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Sporogony of four Haemoproteus species (Haemosporida: Haemoproteidae), with report of in vitro ookinetes of Haemoproteus hirundinis: phylogenetic inference indicates patterns of haemosporidian parasite ookinete development.

ABSTRACT: BACKGROUND:Haemoproteus (Parahaemoproteus) species (Haemoproteidae) are widespread blood parasites that can cause disease in birds, but information about their vector species, sporogonic development and transmission remain fragmentary. This study aimed to investigate the complete sporogonic development of four Haemoproteus species in Culicoides nubeculosus and to test if phylogenies based on the cytochrome b gene (cytb) reflect patterns of ookinete development in haemosporidian parasites. Additionally, one cytb lineage of Haemoproteus was identified to the species level and the in vitro gametogenesis and ookinete development of Haemoproteus hirundinis was characterised. METHODS:Laboratory-reared C. nubeculosus were exposed by allowing them to take blood meals on naturally infected birds harbouring single infections of Haemoproteus belopolskyi (cytb lineage hHIICT1), Haemoproteus hirundinis (hDELURB2), Haemoproteus nucleocondensus (hGRW01) and Haemoproteus lanii (hRB1). Infected insects were dissected at intervals in order to detect sporogonic stages. In vitro exflagellation, gametogenesis and ookinete development of H. hirundinis were also investigated. Microscopic examination and PCR-based methods were used to confirm species identity. Bayesian phylogenetic inference was applied to study the relationships among Haemoproteus lineages. RESULTS:All studied parasites completed sporogony in C. nubeculosus. Ookinetes and sporozoites were found and described. Development of H. hirundinis ookinetes was similar both in vivo and in vitro. Developing ookinetes of this parasite possess long outgrowths, which extend longitudinally and produce the apical end of the ookinetes. A large group of closely related Haemoproteus species with a similar mode of ookinete development was determined. Bayesian analysis indicates that this character has phylogenetic value. The species identity of cytb lineage hDELURB2 was determined: it belongs to H. hirundinis. CONCLUSIONS:Culicoides nubeculosus is susceptible to and is a likely natural vector of numerous species of Haemoproteus parasites, thus worth attention in haemoproteosis epidemiology research. Data about in vitro development of haemoproteids provide valuable information about the rate of ookinete maturation and are recommended to use as helpful step during vector studies of haemosporidian parasites, particularly because they guide proper dissection interval of infected insects for ookinete detection during in vivo experiments. Additionally, in vitro studies readily identified patterns of morphological ookinete transformations, the characters of which are of phylogenetic value in haemosporidian parasites.

SUBMITTER: Chagas CRF

PROVIDER: S-EPMC6714444 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Sporogony of four Haemoproteus species (Haemosporida: Haemoproteidae), with report of in vitro ookinetes of Haemoproteus hirundinis: phylogenetic inference indicates patterns of haemosporidian parasite ookinete development.

Chagas Carolina Romeiro Fernandes CRF Bukauskaitė Dovilė D Ilgūnas Mikas M Bernotienė Rasa R Iezhova Tatjana T Valkiūnas Gediminas G

Parasites & vectors 20190828 1

<h4>Background</h4>Haemoproteus (Parahaemoproteus) species (Haemoproteidae) are widespread blood parasites that can cause disease in birds, but information about their vector species, sporogonic development and transmission remain fragmentary. This study aimed to investigate the complete sporogonic development of four Haemoproteus species in Culicoides nubeculosus and to test if phylogenies based on the cytochrome b gene (cytb) reflect patterns of ookinete development in haemosporidian parasites ...[more]

