High Prevalence and Endemism of Trypanosomatids on a Small Caribbean Island

Votýpka, Jan; Kment, Petr; Kriegová, Eva; Vermeij, Mark J. A.; Keeling, Patrick J.; Yurchenko, Vyacheslav; Lukeš, Julius

doi:10.1111/jeu.12704

Cited by 11 publications

(10 citation statements)

References 42 publications

(100 reference statements)

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“…pyrrhocoris LBVs can be explained by a restricted host range of L . pyrrhocoris , which infects predominantly firebugs [ 4 , 26 ]. This resulted in the evolutionary preservation of the ancestral forms with the full-length M and S segments.…”

Section: Resultsmentioning

confidence: 99%

Diversity of RNA viruses in the cosmopolitan monoxenous trypanosomatid Leptomonas pyrrhocoris

Macedo,

Grybchuk,

Režnarová

et al. 2023

BMC Biol

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Background Trypanosomatids are parasitic flagellates well known because of some representatives infecting humans, domestic animals, and cultural plants. Many trypanosomatid species bear RNA viruses, which, in the case of human pathogens Leishmania spp., influence the course of the disease. One of the close relatives of leishmaniae, Leptomonas pyrrhocoris, has been previously shown to harbor viruses of the groups not documented in other trypanosomatids. At the same time, this species has a worldwide distribution and high prevalence in the natural populations of its cosmopolitan firebug host. It therefore represents an attractive model to study the diversity of RNA viruses. Results We surveyed 106 axenic cultures of L. pyrrhocoris and found that 64 (60%) of these displayed 2–12 double-stranded RNA fragments. The analysis of next-generation sequencing data revealed four viral groups with seven species, of which up to five were simultaneously detected in a single trypanosomatid isolate. Only two of these species, a tombus-like virus and an Ostravirus, were earlier documented in L. pyrrhocoris. In addition, there were four new species of Leishbuviridae, the family encompassing trypanosomatid-specific viruses, and a new species of Qinviridae, the family previously known only from metatranscriptomes of invertebrates. Currently, this is the only qinvirus with an unambiguously determined host. Our phylogenetic inferences suggest reassortment in the tombus-like virus owing to the interaction of different trypanosomatid strains. Two of the new Leishbuviridae members branch early on the phylogenetic tree of this family and display intermediate stages of genomic segment reduction between insect Phenuiviridae and crown Leishbuviridae. Conclusions The unprecedented wide range of viruses in one protist species and the simultaneous presence of up to five viral species in a single Leptomonas pyrrhocoris isolate indicate the uniqueness of this flagellate. This is likely determined by the peculiarity of its firebug host, a highly abundant cosmopolitan species with several habits ensuring wide distribution and profuseness of L. pyrrhocoris, as well as its exposure to a wider spectrum of viruses compared to other trypanosomatids combined with a limited ability to transmit these viruses to its relatives. Thus, L. pyrrhocoris represents a suitable model to study the adoption of new viruses and their relationships with a protist host.

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Section: Resultsmentioning

confidence: 99%

Diversity of RNA viruses in the cosmopolitan monoxenous trypanosomatid Leptomonas pyrrhocoris

Macedo,

Grybchuk,

Režnarová

et al. 2023

BMC Biol

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“…For example, a study on the presence of trypanosomatids in Austrian mosquitoes revealed that 12 out of 19 species harbored these parasites with a prevalence ranging from 16% to 61% [ 8 ]. In other studies, trypanosomatids were identified in eight species of Drosophila analyzed in southwest Ohio (USA), with a prevalence of 1–17% [ 9 ], and the prevalence of trypanosomatids on insects in the island of Curaçao and Papua New Guinea was 38% and 15%, respectively [ 10 , 11 ]. In addition, the presence of monoxenous parasites has been identified in 4.3% of tsetse flies collected in the Dzanga-Sangha Protected Area (Central African Republic) [ 12 ].…”

