Host-dependent impairment of parasite development and reproduction in the acanthocephalan model

Abstract

Background A central question in parasitology is why parasites mature and reproduce in some host species but not in others. Yet, a better understanding of the inability of parasites to complete their life cycles in less suitable hosts may hold clues for their control. To shed light on the molecular basis of parasite (non-)maturation, we analyzed transcriptomes of thorny-headed worms (Acanthocephala: Pomphorhynchus laevis), and compared developmentally arrested worms excised from European eel (Anguilla anguilla) to developmentally unrestricted worms from barbel (Barbus barbus). Results Based on 20 RNA-Seq datasets, we demonstrate that transcriptomic profiles are more similar between P. laevis males and females from eel than between their counterparts from barbel. Impairment of sexual phenotype development was reflected in gene ontology enrichment analyses of genes having differential transcript abundances. Genes having reproduction- and energy-related annotations were found to be affected by parasitizing either eel or barbel. According to this, the molecular machinery of male and female acanthocephalans from the eel is less tailored to reproduction and more to coping with the less suitable environment provided by this host. The pattern was reversed in their counterparts from the definitive host, barbel. Conclusions Comparative analysis of transcriptomes of developmentally arrested and reproducing parasites elucidates the challenges parasites encounter in hosts which are unsuitable for maturation and reproduction. By studying a gonochoric species, we were also able to highlight sex-specific traits. In fact, transcriptomic evidence for energy shortage in female acanthocephalans associates with their larger body size. Thus, energy metabolism and glycolysis should be promising targets for the treatment of acanthocephaliasis. Although inherently enabling a higher resolution in heterosexuals, the comparison of parasites from definitive hosts and less suitable hosts, in which the parasites merely survive, should be applicable to hermaphroditic helminths. This may open new perspectives in the control of other helminth pathogens of humans and livestock.

Hooking the scientific community on thorny-headed worms: interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala

“…Taxa actively feeding on host tissues, such as adult nematodes and monogeneans [64], can be clearly differentiated from acanthocephalans and cestodes that behave as absorptive feeders. Transcriptomic analyses in adult acanthocephalans revealed several genes involved in energy metabolism and carotenoid uptake especially under anaerobic conditions (fermentation) [105,151]. Importantly, definitive host response to intestinal acanthocephalans involves coordinate responses from the enteric neural, endocrine, and immune systems (see Bosi et al (2022) [23] for a review in fish), which relies on molecular crosstalk between host and parasite molecular effectors and modulators.…”

“…Detailed transcriptomics and proteomics analyses should be encouraged in the future in a broader range of acanthocephalan species, to unravel the physiological/molecular pathways of nutrient acquisition in adult acanthocephalans and the molecular basis of inflammation, but also the impact of infection on gut microbiota [33], parasite resource acquisition and allocation in optimal and sub-optimal hosts [151], and ultimately the fitness for both the acanthocephalan and its host. This should also contribute to understand the evolution of acanthocephalan virulence towards their definitive hosts, as under some environmental conditions, acanthocephalans might actually be beneficial to their definitive hosts (cf.…”

Identification of antiparasitic drug targets using a multi-omics workflow in the acanthocephalan model

“…Adapter sequences and low-quality parts of the sequences were trimmed with Trimmomatic v0.39 [98]. For more details of sampling and sequencing see [99]. While we aimed to filter out proteins with constant abundance across conditions in the present study, the referenced study demonstrates overall differing proteomic profiles in male and female worms from different hosts.…”