Research Article: Comparative Transcriptomic Exploration Reveals Unique Molecular Adaptations of Neuropathogenic Trichobilharzia to Invade and Parasitize Its Avian Definitive Host

Date Published: February 10, 2016

Publisher: Public Library of Science

Author(s): Roman Leontovyč, Neil D. Young, Pasi K. Korhonen, Ross S. Hall, Patrick Tan, Libor Mikeš, Martin Kašný, Petr Horák, Robin B. Gasser, Matty Knight.

Abstract: To date, most molecular investigations of schistosomatids have focused principally on blood flukes (schistosomes) of humans. Despite the clinical importance of cercarial dermatitis in humans caused by Trichobilharzia regenti and the serious neuropathologic disease that this parasite causes in its permissive avian hosts and accidental mammalian hosts, almost nothing is known about the molecular aspects of how this fluke invades its hosts, migrates in host tissues and how it interacts with its hosts’ immune system. Here, we explored selected aspects using a transcriptomic-bioinformatic approach. To do this, we sequenced, assembled and annotated the transcriptome representing two consecutive life stages (cercariae and schistosomula) of T. regenti involved in the first phases of infection of the avian host. We identified key biological and metabolic pathways specific to each of these two developmental stages and also undertook comparative analyses using data available for taxonomically related blood flukes of the genus Schistosoma. Detailed comparative analyses revealed the unique involvement of carbohydrate metabolism, translation and amino acid metabolism, and calcium in T. regenti cercariae during their invasion and in growth and development, as well as the roles of cell adhesion molecules, microaerobic metabolism (citrate cycle and oxidative phosphorylation), peptidases (cathepsins) and other histolytic and lysozomal proteins in schistosomula during their particular migration in neural tissues of the avian host. In conclusion, the present transcriptomic exploration provides new and significant insights into the molecular biology of T. regenti, which should underpin future genomic and proteomic investigations of T. regenti and, importantly, provides a useful starting point for a range of comparative studies of schistosomatids and other trematodes.

Partial Text: The bird fluke Trichobilharzia regenti is a member of the Schistosomatidae (= blood flukes; Class Trematoda), a family of parasitic flatworms of medical and veterinary importance [1,2]. T. regenti is widely distributed geographically and is highly prevalent, for instance, in parts of Europe (including Russia), New Zealand and Iran [3–6]. Like blood flukes of the genus Schistosoma, T. regenti is dioecious, has a two-host life cycle (including a lymnaeid snail of the genus Radix) and has an invasive furcocercarial stage that actively penetrates the skin of a definitive vertebrate host. Unlike members of the genus Schistosoma, T. regenti invades and migrates through skin and nerves to then establish within the nasal mucosa [7–9]. During its aquatic phase, T. regenti can accidently penetrate human skin and cause cercarial dermatitis. Cercarial dermatitis, caused by avian schistosomes, is regarded as an emerging disease [10–12] although global economic losses are not known, it is accepted that this condition can have a considerable impact on local, tourism-based economies, and may also represent a debilitating occupational disease of rice farmers (see Horák et al., 2015 for review [12]). As avian (including T. regenti) and human schistosomes can occur in the same water reservoirs, there are at least two issues of relevance in relation to the differential diagnosis of disease: (a) Based on clinical signs, cercarial dermatitis caused by avian schistosomes can be confused with that caused by human schistosomes [13]. (b) Prevalence surveys of hepatointestinal or urogenital schistosomiasis of humans might be influenced/affected by serological cross-reactivity resulting from exposure to cercariae of avian schistosomes [14].

To date, genomic and transcriptomic studies of schistosomatids have focused on S. mansoni, S. japonicum and S. haematobium [52–54]. In the present study, we characterized the first transcriptome of any avian fluke, T. regenti, undertook comparative studies with other schistosomatids and elucidated differences between two key developmental stages responsible for host invasion (cercaria) and migration through the neural tissues (schistosomulum) at the molecular level.



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