Dataset Information

Genomic variation in Plasmodium relictum (lineage SGS1) and its implications for avian malaria infection outcomes: insights from experimental infections and genome-wide analysis.

ABSTRACT:

Background

The globally transmitted avian malaria parasite Plasmodium relictum (lineage SGS1) has been found to infect hundreds of different bird species with differences in infection outcomes ranging from more or less latent to potentially mortal. However, to date basic knowledge about the links between genetic differentiation and variation in infection outcome within this single malaria parasite species is lacking.

Methods

In this study, two different isolates of SGS1, obtained in the wild from two different host species, were used to investigate differences in their development in the blood and virulence in the experimentally infected canaries. Simultaneously, 258 kb of the parasite genome was screened for genetic differences using parasite mRNA and compared between experimental groups.

Results

The two isolates showed differences in development and caused mortality as well as effects on the blood parameters of their hosts. Although previous studies using single genes have shown very limited within lineage genetic diversity in the European population of SGS1, 226 SNPs were found across 322 genes, which separated the two experimental groups with a total of 23 SNPs that were fixed in either of the experimental groups. Moreover, genetic variation was found within each experimental group, hinting that each avian malaria infection harbours standing genetic variation that might be selected during each individual infection episode.

Conclusion

These results highlight extensive genetic variation within the SGS1 population that is transferred into individual infections, thus adding to the complexity of the infection dynamics seen in these host-parasite interactions. Simultaneously, the results open up the possibility of understanding how genetic variation within the parasite populations is linked to the commonly observed differences in infection outcomes, both in experimental settings and in the wild.

SUBMITTER: Kalbskopf V

PROVIDER: S-EPMC11360878 | biostudies-literature | 2024 Aug

REPOSITORIES: biostudies-literature

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Publications

Genomic variation in Plasmodium relictum (lineage SGS1) and its implications for avian malaria infection outcomes: insights from experimental infections and genome-wide analysis.

Kalbskopf Victor V Aželytė Justė J Palinauskas Vaidas V Hellgren Olof O

Malaria journal 20240829 1

<h4>Background</h4>The globally transmitted avian malaria parasite Plasmodium relictum (lineage SGS1) has been found to infect hundreds of different bird species with differences in infection outcomes ranging from more or less latent to potentially mortal. However, to date basic knowledge about the links between genetic differentiation and variation in infection outcome within this single malaria parasite species is lacking.<h4>Methods</h4>In this study, two different isolates of SGS1, obtained ...[more]

PMID: 39210339

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Project description:BACKGROUND:Microscopic research has shown that Plasmodium relictum is the most common agent of avian malaria. Recent molecular studies confirmed this conclusion and identified several mtDNA lineages, suggesting the existence of significant intra-species genetic variation or cryptic speciation. Most identified lineages have a broad range of hosts and geographical distribution. Here, a rare new lineage of P. relictum was reported and information about biological characters of different lineages of this pathogen was reviewed, suggesting issues for future research. METHODS:The new lineage pPHCOL01 was detected in Common chiffchaff Phylloscopus collybita, and the parasite was passaged in domestic canaries Serinus canaria. Organs of infected birds were examined using histology and chromogenic in situ hybridization methods. Culex quinquefasciatus mosquitoes, Zebra finch Taeniopygia guttata, Budgerigar Melopsittacus undulatus and European goldfinch Carduelis carduelis were exposed experimentally. Both Bayesian and Maximum Likelihood analyses identified the same phylogenetic relationships among different, closely-related lineages pSGS1, pGRW4, pGRW11, pLZFUS01, pPHCOL01 of P. relictum. Morphology of their blood stages was compared using fixed and stained blood smears, and biological properties of these parasites were reviewed. RESULTS:Common canary and European goldfinch were susceptible to the parasite pPHCOL01, and had markedly variable individual prepatent periods and light transient parasitaemia. Exo-erythrocytic and sporogonic stages were not seen. The Zebra finch and Budgerigar were resistant. Neither blood stages nor vector stages of all examined P. relictum lineages can be distinguished morphologically. CONCLUSION:Within the huge spectrum of vertebrate hosts, mosquito vectors, and ecological conditions, different lineages of P. relictum exhibit indistinguishable, markedly variable morphological forms. Parasites of same lineages often develop differently in different bird species. Even more, the variation of biological properties (parasitaemia dynamics, blood pathology, prepatent period) in different isolates of the same lineage might be greater than the variation in different lineages during development in the same species of birds, indicating negligible taxonomic value of such features. Available lineage information is excellent for parasite diagnostics, but is limited in predictions about relationships in certain host-parasite associations. A combination of experiments, field observations, microscopic and molecular diagnostics is essential for understanding the role of different P. relictum lineages in bird health.

