Plasmodium vinckei genomes provide insights into the pan-genome and evolution of rodent malaria parasites
Abstract Background Rodent malaria parasites (RMPs) serve as tractable tools to study malaria parasite biology and host-parasite-vector interactions. Among the four RMPs originally collected from wild thicket rats in sub-Saharan Central Africa and adapted to laboratory mice, Plasmodium vinckei is th...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2021-04-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-021-00995-5 |
| _version_ | 1818827642982367232 |
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| author | Abhinay Ramaprasad Severina Klaus Olga Douvropoulou Richard Culleton Arnab Pain |
| author_facet | Abhinay Ramaprasad Severina Klaus Olga Douvropoulou Richard Culleton Arnab Pain |
| author_sort | Abhinay Ramaprasad |
| collection | DOAJ |
| description | Abstract Background Rodent malaria parasites (RMPs) serve as tractable tools to study malaria parasite biology and host-parasite-vector interactions. Among the four RMPs originally collected from wild thicket rats in sub-Saharan Central Africa and adapted to laboratory mice, Plasmodium vinckei is the most geographically widespread with isolates collected from five separate locations. However, there is a lack of extensive phenotype and genotype data associated with this species, thus hindering its use in experimental studies. Results We have generated a comprehensive genetic resource for P. vinckei comprising of five reference-quality genomes, one for each of its subspecies, blood-stage RNA sequencing data for five P. vinckei isolates, and genotypes and growth phenotypes for ten isolates. Additionally, we sequenced seven isolates of the RMP species Plasmodium chabaudi and Plasmodium yoelii, thus extending genotypic information for four additional subspecies enabling a re-evaluation of the genotypic diversity and evolutionary history of RMPs. The five subspecies of P. vinckei have diverged widely from their common ancestor and have undergone large-scale genome rearrangements. Comparing P. vinckei genotypes reveals region-specific selection pressures particularly on genes involved in mosquito transmission. Using phylogenetic analyses, we show that RMP multigene families have evolved differently across the vinckei and berghei groups of RMPs and that family-specific expansions in P. chabaudi and P. vinckei occurred in the common vinckei group ancestor prior to speciation. The erythrocyte membrane antigen 1 and fam-c families in particular show considerable expansions among the lowland forest-dwelling P. vinckei parasites. The subspecies from the highland forests of Katanga, P. v. vinckei, has a uniquely smaller genome, a reduced multigene family repertoire and is also amenable to transfection making it an ideal parasite for reverse genetics. We also show that P. vinckei parasites are amenable to genetic crosses. Conclusions Plasmodium vinckei isolates display a large degree of phenotypic and genotypic diversity and could serve as a resource to study parasite virulence and immunogenicity. Inclusion of P. vinckei genomes provide new insights into the evolution of RMPs and their multigene families. Amenability to genetic crossing and transfection make them also suitable for classical and functional genetics to study Plasmodium biology. |
| first_indexed | 2024-12-19T00:46:49Z |
| format | Article |
| id | doaj.art-d52bba8055e146bab710391f5799072a |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-19T00:46:49Z |
| publishDate | 2021-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-d52bba8055e146bab710391f5799072a2022-12-21T20:44:14ZengBMCBMC Biology1741-70072021-04-0119112210.1186/s12915-021-00995-5Plasmodium vinckei genomes provide insights into the pan-genome and evolution of rodent malaria parasitesAbhinay Ramaprasad0Severina Klaus1Olga Douvropoulou2Richard Culleton3Arnab Pain4Pathogen Genomics Group, BESE Division, King Abdullah University of Science and Technology (KAUST)Malaria Unit, Department of Pathology, Institute of Tropical Medicine (NEKKEN), Nagasaki UniversityPathogen Genomics Group, BESE Division, King Abdullah University of Science and Technology (KAUST)Malaria Unit, Department of Pathology, Institute of Tropical Medicine (NEKKEN), Nagasaki UniversityPathogen Genomics Group, BESE Division, King Abdullah University of Science and Technology (KAUST)Abstract Background Rodent malaria parasites (RMPs) serve as tractable tools to study malaria parasite biology and host-parasite-vector interactions. Among the four RMPs originally collected from wild thicket rats in sub-Saharan Central Africa and adapted to laboratory mice, Plasmodium vinckei is the most geographically widespread with isolates collected from five separate locations. However, there is a lack of extensive phenotype and genotype data associated with this species, thus hindering its use in experimental studies. Results We have generated a comprehensive genetic resource for P. vinckei comprising of five reference-quality genomes, one for each of its subspecies, blood-stage RNA sequencing data for five P. vinckei isolates, and genotypes and growth phenotypes for ten isolates. Additionally, we sequenced seven isolates of the RMP species Plasmodium chabaudi and Plasmodium yoelii, thus extending genotypic information for four additional subspecies enabling a re-evaluation of the genotypic diversity and evolutionary history of RMPs. The five subspecies of P. vinckei have diverged widely from their common ancestor and have undergone large-scale genome rearrangements. Comparing P. vinckei genotypes reveals region-specific selection pressures particularly on genes involved in mosquito transmission. Using phylogenetic analyses, we show that RMP multigene families have evolved differently across the vinckei and berghei groups of RMPs and that family-specific expansions in P. chabaudi and P. vinckei occurred in the common vinckei group ancestor prior to speciation. The erythrocyte membrane antigen 1 and fam-c families in particular show considerable expansions among the lowland forest-dwelling P. vinckei parasites. The subspecies from the highland forests of Katanga, P. v. vinckei, has a uniquely smaller genome, a reduced multigene family repertoire and is also amenable to transfection making it an ideal parasite for reverse genetics. We also show that P. vinckei parasites are amenable to genetic crosses. Conclusions Plasmodium vinckei isolates display a large degree of phenotypic and genotypic diversity and could serve as a resource to study parasite virulence and immunogenicity. Inclusion of P. vinckei genomes provide new insights into the evolution of RMPs and their multigene families. Amenability to genetic crossing and transfection make them also suitable for classical and functional genetics to study Plasmodium biology.https://doi.org/10.1186/s12915-021-00995-5Plasmodium vinckeiMalariaRodent malaria parasitesGenomicsTranscriptomicsGenetics |
| spellingShingle | Abhinay Ramaprasad Severina Klaus Olga Douvropoulou Richard Culleton Arnab Pain Plasmodium vinckei genomes provide insights into the pan-genome and evolution of rodent malaria parasites BMC Biology Plasmodium vinckei Malaria Rodent malaria parasites Genomics Transcriptomics Genetics |
| title | Plasmodium vinckei genomes provide insights into the pan-genome and evolution of rodent malaria parasites |
| title_full | Plasmodium vinckei genomes provide insights into the pan-genome and evolution of rodent malaria parasites |
| title_fullStr | Plasmodium vinckei genomes provide insights into the pan-genome and evolution of rodent malaria parasites |
| title_full_unstemmed | Plasmodium vinckei genomes provide insights into the pan-genome and evolution of rodent malaria parasites |
| title_short | Plasmodium vinckei genomes provide insights into the pan-genome and evolution of rodent malaria parasites |
| title_sort | plasmodium vinckei genomes provide insights into the pan genome and evolution of rodent malaria parasites |
| topic | Plasmodium vinckei Malaria Rodent malaria parasites Genomics Transcriptomics Genetics |
| url | https://doi.org/10.1186/s12915-021-00995-5 |
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