The principal investigator in the project was Albina Tsekova, Researcher at the Laboratory of Ecological Biochemistry, Institute of Biology KarRC RAS. In 2024, the scientist was awarded a medal of the Russian Academy of Sciences for her research of such adaptations.
– Unpacking the molecular mechanisms of host-parasite interactions is a basic task for parasitology. These relationships are an evolutionary arms race: the parasite wants to secure nutrients and evade the host's immune defense, while the host needs to mitigate the harmful effects of the invasion, – explains Albina Tsekova.
In this study, the biologists focused on the bream (Abramis brama) and the tapeworm Ligula intestinalis – a widespread parasite of cyprinid fishes, which grows and develops inside the host's body cavity. Over its life cycle, Ligula successively exploits three hosts: first a crustacean, then a fish, and finally a piscivorous bird. Although this host-parasite pair is considered a common model for investigating the various aspects of parasitology, the molecular dimension of their interaction has remained poorly studied.
Tapeworm Ligula intestinalis – a widespread parasite of Cyprinid fishes
Healthy and infected breams were captured in Lake Syamozero (Karelia). The researchers took swabs from the body surface of parasites and from the abdominal cavity of the fish, i.e. from the host-parasite contact zone, and performed a proteomic analysis of the samples. This included mass-spectrometric determination of the molecules in the swabs, followed by identification of the detected proteins, and their statistical and functional analysis.
The proteomic analysis of swabs from the parasite body surface revealed nearly 3,500 amino acid sequences, with a comparable number for fish abdominal cavity. Having analyzed them, the scientists detected both the parasite’s and the host’s proteins on the surface of the Ligula worms, indicating active molecular interaction.
– Our findings suggest that the parasite may not be a passive tenant of the bream, but rather an active manipulator that modulates the host's metabolism to facilitate immune evasion and nutrient acquisition, – shared Albina Tsekova.
Among the host-derived proteins found on the Ligula body there were key immune factors that may help the parasite avoid being recognized by the immune system of the fish. It is possible, for instance, that Ligula may camouflage its own antigens to resemble the host’s "self" molecules. The study also revealed that the parasite can control nutrient availability to the host, thus regulating its own metabolism and development.
Ligula grows and develops in the host fish body cavity
Proteomic analysis of swabs from the abdominal cavity of infected breams detected proteins different from those in uninfected fish. These differences reflect active interaction between the parasite and the host's immune system. In particular, a complex protein profile identified in the parasite was geared toward enabling successful invasion and prolonged parasitism within the fish.
The researchers were especially excited by the finding that swabs from the infected fish contained acetylcholinesterase – the enzyme that breaks down the neurotransmitter acetylcholine, which sustains alertness and nervous system activity. Acetylcholine decline leads to a weaker neuromuscular transmission, making the fish languid and less cautious. This likely explains why infected fish can be seen very close to water surface. They are not as responsive to danger as healthy individuals. This improves Ligula’s chances of completing the life cycle: a sluggish fish is easier for birds to catch. Inside the intestine of a gull, the parasite matures and begins releasing eggs, which then fall into water with the birds' droppings, are consumed by crustaceans, which are then eaten by fish – looping the cycle.
– This study provides new insights into the key molecular aspects of host-parasite interaction. We have demonstrated a dynamic and bidirectional interaction, which likely perpetuates the infection. The data can be applied to find target proteins when developing veterinary, diagnostic, and anthelmintic drugs, – summarized Albina Tsekova.
Research team of the Institute of Biology KarRC RAS investigating fish-parasite relationships in Lake Syamozero
The results of the study were published in the international journal Molecular Biology Reports and Parasitology.
Previously, biochemists and parasitologists of the KarRC RAS explored the effects of ligula infection on the condition and dietary value of breams. The analysis showed that, being safe for humans, this parasite does not significantly affect the fish quality either.
Photos provided by IB KarRC RAS staff