PMID: 31462309

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Project description:BackgroundHaemoproteus is a sister genus to malaria parasites (Plasmodium), which both belong to the order Haemosporida (Apicomplexa). Parasites of both genera are flourishing in birds, however, Haemoproteus species are noticeably less investigated. This is unfortunate because knowledge about close relatives of malaria pathogens is important for better understanding the evolutionary origin and basic biological features of the entire group of haemosporidian infections. Moreover, recent findings show that Haemoproteus species can cause severe damage of various bird organs due to megalomeronts and other exo-erythrocytic stages. These haemosporidians are remarkably diverse, but remain neglected partly due to difficulties in species identification. Hundreds of Haemoproteus genetic lineages have been reported in birds, and numerous new lineages are found each year, but most remain unidentified to the species level. Numerous new Haemoproteus pathogens were described during the past 20 years. However, keys for their identification are absent. Identification of Haemoproteus species remains a difficult task and is an obstacle for better understanding of the distribution and epidemiology of these parasites. This study aimed to develop comprehensive keys for the identification of described avian Haemoproteus species using morphological features of their blood stages (gametocytes).MethodsType and voucher preparations of avian Haemoproteus species were accessed in museums in Europe, Australia and the USA. Gametocytes of most described species were examined, and these data formed a background for this study. The data also were considered from published articles containing parasite species descriptions. The method of dichotomous keys was applied. The most difficult steps in the keys were accompanied with references to the corresponding parasite pictures.ResultsIn all, 201 published articles were included in this review. Morphological diagnostic features of gametocytes of all described Haemoproteus species were analysed and compared. Illustrated keys for identification of these parasite species were developed. Available information about the molecular characterization of Haemoproteus parasites was provided.ConclusionThis review shows that 177 described species of avian Haemoproteus can be distinguished and identified in blood films using morphological characters of their gametocytes and host cells. These species were incorporated in the keys. Information about possible morphologically cryptic parasites was provided. Molecular markers are available for only 42% of the described Haemoproteus parasites, calling for researchers to fill this gap.

Project description:BackgroundHaemoproteus parasites (Haemosporida, Haemoproteidae) are cosmopolitan in birds and recent molecular studies indicate enormous genetic diversity of these pathogens, which cause diseases in non-adapted avian hosts. However, life-cycles remain unknown for the majority of Haemoproteus species. Information on their exoerythrocytic development is particularly fragmental and controversial. This study aimed to gain new knowledge on life-cycle of the widespread blood parasite Haemoproteus majoris.MethodsTurdus pilaris and Parus major naturally infected with lineages hPHYBOR04 and hPARUS1 of H. majoris, respectively, were wild-caught and the parasites were identified using microscopic examination of gametocytes and PCR-based testing. Bayesian phylogeny was used to determine relationships between H. majoris lineages. Exoerythrocytic stages (megalomeronts) were reported using histological examination and laser microdissection was applied to isolate single megalomeronts for genetic analysis. Culicoides impunctatus biting midges were experimentally exposed in order to follow sporogonic development of the lineage hPHYBOR04.ResultsGametocytes of the lineage hPHYBOR04 are indistinguishable from those of the widespread lineage hPARUS1 of H. majoris, indicating that both of these lineages belong to the H. majoris group. Phylogenetic analysis supported this conclusion. Sporogony of the lineage hPHYBOR04 was completed in C. impunctatus biting midges. Morphologically similar megalomeronts were reported in internal organs of both avian hosts. These were big roundish bodies (up to 360 μm in diameter) surrounded by a thick capsule-like wall and containing irregularly shaped cytomeres, in which numerous merozoites developed. DNA sequences obtained from single isolated megalomeronts confirmed the identification of H. majoris.ConclusionsPhylogenetic analysis identified a group of closely related H. majoris lineages, two of which are characterized not only by morphologically identical blood stages, but also complete sporogonic development in C. impunctatus and development of morphologically similar megalomeronts. It is probable that other lineages belonging to the same group would bear the same characters and phylogenies based on partial cytb gene could be used to predict life-cycle features in avian haemoproteids including vector identity and patterns of exoerythrocytic merogony. This study reports morphologically unique megalomeronts in naturally infected birds and calls for research on exoerythrocytic development of haemoproteids to better understand pathologies caused in avian hosts.

