Abstract
Giardiasis, currently considered a neglected disease, is caused by the intestinal protozoan parasite Giardia duodenalis and is widely spread in human as well as domestic and wild animals. The lack of appropriate medications and the spread of resistant parasite strains urgently call for the development of novel therapeutic strategies. Host microbiota or certain probiotic strains have the capacity to provide some protection against giardiasis. By combining biological and biochemical approaches, we have been able to decipher a molecular mechanism used by the probiotic strain Lactobacillus johnsonii La1 to prevent Giardia growth in vitro. We provide evidence that the supernatant of this strain contains active principle(s) not directly toxic to Giardia but able to convert non-toxic components of bile into components highly toxic to Giardia. By using bile acid profiling, these components were identified as deconjugated bile-salts. A bacterial bile-salt-hydrolase of commercial origin was able to mimic the properties of the supernatant. Mass spectrometric analysis of the bacterial supernatant identified two of the three bile-salt-hydrolases encoded in the genome of this probiotic strain. These observations document a possible mechanism by which L. johnsonii La1, by secreting, or releasing BSH-like activity(ies) in the vicinity of replicating Giardia in an environment where bile is present and abundant, can fight this parasite. This discovery has both fundamental and applied outcomes to fight giardiasis, based on local delivery of deconjugated bile salts, enzyme deconjugation of bile components, or natural or recombinant probiotic strains that secrete or release such deconjugating activities in a compartment where both bile salts and Giardia are present.
Highlights
Giardia duodenalis is a parasitic protozoa responsible for giardiasis, a disease characterized by acute or chronic intestinal malabsorption, diarrhea, weight loss, dehydration, and abdominal pain in humans and a variety of vertebrates
After 10 h in the presence of 0.75 g/L of bovine bile, G. duodenalis trophozoite survival was slightly impacted by L. johnsonii La1 supernatant, but survival was largely affected after 24 h of contact (9.104 and 1.104 trophozoite/ml, respectively, Figure 1A, Video S2, Figure S1)
Probiotics constitute promising protective alternatives against pathogens, at least as prophylactic agents in various diseases or when used in combination with other therapeutic agents, through a variety of mechanisms relying on immunomodulation properties, competition for nutrients, and habitats, and secretion of active molecules
Summary
Giardia duodenalis is a parasitic protozoa responsible for giardiasis, a disease characterized by acute or chronic intestinal malabsorption, diarrhea, weight loss, dehydration, and abdominal pain in humans and a variety of vertebrates. It is one of the most common intestinal parasites, with 200–300 million human cases estimated worldwide per year (Lane and Lloyd, 2002). Giardia duodenalis exists under two development forms, a resistant form called cyst, responsible for the transmission of the parasite between vertebrate hosts, and an active form called trophozoite, that replicates within intestinal tracts of hosts. After encystation in the lower part of the small intestine, parasites exit the host in the feces (Lane and Lloyd, 2002; Ali and Hill, 2003; Ankarklev et al, 2010)
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