Project description:BackgroundPlasmodium parasites that cause bird malaria occur in all continents except Antarctica and are primarily transmitted by mosquitoes in the genus Culex. Culex quinquefasciatus, the mosquito vector of avian malaria in Hawai'i, became established in the islands in the 1820s. While the deadly effects of malaria on endemic bird species have been documented for many decades, vector-parasite interactions in avian malaria systems are relatively understudied.MethodsTo evaluate the gene expression response of mosquitoes exposed to a Plasmodium infection intensity known to occur naturally in Hawai'i, offspring of wild-collected Hawaiian Cx. quinquefasciatus were fed on a domestic canary infected with a fresh isolate of Plasmodium relictum GRW4 from a wild-caught Hawaiian honeycreeper. Control mosquitoes were fed on an uninfected canary. Transcriptomes of five infected and three uninfected individual mosquitoes were sequenced at each of three stages of the parasite life cycle: 24 h post feeding (hpf) during ookinete invasion; 5 days post feeding (dpf) when oocysts are developing; 10 dpf when sporozoites are released and invade the salivary glands.ResultsDifferential gene expression analyses showed that during ookinete invasion (24 hpf), genes related to oxidoreductase activity and galactose catabolism had lower expression levels in infected mosquitoes compared to controls. Oocyst development (5 dpf) was associated with reduced expression of a gene with a predicted innate immune function. At 10 dpf, infected mosquitoes had reduced expression levels of a serine protease inhibitor, and further studies should assess its role as a Plasmodium agonist in C. quinquefasciatus. Overall, the differential gene expression response of Hawaiian Culex exposed to a Plasmodium infection intensity known to occur naturally in Hawai'i was low, but more pronounced during ookinete invasion.ConclusionsThis is the first analysis of the transcriptional responses of vectors to malaria parasites in non-mammalian systems. Interestingly, few similarities were found between the response of Culex infected with a bird Plasmodium and those reported in Anopheles infected with human Plasmodium. The relatively small transcriptional changes observed in mosquito genes related to immune response and nutrient metabolism support conclusions of low fitness costs often documented in experimental challenges of Culex with avian Plasmodium.

Project description:BackgroundThe merozoite surface protein 1 (msp1) is one of the most studied vaccine candidate genes in mammalian Plasmodium spp. to have been used for investigations of epidemiology, population structures, and immunity to infections. However methodological difficulties have impeded the use of nuclear markers such as msp1 in Plasmodium parasites causing avian malaria. Data from an infection transcriptome of the host generalist avian malaria parasite Plasmodium relictum was used to identify and characterize the msp1 gene from two different isolates (mtDNA lineages SGS1 and GRW4). The aim was to investigate whether the msp1 gene in avian malaria species shares the properties of the msp1 gene in Plasmodium falciparum in terms of block variability, conserved anchor points and repeat motifs, and further to investigate the degree to which the gene might be informative in avian malaria parasites for population and epidemiological studies.MethodsReads from 454 sequencing of birds infected with avian malaria was used to develop Sanger sequencing protocols for the msp1 gene of P. relictum. Genetic variability between variable and conserved blocks of the gene was compared within and between avian malaria parasite species, including P. falciparum. Genetic variability of the msp1 gene in P. relictum was compared with six other nuclear genes and the mtDNA gene cytochrome b.ResultsThe msp1 gene of P. relictum shares the same general pattern of variable and conserved blocks as found in P. falciparum, although the variable blocks exhibited less variability than P. falciparum. The variation across the gene blocks in P. falciparum spanned from being as conserved as within species variation in P. relictum to being as variable as between the two avian malaria species (P. relictum and Plasmodium gallinaceum) in the variable blocks. In P. relictum the highly conserved p19 region of the peptide was identified, which included two epidermal growth factor-like domains and a fully conserved GPI anchor point.ConclusionThis study provides protocols for evaluation of the msp1 gene in the avian malaria generalist parasite P. relictum. The msp1 gene in avian Plasmodium shares the genetic properties seen in P. falciparum, indicating evolutionary conserved functions for the gene. The data on the variable blocks of the gene show that the msp1 gene in P. relictum might serve as a good candidate gene for future population and epidemiological studies of the parasite.

Project description:BackgroundPlasmodium elongatum (cytochrome b lineage pGRW6) is a widespread avian malaria parasite, often causing severe disease in non-adapted hosts. This parasite lineage is of global distribution however, its virulence remains insufficiently understood, particularly in wild birds. Surprisingly, this infection has never been reported in Common starlings Sturnus vulgaris and Common crossbills Loxia curvirostra, common European songbirds which were extensively sampled across Europe. A hypothesis was proposed that these birds might be resistant to the pGRW6 infection. The aim of this study was to test this hypothesis.MethodsLineage pGRW6 was isolated from a naturally infected Eurasian reed warbler, multiplied in vivo and inoculated in Common starlings and Common crossbills. Experimental and control groups (8 birds in each) were maintained in controlled conditions and examined microscopically every 4 days. Haematocrit value and body mass were monitored in parallel. At the end of the experiment (44 days post exposure), samples of internal organs were collected and examined using histological methods for possible presence of phanerozoites.ResultsAll control birds remained uninfected. Experimental starlings were resistant. All exposed crossbills were susceptible and survived until the end of this study. Prepatent period was 12-16 days post exposure. Light parasitaemia (< 0.7%) developed in all birds, and only few phanerozoites were seen in bone marrow cells of 5 of 8 experimentally infected crossbills. Significant changes were reported only in haematocrit value but not body mass in the exposed crossbills compared to controls.ConclusionPlasmodium elongatum (pGRW6) is of low virulence in Common crossbills and is unable to develop in Common starlings, indicating innate resistance of the later bird species. Low virulence in Common crossbills is likely due to the inability or low ability of this parasite lineage to develop phanerozoites resulting in light (if at all) damage of stem bone marrow cells. This study suggests that susceptibility of different bird species to the lineage pGRW6 is markedly variable. The global distribution of this parasite might be due to low virulence in wild adapted avian hosts, which survive this infection and serve as reservoirs host for non-adapted birds in whom this infection is often lethal.

Dataset Information

Genomic variation in Plasmodium relictum (lineage SGS1) and its implications for avian malaria infection outcomes: insights from experimental infections and genome-wide analysis.

Background

Methods

Results

Conclusion

Publications

Genomic variation in Plasmodium relictum (lineage SGS1) and its implications for avian malaria infection outcomes: insights from experimental infections and genome-wide analysis.

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