Project description:Haemoproteus parasites are widespread, and several species cause diseases both in birds and blood-sucking insects. These pathogens are transmitted by dipterans belonging to the Ceratopogonidae and Hippoboscidae, however certain vector species remain unknown for the majority of Haemoproteus spp. Owls are often infected by Haemoproteus parasites, but experimental studies on vectors of these infections are lacking. The aim of this study was to investigate sporogonic development of two widespread Haemoproteus parasites of owls, H. noctuae and H. syrnii in experimentally infected biting midges Culicoides impunctatus and Culicoides nubeculosus. We also followed in vitro sporogonic development of these infections and determined their phylogenetic relationships with Haemoproteus spp., for which vectors have been identified.Wild-caught C. impunctatus and laboratory reared C. nubeculosus were infected experimentally by allowing them to take blood meals on one individual long-eared owl (Asio otus) and one tawny owl (Strix aluco) harbouring mature gametocytes of H. noctuae (lineage hCIRCUM01) and H. syrnii (hCULCIB01), respectively. The engorged insects were maintained in the laboratory at 16-18 °C, and dissected at intervals in order to follow the development of ookinetes, oocysts and sporozoites. We also observed in vitro development of sexual stages of both parasites by exposure of infected blood to air. The parasite lineages were determined by polymerase chain reaction-based methods. Bayesian phylogeny was constructed in order to determine the relationships of owl parasites with other avian Haemoproteus spp., for which vectors have been identified.Both H. noctuae and H. syrnii completed sporogony in C. nubeculosus, and H. noctuae completed sporogony in C. impunctatus. Ookinetes, oocysts and sporozoites of these parasites were reported and described. Gametes and ookinetes of both species readily developed in vitro. In accordance with sporogony data, the phylogenetic analysis placed both parasite lineages in a clade of Culicoides spp.-transmitted avian Haemoproteus (Parahaemoproteus) spp.Culicoides nubeculosus and C. impunctatus are vectors of H. noctuae and H. syrnii. Phylogenies based on cytochrome b gene indicate parasite-vector relationships, and we recommend using them in predicting possible parasite-vector relationships and planning research on avian Haemoproteus spp. vectors in wildlife.

Project description:BackgroundHaemoproteus parasites are widespread, and some species cause disease in wild and domestic birds. However, the insect vectors remain unknown for the majority of species and genetic lineages of avian Haemoproteus. This information is crucial for better understanding the biology of haemoproteids, the epidemiology of haemoproteosis, and the development of morphological characters of sporogonic stages in wildlife haemosporidian parasites. It remains unclear whether the specificity of Haemoproteus parasites for vectors is broad or the transmission of a given parasite can be restricted to a single or few species of vectors. The aim of this study was to examine the sporogonic development of four species of common European avian haemoproteids in the common biting midge Culicoides impunctatus.MethodsWild-caught females of C. impunctatus were infected experimentally by allowing them to take blood meals on naturally infected Muscicapa striata, Cyanistes caeruleus, Ficedula hypoleuca and Motacilla flava harbouring mature gametocytes of Haemoproteus balmorali (genetic lineage hSFC9), H. majoris (hPARUS1), H. motacillae (hYWT1) and H. pallidus (hPFC1), respectively. Infected insects were collected, maintained under laboratory conditions and dissected daily in order to detect the development of ookinetes, oocysts and sporozoites. Microscopic examination and polymerase chain reaction based methods were used to detect the parasites. Bayesian analysis was applied to identify phylogenetic relationships among Haemoproteus lineages.ResultsAll investigated parasites completed sporogony in C. impunctatus, indicating broad susceptibility of this biting midge for numerous Haemoproteus parasites. Ookinetes, oocysts and sporozoites were reported, described and compared morphologically. The investigated parasite species can be distinguished at the sporogony stage, particularly with regards to the morphology and rate of development of mature ookinetes. Analysis of data from the literature, and this study, shows that 12 genetically distantly related Haemoproteus parasites complete sporogony in C. impunctatus.ConclusionsSusceptibility of C. impunctatus is broad for Haemoproteus parasites, indicating that this biting midge is an important natural vector of numerous species of avian haemoproteids in Europe. Some Haemoproteus species can be readily distinguished using morphological characters of ookinetes and sporozoites, as well as the rate of ookinete development. These characters can be used for the identification of Haemoproteus species during sporogony in vectors, and are worth more attention in these parasite taxonomy studies at the species levels.

