Plasmodium delichoni n. sp.: description, molecular characterisation and remarks on the exoerythrocytic merogony, persistence, vectors and transmission

Abstract

Malaria parasite Plasmodium (Novyella) delichoni n. sp. (Haemosporida, Plasmodiidae) was found in a widespread Eurasian songbird, the common house martin Delichon urbicum (Hirundinidae). It is described based on the morphology of its blood stages and segments of the mitochondrial cytochrome b and apicoplast genes, which can be used for molecular identification of this species. Erythrocytic meronts and gametocytes are strictly nucleophilic, and mature gametocytes possess pigment granules of markedly variable size, including large ones (1 μm in length). Due to these features, P. delichoni can be readily distinguished from all described species of avian malaria parasites belonging to subgenus Novyella. Additionally, mature erythrocytic merozoites contain a dense clump of chromatin, a rare character in avian malaria parasites. Erythrocytic merogony is asynchronous. Illustrations of blood stages of the new species are given, and phylogenetic analysis identifies DNA lineages closely related to this parasite. Domestic canary Serinus canaria and Eurasian siskin Carduelis spinus were infected after subinoculation of infected blood obtained from the house martin. Parasitemia was long lasting in both these hosts, but it was high (up to 70 %) in Eurasian siskins and low (up to 1 %) in canaries. Mortality was not observed, and histological examination and chromogenic in situ hybridisation did not reveal secondary exoerythrocytic meronts (phanerozoites) in the exposed birds. It is likely that persistence of this infection occurs due to long-lasting parasitemia in avian hosts. Sporogony was abortive in mosquitoes Culex pipiens pipiens form molestus, Culex quinquefasciatus and Aedes aegypti at gametogenesis or ookinete stages. The new species is absent from juvenile birds at breeding sites in Europe, indicating that transmission occurs at African wintering grounds.

Delineation of the Genera Haemoproteus and Plasmodium Using RNA-Seq and Multi-gene Phylogenetics

“…These phylogenetic reconstructions based on both Bayesian and likelihood methods found a sister relationship between Plasmodium and Parahaemoproteus . To summarize previous research, four articles supported a Parahaemoproteus /subgenus Haemoproteus sister relationship (Valkiūnas et al 2010, 2016; Palinauskas et al 2015; Lutz et al 2016), five articles supported a Plasmodium / Parahaemoproteus sister relationship (Martinsen et al 2008; Santiago-Alarcón et al 2010; Martinezde la Puente et al 2011; Pacheco et al 2018) and one article obtained mixed results depending on the taxa, evolutionary model and genes analyzed (Borner et al 2016). Pacheco et al (2018) bears special mention as the most recent study with the largest dataset in terms of complete mitochondrial genes (Pacheco et al 2018).…”

“…Interestingly, the authors found Plasmodium as a paraphyletic clade (Lutz et al 2016). Recent work by Valkiūnas describing a new malaria parasite Plasmodium delichoni included phylogenetic analyses describing a sister relationship of the subgenus Haemoproteus and Parahaemoproteus , and a more distant relationship with Plasmodium (Valkiūnas et al 2016). Finally, work by Pacheco et al (2018) used 114 complete mitochondrial genomes of many taxa to infer the relationships of haemosporidians for the genera Leucocytozoon, Plasmodium, Haemoproteus and Hepatocystis .…”

“…1a (Martinsen et al 2008; Santiago-Alarcón et al 2010; Martinez-de la Puente et al 2011; Pacheco et al 2018) or with both subgenera forming a monophyletic clade as in Fig. 1b (Valkiūnas et al 2010, 2016; Levin et al 2012; Carlson et al 2013; Palinauskas et al 2015; Lutz et al 2016). While the dataset used in Borner et al (2016) provided strong resolution for all other clades, it is interesting that H. columbae ’s placement could not be resolved.…”

Exo-erythrocytic development of avian malaria and related haemosporidian parasites

“…It is difficult to see phanerozoites in some Novyella species even if parasitaemia is high [2, 4, 130–132]. Recent histological studies, combined with chromogenic in situ hybridization diagnostic tools indicate that exo-erythrocytic development in some tropical Novyella species is mainly primary, and the persistence of infection is due to long-lasting light parasitaemia [133]. In other words, merozoites developing in erythrocytic meronts of these parasites might be unable or have limited ability to produce phanerozoites.…”

Molecular characterization and distribution of Plasmodium matutinum, a common avian malaria parasite

“…One blood film from each bird was rapidly stained and examined microscopically, as described by Valkiunas et al (2016). One nightingale infected with an unidentified lineage of P. matutinum was determined and used for the strain isolation during this study.…”