Parasite Control

We are investigating genomes, transcriptomes and proteomes of parasitic helminths belonging to thorny-headed worms (Acanthocephala). We found energy supply and reproduction to be particularly important factors in acanthocephalan life (Schmidt et al. 2022a). Our research uncovered the molecular basis of a complex energy strategy with simultaneous respiration and fermentation in acanthocephalans (see figure below, as taken from Mauer et al. 2020). Based on these findings, we proposed acanthocephalan proteins as candidate targets for effective and specific control in fish aquaculture. This included the identification of potential deworming agents which can be tested in the acanthocephalan model (Schmidt et al. 2022b).

Parasitic Transcriptional Profiles Reflect Host Suitability

Parasitic life cycles depend on the infection of suitable hosts in which the parasites mature and reproduce. However, an individual parasite might also infect a less suitable host in which it can survive but usually does not mature and reproduce. We studied the effect of different host types on transcriptional profiles in the acanthocephalan model Pomphorhynchus laevis. In Principal Component Analysis, maturation and reproduction in the suitable host, barble, was reflected in clear separation of the datapoints giving females and males. In contrast, the datapoints representing male and female worms from an unsuitable host, European eel, clustered together. Probably, developmental arrest of most of the males and females in the eel led their transcriptional profiles appear quite similar. In only few cases, the worms continued development toward the full male or female phenotype, without having reached this state. This is the reason for the green-rimmed datapoints near the yellow-rimmed ones in the graphic below (Schmidt et al. 2022a). The comparative approach applied was useful for determining transcripts coding for essential parasite proteins.

Phylogenetic Relationships of Thorny-Headed Worms

Thorny-headed worms (Acanthocephala) are closely related with monogonont, bdelloid and seisonid wheel animals (Rotifera). However, the lineage to seisonids branches basally in part of the phylogenetic reconstructions, while seisonids group with acanthocephalans in others. According to our results, basal branching of seisonids within the Rotifera-Acanthocephala clade is an artifact resulting from long-branch attraction. The below figure may illustrate this (for the species included, see original figure in Mauer et al. 2021). The trees shown have been derived from an alignment of 100 concatenated proteins (21,042 amino acids) applying Bayesian Inference (BI). Tree topologies and node support values (100) were reproduced in Maximum Likelihood (ML) analysis. In the unrooted tree on the left, both seisonid strains cluster with a representative of remotely related Platyhelminthes. Rooting via the platyhelminth results in a basal branching of the seisonid stem line within Rotifera-Acanthocephala (not shown). However, seisonids clusters with the acanthocephalan if the tree is rooted via the Last Common Ancestor of Rotifera-Acanthocephala. We had reconstructed a corresponding sequence by ML implementing a star-like topology for Rotifera-Acanthocephala. A basal branching of monogononts, as shown on the right, was reproduced in mitochondrial and nuclear gene order analyses (Sielaff et al. 2016; Vasilikopoulos et al. 2024). In addition, the topology on the right was recovered in molecular analyses upon the implementation of measures reducing branch-length heterogeneity (Wey-Fabrizius et al. 2014; Mauer et al. 2021; see also Herlyn et al. 2003).

Phylogeny Elucidates Lifecycle Evolution of Thorny-Headed Worms

Extant thorny-headed worms (Acanthocephala) use crustaceans, myriapods and insects for larval development whereas maturation and reproduction take place in jawed vertebrates like fish, snakes, birds, and mammals. We have derived molecular phylogenies to address how the endoparasitic two-host cycle of thorny-headed worms (Acanthocephala) might have evolved. Mapping lifestyles onto the phylogenetic tree in the figure below suggests the following sequence of evolutionary changes: The first step should have been a transition from aquatic free-living (as retained in the stem lines of Monogononta and Bdelloidea) to living on an aquatic jawed arthropod (as displayed by Seisonidea). Subsequently, this first host was entered, thus establishing an endoparasitic lifestyle. Jaw-bearing vertebrates feeding on infected jawed arthropods were added later on to the acanthocephalan lifecycle (see Wey-Fabrizius et al. 2014; Herlyn 2021; Vasilikopoulos et al. 2024 etc.). Such evolutionary scenario would be a rare example of so-called upward inclusion of the second host into a complex parasite life cycle.

Expression Regulation And Why Parasites Are Not Just Simplified

We have investigated how expression regulation might have evolved on the lineage to thorny-headed worms (Acanthocephala). Across the tips of the phylogenetic tree shown below, the level of parasitism can be said to increase toward thorny-headed worms. In contrast, the repertoire of expression-regulatory microRNAs gets smaller toward Acanthocephala. This appears to reflect an enhanced loss of metazoan core genes and evolutionarily older morphological traits. In fact, parasites are known to delegate functions to their hosts. Less functions require less structures to be maintained, which necessitates less evolutionarily older genes to express these structures. Nevertheless, it would be an oversimplification to consider parasites just as simplified versions of their free-living phylogenetic relatives. On the lineage to Acanthocephala, the establishment of an endoparasitic two-host cycle went along with the emergence of an increasing number of novel traits (Herlyn et al. 2025). The most prominent example is the eponymous hooked anterior body section which enables acanthocephalans to attach to the intestinal wall of the gnathostome host.

Phenotype Evolution in Light of Molecular Trees

As foreshadowed above, our research includes morphological features too. This is exemplified in sensory structures at the base and apex of the attachment organ, the proboscis, in some acanthocephalans. Mapping the presence-absence of the sensory organs in different acanthocephalan groups on the molecular tree in the below figure suggests: Paired lateral sensory organs could have emerged in the acanthocephalan stem line (+ LSO), whereas paired apical sensory organs (+ ASOs) might have evolved in the stem line of Archiacanthocephala, followed by fusion of the paired structures to an unpaired one within the same group (ASO fusion). Reduction of lateral sensory organs might also have occured in acanthocephalan evolution (- LSO). Alternative evolutionary scenarios are possible depending on the phylogenetic relationships assumed. In any case, the presence-absence pattern of acanthocephalan sensory organs illustrates a perhaps surprizing degree of morphological plasticity in parasite evolution (Weber et al. 2013).