Project description:BACKGROUND: One of the major issues concerning disease ecology and conservation is knowledge of the factors that influence the distribution of parasites and consequently disease outbreaks. This study aimed to investigate avian haemosporidian composition and the distribution of these parasites in three altitudinally separated great tit (Parus major) populations in western Switzerland over a three-year period. The objectives were to determine the lineage diversity of parasites occuring across the study populations and to investigate whether altitudinal gradients govern the distribution of haemosporidian parasites by lineage. METHODS: In this study molecular approaches (PCR and sequencing) were used to detect avian blood parasites (Plasmodium sp., Haemoproteus sp. and Leucocytozoon sp.) in populations of adult great tits caught on their nests during three consecutive breeding seasons. RESULTS: High levels of parasite prevalence (88-96%) were found across all of the study populations with no significant altitude effect. Altitude did, however, govern the distribution of parasites belonging to different genera, with Plasmodium parasites being more prevalent at lower altitudes, Leucocytozoon parasites more at high altitude and Haemoproteus parasite prevalence increasing with altitude. A total of 27 haemosporidian parasite lineages were recorded across all study sites, with diversity showing a positive correlation to altitude. Parasites belonging to lineage SGS1 (P. relictum) and PARUS4 and PARUS19 (Leucocytozoon sp.) dominated lower altitudes. SW2 (P. polare) was the second most prevalent lineage of parasite detected overall and these parasites were responsible for 68% of infections at intermediate altitude, but were only documented at this one study site. CONCLUSIONS: Avian haemosporidian parasites are not homogeneously distributed across host populations, but differ by altitude. This difference is most probably brought about by environmental factors influencing vector prevalence and distribution. The high occurrence of co-infection by different genera of parasites might have pronounced effects on host fitness and should consequently be investigated more rigorously.

Project description:BACKGROUND:New World vultures (Cathartiformes: Cathartidae) are obligate scavengers comprised of seven species in five genera throughout the Americas. Of these, turkey vultures (Cathartes aura) and black vultures (Coragyps atratus) are the most widespread and, although ecologically similar, have evolved differences in morphology, physiology, and behaviour. Three species of haemosporidians have been reported in New World vultures to date: Haemoproteus catharti, Leucocytozoon toddi and Plasmodium elongatum, although few studies have investigated haemosporidian parasites in this important group of species. In this study, morphological and molecular methods were used to investigate the epidemiology and molecular biology of haemosporidian parasites of New World vultures in North America. METHODS:Blood and/or tissue samples were obtained from 162 turkey vultures and 95 black vultures in six states of the USA. Parasites were identified based on their morphology in blood smears, and sequences of the mitochondrial cytochrome b and nuclear adenylosuccinate lyase genes were obtained for molecular characterization. RESULTS:No parasites were detected in black vultures, whereas 24% of turkey vultures across all sampling locations were positive for H. catharti by blood smear analysis and/or PCR testing. The phylogenetic analysis of cytochrome b gene sequences revealed that H. catharti is closely related to MYCAMH1, a yet unidentified haemosporidian from wood storks (Mycteria americana) in southeastern USA and northern Brazil. Haemoproteus catharti and MYCAMH1 represent a clade that is unmistakably separate from all other Haemoproteus spp., being most closely related to Haemocystidium spp. from reptiles and to Plasmodium spp. from birds and reptiles. CONCLUSIONS:Haemoproteus catharti is a widely-distributed parasite of turkey vultures in North America that is evolutionarily distinct from other haemosporidian parasites. These results reveal that the genetic diversity and evolutionary relationships of avian haemosporidians are still being uncovered, and future studies combining a comprehensive evaluation of morphological and life cycle characteristics with the analysis of multiple nuclear and mitochondrial genes will be useful to redefine the genus boundaries of these parasites and to re-evaluate the relationships amongst haemosporidians of birds, reptiles and mammals.

Dataset Information

Sporogony of four Haemoproteus species (Haemosporida: Haemoproteidae), with report of in vitro ookinetes of Haemoproteus hirundinis: phylogenetic inference indicates patterns of haemosporidian parasite ookinete development.

Publications

Sporogony of four Haemoproteus species (Haemosporida: Haemoproteidae), with report of in vitro ookinetes of Haemoproteus hirundinis: phylogenetic inference indicates patterns of haemosporidian parasite ookinete development.

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