Major host transitions are modulated through transcriptome‐wide reprogramming events in Schistocephalus solidus, a threespine stickleback parasite

Abstract

Parasites with complex life cycles have developed numerous phenotypic strategies, closely associated with developmental events, to enable the exploitation of different ecological niches and facilitate transmission between hosts. How these environmental shifts are regulated from a metabolic and physiological standpoint, however, still remain to be fully elucidated. We examined the transcriptomic response of Schistocephalus solidus, a trophically transmitted parasite with a complex life cycle, over the course of its development in an intermediate host, the threespine stickleback, and the final avian host. Results from our differential gene expression analysis show major reprogramming events among developmental stages. The final host stage is characterized by a strong activation of reproductive pathways and redox homoeostasis. The attainment of infectivity in the fish intermediate host—which precedes sexual maturation in the final host and is associated with host behaviour changes—is marked by transcription of genes involved in neural pathways and sensory perception. Our results suggest that un‐annotated and S. solidus‐specific genes could play a determinant role in host–parasite molecular interactions required to complete the parasite's life cycle. Our results permit future comparative analyses to help disentangle species‐specific patterns of infection from conserved mechanisms, ultimately leading to a better understanding of the molecular control and evolution of complex life cycles.

The missing link in parasite manipulation of host behaviour

“…In order to validate this thought process, we need to have avenues, other than observation, for identifying the potential existence of manipulative factors and their source. Recently it was found in a stickleback-cestode host-parasite system that major changes in parasite gene expression occurred during the transition from the cestode’s intermediate host to its definitive host [ 14 ]. The transition from intermediate to definitive host is aided by loss of anti-predator behaviour in the intermediate host.…”

Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation

“…Recently, Hébert et al (2017) have provided a potential avenue for identifying these potential manipulation factors and their source. They found that major genome wide reprogramming events in Schistocephalus solidus (cestode) were associated in transitioning to its intermediate fish host and then to its final avian host.…”

“…Changes in gene expression in the parasite just prior to host transition (Hébert et al, 2017) suggest a rapid temporal profile for behavioral manipulation is possible, at least in this host-parasite system. Yet if a gradual temporal profile for behavioral manipulation takes place in other host-parasite systems, the rapid gene expression changes during host transition should be not be associated with potential behavioral manipulation mechanisms.…”

Temperature-induced reorganisation of Schistocephalus solidus (Cestoda) proteome during the transition to the warm-blooded host

“…The unique S. solidus protein sequences were filtered from S. solidus protein database loaded from UniProt/Swiss-Prot (access in May 2020; 43048 sequence identifiers) using the CD-HIT Suite service with 100% sequence identity cut-off settings (Huang et al, 2010). The resulting groups, consisting of synonymous names of protein sequences, were used to compare the expression of S. solidus proteins with the previously described transcriptomic (Hébert et al, 2017) and other published data (Tables S3, S4).…”

“…The transcription of S. solidus genes, which presumably provide the successful colonization of a warm-blooded host, have been previously investigated by Hébert with colleagues in the model in vitro experiment (Hébert et al, 2017). Overexpression of certain gene products has been reported either in larvae or in adult worms (the "molecular signature" of the corresponding life stage).…”