Characterization of Plasmodium relictum, a cosmopolitan agent of avian malaria

Abstract

BackgroundMicroscopic 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.MethodsThe 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.ResultsCommon 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.ConclusionWithin 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.Electronic supplementary materialThe online version of this article (10.1186/s12936-018-2325-2) contains supplementary material, which is available to authorized users.

Penguins are competent hosts of Haemoproteus parasites: the first detection of gametocytes, with molecular characterization of Haemoproteus larae

“…3). Similar intraspecific variations have been reported in the relatively well-studied morphospecies Haemoproteus majoris [59], Plasmodium relictum [60] and other avian haemosporidians, in which morphologically defined species are known to consist of multiple closely related cytb lineages. While there have been a few reports of H. larae in gulls, these reports are all solely based on morphological identification [61], and future investigation using a combination of molecular and morphological methods may reveal other molecular lineages of H. larae.…”

Haemoproteus minutus is highly virulent for Australasian and South American parrots

“…Most notable are the major extinctions of the endemic bird population of Hawaiian honeycreepers (Fringillidae, subfamily Carduelinae) [7, 9]. Plasmodium relictum is the most successful malaria parasite worldwide, and is reported from over 300 avian species belonging to 11 orders [10]. Studies on experimentally infected birds found the P. relictum lineage GRW4 and the related species P. elongatum to be highly virulent for naïve hosts [11, 12].…”

Host Transcriptional Responses to High- and Low-Virulent Avian Malaria Parasites

“…Plasmodium relictum is a well-known parasite of birds and is considered to be one of the world's top 100 most invasive species (Alowe et al 2000;Valkiūnas et al 2018). The morphologically defined species P. relictum consists of several cryptic lineages based on absolute differences in the mitochondrial gene cytochrome b, and the most prevalent lineage is SGS1 (Palinauskas et al 2007;Hellgren et al 2009Hellgren et al , 2015.…”

“…Closely related to SGS1 is the P. relictum lineage GRW4 (Valkiūnas et al 2007(Valkiūnas et al , 2018, which also encompasses a broad host range of 80 bird species spanning five orders (Beadell et al 2006;Bensch et al 2009). When identified in the blood of wild birds, GRW4 normally displays low parasitemia and seems in general to be quite avirulent with little or no fitness consequences for the host (Bensch et al 2007;Asghar et al 2011;Dimitrov et al 2015).…”

“…However, naive bird species that have evolved on remote islands without malaria parasites seem to experience exceptionally high parasitemia and mortality when exposed to GRW4 (Atkinson et al 1995(Atkinson et al , 2000Beadell et al 2006). Crucially, the two P. relictum lineages SGS1 and GRW4 are morphologically indistinguishable (Valkiūnas et al 2018) and differ by only 1.8% nucleotides in cytochrome b (Bensch et al 2009). It is possible that SGS1 and GRW4 should be considered separate (cryptic) species, as they have also been shown to harbor additional differences in their nuclear genes (Hellgren et al 2013(Hellgren et al , 2015Garcia-Longoria et al 2014).…”