Novel RNA viruses associated with Plasmodium vivax in human malaria and Leucocytozoon parasites in avian disease

Justine Charon, Matthew J. Grigg, John Sebastian Eden, Kim A. Piera, Hafsa Rana, Timothy William, Karrie Rose, Miles P. Davenport, Nicholas M. Anstey, Edward C. Holmes

    Research output: Contribution to journalArticleResearchpeer-review

    64 Downloads (Pure)

    Abstract

    Eukaryotes of the genus Plasmodium cause malaria, a parasitic disease responsible for substantial morbidity and mortality in humans. Yet, the nature and abundance of any viruses carried by these divergent eukaryotic parasites is unknown. We investigated the Plasmodium virome by performing a meta-transcriptomic analysis of blood samples taken from patients suffering from malaria and infected with P. vivax, P. falciparum or P. knowlesi. This resulted in the identification of a narnavirus-like sequence, encoding an RNA polymerase and restricted to P. vivax samples, as well as an associated viral segment of unknown function. These data, confirmed by PCR, are indicative of a novel RNA virus that we term Matryoshka RNA virus 1 (MaRNAV-1) to reflect its analogy to a "Russian doll": A virus, infecting a parasite, infecting an animal. Additional screening revealed that MaRNAV-1 was abundant in geographically diverse P. vivax derived from humans and mosquitoes, strongly supporting its association with this parasite, and not in any of the other Plasmodium samples analyzed here nor Anopheles mosquitoes in the absence of Plasmodium. Notably, related bi-segmented narnavirus-like sequences (MaRNAV-2) were retrieved from Australian birds infected with a Leucocytozoon -a genus of eukaryotic parasites that group with Plasmodium in the Apicomplexa subclass hematozoa. Together, these data support the establishment of two new phylogenetically divergent and genomically distinct viral species associated with protists, including the first virus likely infecting Plasmodium parasites. As well as broadening our understanding of the diversity and evolutionary history of the eukaryotic virosphere, the restriction to P. vivax may be of importance in understanding P. vivax-specific biology in humans and mosquitoes, and how viral co-infection might alter host responses at each stage of the P. vivax life-cycle.

    Original languageEnglish
    Article numbere1008216
    Pages (from-to)1-26
    Number of pages26
    JournalPLoS Pathogens
    Volume15
    Issue number12
    DOIs
    Publication statusPublished - 30 Dec 2019

    Fingerprint

    Bird Diseases
    Plasmodium vivax
    RNA Viruses
    Plasmodium
    Malaria
    Parasites
    Culicidae
    Viruses
    Plasmodium malariae
    Apicomplexa
    Parasitic Diseases
    Anopheles
    Virus Diseases
    DNA-Directed RNA Polymerases
    Life Cycle Stages
    Eukaryota
    Coinfection
    Birds
    Meta-Analysis
    Morbidity

    Cite this

    Charon, Justine ; Grigg, Matthew J. ; Eden, John Sebastian ; Piera, Kim A. ; Rana, Hafsa ; William, Timothy ; Rose, Karrie ; Davenport, Miles P. ; Anstey, Nicholas M. ; Holmes, Edward C. / Novel RNA viruses associated with Plasmodium vivax in human malaria and Leucocytozoon parasites in avian disease. In: PLoS Pathogens. 2019 ; Vol. 15, No. 12. pp. 1-26.
    @article{e89b18737eca41748f0638dd58b91ee2,
    title = "Novel RNA viruses associated with Plasmodium vivax in human malaria and Leucocytozoon parasites in avian disease",
    abstract = "Eukaryotes of the genus Plasmodium cause malaria, a parasitic disease responsible for substantial morbidity and mortality in humans. Yet, the nature and abundance of any viruses carried by these divergent eukaryotic parasites is unknown. We investigated the Plasmodium virome by performing a meta-transcriptomic analysis of blood samples taken from patients suffering from malaria and infected with P. vivax, P. falciparum or P. knowlesi. This resulted in the identification of a narnavirus-like sequence, encoding an RNA polymerase and restricted to P. vivax samples, as well as an associated viral segment of unknown function. These data, confirmed by PCR, are indicative of a novel RNA virus that we term Matryoshka RNA virus 1 (MaRNAV-1) to reflect its analogy to a {"}Russian doll{"}: A virus, infecting a parasite, infecting an animal. Additional screening revealed that MaRNAV-1 was abundant in geographically diverse P. vivax derived from humans and mosquitoes, strongly supporting its association with this parasite, and not in any of the other Plasmodium samples analyzed here nor Anopheles mosquitoes in the absence of Plasmodium. Notably, related bi-segmented narnavirus-like sequences (MaRNAV-2) were retrieved from Australian birds infected with a Leucocytozoon -a genus of eukaryotic parasites that group with Plasmodium in the Apicomplexa subclass hematozoa. Together, these data support the establishment of two new phylogenetically divergent and genomically distinct viral species associated with protists, including the first virus likely infecting Plasmodium parasites. As well as broadening our understanding of the diversity and evolutionary history of the eukaryotic virosphere, the restriction to P. vivax may be of importance in understanding P. vivax-specific biology in humans and mosquitoes, and how viral co-infection might alter host responses at each stage of the P. vivax life-cycle.",
    author = "Justine Charon and Grigg, {Matthew J.} and Eden, {John Sebastian} and Piera, {Kim A.} and Hafsa Rana and Timothy William and Karrie Rose and Davenport, {Miles P.} and Anstey, {Nicholas M.} and Holmes, {Edward C.}",
    year = "2019",
    month = "12",
    day = "30",
    doi = "10.1371/journal.ppat.1008216",
    language = "English",
    volume = "15",
    pages = "1--26",
    journal = "PLoS Pathogens",
    issn = "1553-7366",
    publisher = "Public Library of Science (PLoS)",
    number = "12",

