Herpetomonas trimorpha sp. nov. (Trypanosomatidae, Kinetoplastida), a parasite of the biting midge Culicoides truncorum (Ceratopogonidae, Diptera)

Abstract

Monoxenous trypanosomatid Herpetomonas trimorpha sp. nov. was isolated from the digestive tract of the biting midge Culicoides truncorum (Ceratopogonidae, Diptera). This species forms three distinct morphotypes in culture: the microflagellate promastigote, the small promastigote and the long promastigote. The last form is unique for the newly described species. Phylogenetic analyses of SSU rRNA and glycosomal glyceraldehyde phosphate dehydrogenase genes showed that H. trimorpha sp. nov. is the closest relative of Herpetomonas ztiplika, another monoxenous trypanosomatid isolated from biting midges. However, morphological and randomly amplified polymorphic DNA analyses confirmed that H. trimorpha sp. nov. is distinct from H. ztiplika. INTRODUCTIONThe genus Herpetomonas comprises monoxenous trypanosomatids, which mainly parasitize the digestive tract of muscid Diptera (Wallace, 1966;Molyneux, 1977;McGhee & Cosgrove, 1980;Podlipaev, 1990). However, herpetomonads have also been isolated from plants and even mammals (Morsy et al., 1988; Catarino et al., 2001;Fiorini et al., 2001;Podlipaev et al., 2004a;Marín et al., 2007). The classification of the genus Herpetomonas is problematic and, similar to most other monoxenous trypanosomatid genera, the genus is polyphyletic (Camargo et al., 1992;Teixeira et al., 1997;Hollar et al., 1998;Hughes & Piontkivska, 2003;Podlipaev et al., 2004a). Therefore, a major taxonomic revision of 'lower' trypanosomatids is needed (see Bulat et al., 1999;Podlipaev, 2000Podlipaev, , 2001Maslov et al., 2001;Merzlyak et al., 2001;Momen, 2001;Yurchenko et al., 2008Yurchenko et al., , 2009).Over 30 herpetomonad species have been described at the time of writing (McGhee & Cosgrove, 1980;Podlipaev, 1990) , 2008, 2009). Indeed, the classical diagnostic character, i.e. the presence of promastigotes and opisthomastigotes, is no longer considered to be sufficient for assigning a trypanosomatid to the genus Herpetomonas (Camargo et al., 1992;Podlipaev et al., 2004b). On the other hand, some trypanosomatids were described solely on the basis of their host specificity, following the 'one host -one parasite' paradigm. However, this approach was not found universally applicable as single trypanosomatid species have been shown to infect more host species and vice versa (Bulat et al., 1999;Podlipaev, 2003;Podlipaev et al., 2004a;Svobodová et al., 2007). Recently, the most promising approach for species description seems to be a combination of several methods including molecular phylogenetics (Batistoti et al., 2001;Yurchenko et al., 2006;Svobodová et al., 2007).Here, based on morphology, ultrastructure, phylogenetic analysis of SSU rRNA and glycosomal glyceraldehyde phosphate dehydrogenase (gGAPDH) genes, and randomly amplified polymorphic DNA (RAPD) analysis, we describe Herpetomonas trimorpha sp. nov. as a parasite of the intestinal tract of biting midges (Ceratopogonidae), closely related to Herpetomonas ztiplika. The main feature of the novel species is the ability to form three distinct morphotypes in cu...

Biting midges (Ceratopogonidae) as vectors of avian trypanosomes

“…In our previous study on ornithophilic biting midges, dissections of 2493 guts of midges belonging to seven Culicoides species revealed 1.4% prevalence of kinetoplastids. From 36 positive guts, eight strains have been established that belonged to monoxenous trypanosomatids [10, 21, 22]. Potentially, some of the unsuccessful cultures might belong to T. bennetti clade.…”

Free-living ciliates as potential reservoirs for eukaryotic parasites: occurrence of a trypanosomatid in the macronucleus of Euplotes encysticus

“…A similarity value (Additional file 2: Table S2) of 99.42% and 99.84%, respectively, is shared among the trypanosomatid 18S rRNA gene sequence described here and Herpetomonas ztiplika AY308760 [8] and Herpetomonas trimorpha EU179326 [9]. All three sequences formed a highly stable association (Figure 5.…”

“…It has already been shown that the existence of extensive size and shape polymorphism within a single trypanosomatid species according to cultivation conditions strongly impairs the resolution power of those characters for identification and taxonomy [1,8,9,15]. The consequential conflict between traditional taxonomy and molecular phylogeny is well known also for the genus Herpetomonas and resulted in the recent redescription of this taxon, based mainly on molecular data [5].…”

“…Furthermore, it was shown that some of these parasites can exhibit extremely diverse morphologies which may even differ depending on the growth environment, i.e. host or culture medium [1,8,9]. Molecular phylogenetics, based on the 18S rRNA, glycosomal glyceraldehyde phosphate dehydrogenase (gGAPDH) and spliced leader (SL) RNA genes are nowadays considered the method of choice to assess taxonomy and phylogenetic relationships of kinetoplastid flagellates [3-5,10-12].…”

First detection of Leishmania infantum (Kinetoplastida: Trypanosomatidae) in Culicoides spp. (Diptera: Ceratopogonidae)

“…However, since this date and until the beginning of the 20th century, no data were published concerning the potential involvement of biting midges in Leishmania transmission. Between 2004 and 2010, some researchers reported the natural infection of Culicoides biting midges by Herpetomonas and Sergeia kinetoplastid protozoa [3-5]. …”