CTDR (CNE: E-26/202.921/2018), MFFC, PB and RLO are also supported by Faperj as Cientistas do nosso estado. AdP-C was supported by a postdoctoral fellowship from the Faperj and DAMA by a fellowship from the CGZV-SVS (Brazilian Ministry of Health) TED 49/2018 grant. SF was supported by a Wellcome Seed Award in Science to DCJ (208965/Z/17/Z).

PY - 2021/10/1

Y1 - 2021/10/1

N2 - Abstract Background Plasmodium simium, a malaria parasite of non-human primates (NHP), was recently shown to cause zoonotic infections in humans in Brazil. We sequenced the P. simium genome to investigate its evolutionary history and to identify any genetic adaptions that may underlie the ability of this parasite to switch between host species. Results Phylogenetic analyses based on whole genome sequences of P. simium from humans and NHPs reveals that P. simium is monophyletic within the broader diversity of South American Plasmodium vivax, suggesting P. simium first infected NHPs as a result of a host switch of P. vivax from humans. The P. simium isolates show the closest relationship to Mexican P. vivax isolates. Analysis of erythrocyte invasion genes reveals differences between P. vivax and P. simium, including large deletions in the Duffy-binding protein 1 (DBP1) and reticulocyte-binding protein 2a genes of P. simium. Analysis of P. simium isolated from NHPs and humans revealed a deletion of 38 amino acids in DBP1 present in all human-derived isolates, whereas NHP isolates were multi-allelic. Conclusions Analysis of the P. simium genome confirmed a close phylogenetic relationship between P. simium and P. vivax, and suggests a very recent American origin for P. simium. The presence of the DBP1 deletion in all human-derived isolates tested suggests that this deletion, in combination with other genetic changes in P. simium, may facilitate the invasion of human red blood cells and may explain, at least in part, the basis of the recent zoonotic infections.

AB - Abstract Background Plasmodium simium, a malaria parasite of non-human primates (NHP), was recently shown to cause zoonotic infections in humans in Brazil. We sequenced the P. simium genome to investigate its evolutionary history and to identify any genetic adaptions that may underlie the ability of this parasite to switch between host species. Results Phylogenetic analyses based on whole genome sequences of P. simium from humans and NHPs reveals that P. simium is monophyletic within the broader diversity of South American Plasmodium vivax, suggesting P. simium first infected NHPs as a result of a host switch of P. vivax from humans. The P. simium isolates show the closest relationship to Mexican P. vivax isolates. Analysis of erythrocyte invasion genes reveals differences between P. vivax and P. simium, including large deletions in the Duffy-binding protein 1 (DBP1) and reticulocyte-binding protein 2a genes of P. simium. Analysis of P. simium isolated from NHPs and humans revealed a deletion of 38 amino acids in DBP1 present in all human-derived isolates, whereas NHP isolates were multi-allelic. Conclusions Analysis of the P. simium genome confirmed a close phylogenetic relationship between P. simium and P. vivax, and suggests a very recent American origin for P. simium. The presence of the DBP1 deletion in all human-derived isolates tested suggests that this deletion, in combination with other genetic changes in P. simium, may facilitate the invasion of human red blood cells and may explain, at least in part, the basis of the recent zoonotic infections.

UR - http://hdl.handle.net/10754/664279

UR - https://bmcbiol.biomedcentral.com/articles/10.1186/s12915-021-01139-5

U2 - 10.1186/s12915-021-01139-5

DO - 10.1186/s12915-021-01139-5

M3 - Article

C2 - 34592986

SN - 1741-7007

VL - 19

JO - BMC Biology

JF - BMC Biology

IS - 1

ER -

The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host switching

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The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptions to host-switching

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The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host switching

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Bibliographical note

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UN SDGs

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The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptions to host-switching

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