    }

    Charon, J, Grigg, MJ, Eden, JS, Piera, KA, Rana, H, William, T, Rose, K, Davenport, MP, Anstey, NM & Holmes, EC 2019, 'Novel RNA viruses associated with Plasmodium vivax in human malaria and Leucocytozoon parasites in avian disease', PLoS Pathogens, vol. 15, no. 12, e1008216, pp. 1-26. https://doi.org/10.1371/journal.ppat.1008216

    Novel RNA viruses associated with Plasmodium vivax in human malaria and Leucocytozoon parasites in avian disease. / Charon, Justine; Grigg, Matthew J.; Eden, John Sebastian; Piera, Kim A.; Rana, Hafsa; William, Timothy; Rose, Karrie; Davenport, Miles P.; Anstey, Nicholas M.; Holmes, Edward C.

    In: PLoS Pathogens, Vol. 15, No. 12, e1008216, 30.12.2019, p. 1-26.

    Research output: Contribution to journalArticleResearchpeer-review

    TY - JOUR

    T1 - Novel RNA viruses associated with Plasmodium vivax in human malaria and Leucocytozoon parasites in avian disease

    AU - Charon, Justine

    AU - Grigg, Matthew J.

    AU - Eden, John Sebastian

    AU - Piera, Kim A.

    AU - Rana, Hafsa

    AU - William, Timothy

    AU - Rose, Karrie

    AU - Davenport, Miles P.

    AU - Anstey, Nicholas M.

    AU - Holmes, Edward C.

    PY - 2019/12/30

    Y1 - 2019/12/30

    N2 - Eukaryotes of the genus Plasmodium cause malaria, a parasitic disease responsible for substantial morbidity and mortality in humans. Yet, the nature and abundance of any viruses carried by these divergent eukaryotic parasites is unknown. We investigated the Plasmodium virome by performing a meta-transcriptomic analysis of blood samples taken from patients suffering from malaria and infected with P. vivax, P. falciparum or P. knowlesi. This resulted in the identification of a narnavirus-like sequence, encoding an RNA polymerase and restricted to P. vivax samples, as well as an associated viral segment of unknown function. These data, confirmed by PCR, are indicative of a novel RNA virus that we term Matryoshka RNA virus 1 (MaRNAV-1) to reflect its analogy to a "Russian doll": A virus, infecting a parasite, infecting an animal. Additional screening revealed that MaRNAV-1 was abundant in geographically diverse P. vivax derived from humans and mosquitoes, strongly supporting its association with this parasite, and not in any of the other Plasmodium samples analyzed here nor Anopheles mosquitoes in the absence of Plasmodium. Notably, related bi-segmented narnavirus-like sequences (MaRNAV-2) were retrieved from Australian birds infected with a Leucocytozoon -a genus of eukaryotic parasites that group with Plasmodium in the Apicomplexa subclass hematozoa. Together, these data support the establishment of two new phylogenetically divergent and genomically distinct viral species associated with protists, including the first virus likely infecting Plasmodium parasites. As well as broadening our understanding of the diversity and evolutionary history of the eukaryotic virosphere, the restriction to P. vivax may be of importance in understanding P. vivax-specific biology in humans and mosquitoes, and how viral co-infection might alter host responses at each stage of the P. vivax life-cycle.

    AB - Eukaryotes of the genus Plasmodium cause malaria, a parasitic disease responsible for substantial morbidity and mortality in humans. Yet, the nature and abundance of any viruses carried by these divergent eukaryotic parasites is unknown. We investigated the Plasmodium virome by performing a meta-transcriptomic analysis of blood samples taken from patients suffering from malaria and infected with P. vivax, P. falciparum or P. knowlesi. This resulted in the identification of a narnavirus-like sequence, encoding an RNA polymerase and restricted to P. vivax samples, as well as an associated viral segment of unknown function. These data, confirmed by PCR, are indicative of a novel RNA virus that we term Matryoshka RNA virus 1 (MaRNAV-1) to reflect its analogy to a "Russian doll": A virus, infecting a parasite, infecting an animal. Additional screening revealed that MaRNAV-1 was abundant in geographically diverse P. vivax derived from humans and mosquitoes, strongly supporting its association with this parasite, and not in any of the other Plasmodium samples analyzed here nor Anopheles mosquitoes in the absence of Plasmodium. Notably, related bi-segmented narnavirus-like sequences (MaRNAV-2) were retrieved from Australian birds infected with a Leucocytozoon -a genus of eukaryotic parasites that group with Plasmodium in the Apicomplexa subclass hematozoa. Together, these data support the establishment of two new phylogenetically divergent and genomically distinct viral species associated with protists, including the first virus likely infecting Plasmodium parasites. As well as broadening our understanding of the diversity and evolutionary history of the eukaryotic virosphere, the restriction to P. vivax may be of importance in understanding P. vivax-specific biology in humans and mosquitoes, and how viral co-infection might alter host responses at each stage of the P. vivax life-cycle.

    UR - http://www.scopus.com/inward/record.url?scp=85077779923&partnerID=8YFLogxK

    U2 - 10.1371/journal.ppat.1008216

    DO - 10.1371/journal.ppat.1008216

    M3 - Article

    VL - 15

    SP - 1

    EP - 26

    JO - PLoS Pathogens

    JF - PLoS Pathogens

    SN - 1553-7366

    IS - 12

    M1 - e1008216

    ER -