Surviving in the fish gut: Comparative inhibitory capacities against the host proteinases in cestodes of the genus Proteocephalus

Abstract

Currently, little is known about inhibitory substances enabling tapeworms to settle in fish intestines thereby avoiding proteolysis. Contrary to previous studies with certain host–parasite pairs, this research compares the inhibitory capacities in three tapeworm species of the same genus Proteocephalus from four different fishes (P. torulosus from dace and zope, P. sagittus from stone loach and P. cernuae from ruffe). The tapeworm extracts studied significantly reduced the activity of commercial trypsin (although to a lesser degree than the synthetic inhibitor of serine proteinases PMSF), displaying clear inter‐specific variation in worms’ inhibitory ability. We also measured the proteolytic activity of the host intestinal mucosa exposed to tapeworm extracts which served as inhibitors. Based on per cent inhibition values, all tapeworm extracts significantly suppressed the mucosal proteolytic activity, with marked differences between certain host–parasite pairs. SDS‐PAGE electrophoresis of the incubation media and extracts detected in each tapeworm species 20–36 protein bands with apparent molecular weights from 10–12 to 312.5 kDa, mostly below 50 kDa. The incubation medium and extract of each parasite shared one to six bands ranging from 12 to 35 kDa, depending on its species, with only four bands common for two or more species. The band profiles suggest that in various Proteocephalus species inhibitory capacities against host proteinases can be ensured by different proteins.

Two proteocephalid cestodes in the fish Malapterurus electricus and Heterobranchus bidorsalis from Lake Nasser, Egypt: a morphological, molecular, and histopathological study

“…For example, Eubothrium rugosum secretes proteinase inhibitor that inactivates the digestive enzymes of its host burbot ( Lota lota ) [ 43 ]. Similar finding were reported by Izvekova et al [ 44 ] on several mechanisms performed by cestodes to protect its tegument from the powerful digestive enzymes. Whether or not the increased thickness of the Proteocephalus sp.…”

First insights into the activity of major digestive enzymes in the intestine of the European catfish Silurus glanis and protective anti‐enzymatic potential of its gut parasite Silurotaenia siluri

“…To prepare a homogenate of the catfish intestinal mucosa, the mucous membrane was removed from the anterior part (5–10 cm) of the intestine using a plastic spatula; cleared of chyme; and then homogenized, diluted and centrifuged as detailed earlier (Izvekova et al, 2022). After the intestines in fish infected with cestodes S. siluri were dissected, helminths were removed using forceps and thoroughly rinsed in three consecutive 10 ml portions of Ringer's solution for cold‐blooded animals to remove the host enzymes from the tegument surface.…”

“…It is known that protease inhibitors are of protein nature (Rawlings et al, 2004), so the amount of protein is certainly reflected in the inhibitory effects. By now, large factual material has been accumulated on the effect of cestodes on the proteolytic activity of their definitive host fish, including the ability of helminths to inhibit this activity (Izvekova et al, 2011(Izvekova et al, , 2022. The fact that the incubation medium and S. siluri extract much more effectively inhibit the activity of trypsin and chymotrypsin than the total proteolytic activity of the catfish intestinal mucosa indicates a greater specificity of tapeworm inhibitors towards trypsin and chymotrypsin.…”

“…At the same time, metazoan parasites are known as common natural stressors of freshwater and marine organisms, which can affect host physiology and population structure (Morley, 2019). Thus, some cestode species reportedly influence the activity of digestive enzymes of their host fishes (Izvekova et al, 2011(Izvekova et al, , 2022.…”