Section: Introductionmentioning

confidence: 99%

Development of a TaqMan qPCR assay for trypanosomatid multi-species detection and quantification in insects

et al. 2023

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Background Trypanosomatid parasites are widely distributed in nature and can have a monoxenous or dixenous life-cycle. These parasites thrive in a wide number of insect orders, some of which have an important economic and environmental value, such as bees. The objective of this study was to develop a robust and sensitive real-time quantitative PCR (qPCR) assay for detecting trypanosomatid parasites in any type of parasitized insect sample. Methods A TaqMan qPCR assay based on a trypanosomatid-conserved region of the α-tubulin gene was standardized and evaluated. The limits of detection, sensitivity and versatility of the α-tubulin TaqMan assay were tested and validated using field samples of honeybee workers, wild bees, bumblebees and grasshoppers, as well as in the human infective trypanosomatid Leishmania major. Results The assay showed a detection limit of 1 parasite equivalent/µl and successfully detected trypanosomatids in 10 different hosts belonging to the insect orders Hymenoptera and Orthoptera. The methodology was also tested using honeybee samples from four apiaries (n = 224 worker honeybees) located in the Alpujarra region (Granada, Spain). Trypanosomatids were detected in 2.7% of the honeybees, with an intra-colony prevalence of 0% to 13%. Parasite loads in the four different classes of insects ranged from 40.6 up to 1.1 × 108 cell equivalents per host. Conclusions These results show that the α-tubulin TaqMan qPCR assay described here is a versatile diagnostic tool for the accurate detection and quantification of trypanosomatids in a wide range of environmental settings. Graphical Abstract

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“…While the last decade has seen a significant expansion of the known diversity of insect and plant trypanosomatids including some studies from Asia, Europe and Africa (Votýpka et al, 2010(Votýpka et al, , 2012aLukeš et al, 2018;Frolov et al, 2019Frolov et al, , 2020, it was continental South and Central America where most sampling occurred (Teixeira et al, 1997(Teixeira et al, , 2011Maslov et al, 2007Maslov et al, , 2010Borghesan et al, 2013;Kozminsky et al, 2015;Dario et al, 2021). However, except for a single study conducted on the island of Curacao (Votýpka et al, 2019), so far, no information was available on these interesting protists in the Caribbean. Here, we present such a study from Cuba, in which we have not only mapped the distribution and diversity of trypanosomatids but also applied ONT sequencing to examine their frequency and extent of co-infections within a single insect host.…”

Section: Discussionmentioning

confidence: 99%

Multiple and frequent trypanosomatid co-infections of insects: the Cuban case study

Votýpka,

Zeman,

Stříbrná

et al. 2024

Parasitology

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Trypanosomatids are obligate parasites of animals, predominantly insects and vertebrates, and flowering plants. Monoxenous species, representing the vast majority of trypanosomatid diversity, develop in a single host, whereas dixenous species cycle between two hosts, of which primarily insect serves as a vector. To explore in-depth the diversity of insect trypanosomatids including their co-infections, sequence profiling of their 18S rRNA gene was used for true bugs (Hemiptera; 18% infection rate) and flies (Diptera; 10%) in Cuba. Out of 48 species (molecular operational taxonomic units) belonging to the genera Vickermania (16 spp.), Blastocrithidia (7), Obscuromonas (4), Phytomonas (5), Leptomonas/Crithidia (5), Herpetomonas (5), Wallacemonas (2), Kentomonas (1), Angomonas (1) and two unnamed genera (1 + 1), 38 species have been encountered for the first time. The detected Wallacemonas and Angomonas species constitute the most basal lineages of their respective genera, while Vickermania emerged as the most diverse group. The finding of Leptomonas seymouri, which is known to rarely infect humans, confirms that Dysdercus bugs are its natural hosts. A clear association of Phytomonas with the heteropteran family Pentatomidae hints at its narrow host association with the insect rather than plant hosts. With a focus on multiple infections of a single fly host, using deep Nanopore sequencing of 18S rRNA, we have identified co-infections with up to 8 trypanosomatid species. The fly midgut was usually occupied by several Vickermania species, while Herpetomonas and/or Kentomonas species prevailed in the hindgut. Metabarcoding was instrumental for analysing extensive co-infections and also allowed the identification of trypanosomatid lineages and genera.

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High Prevalence and Endemism of Trypanosomatids on a Small Caribbean Island

Cited by 11 publications

References 42 publications

Diversity of RNA viruses in the cosmopolitan monoxenous trypanosomatid Leptomonas pyrrhocoris

Diversity of RNA viruses in the cosmopolitan monoxenous trypanosomatid Leptomonas pyrrhocoris

Development of a TaqMan qPCR assay for trypanosomatid multi-species detection and quantification in insects

Multiple and frequent trypanosomatid co-infections of insects: the Cuban case study

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