Dataset Information

Evidence for a structural role for acid-fast lipids in oocyst walls of Cryptosporidium, Toxoplasma, and Eimeria.

ABSTRACT:

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Coccidia are protozoan parasites that cause significant human disease and are of major agricultural importance. Cryptosporidium spp. cause diarrhea in humans and animals, while Toxoplasma causes disseminated infections in fetuses and untreated AIDS patients. Eimeria is a major pathogen of commercial chickens. Oocysts, which are the infectious form of Cryptosporidium and Eimeria and one of two infectious forms of Toxoplasma (the other is tissue cysts in undercooked meat), have a multilayered wall. Recently we showed that the inner layer of the oocyst walls of Toxoplasma and Eimeria is a porous scaffold of fibers of ?-1,3-glucan, which are also present in fungal walls but are absent from Cryptosporidium oocyst walls. Here we present evidence for a structural role for lipids in the oocyst walls of Cryptosporidium, Toxoplasma, and Eimeria. Briefly, oocyst walls of each organism label with acid-fast stains that bind to lipids in the walls of mycobacteria. Polyketide synthases similar to those that make mycobacterial wall lipids are abundant in oocysts of Toxoplasma and Eimeria and are predicted in Cryptosporidium. The outer layer of oocyst wall of Eimeria and the entire oocyst wall of Cryptosporidium are dissolved by organic solvents. Oocyst wall lipids are complex mixtures of triglycerides, some of which contain polyhydroxy fatty acyl chains like those present in plant cutin or elongated fatty acyl chains like mycolic acids. We propose a two-layered model of the oocyst wall (glucan and acid-fast lipids) that resembles the two-layered walls of mycobacteria (peptidoglycan and acid-fast lipids) and plants (cellulose and cutin).

Importance

Oocysts, which are essential for the fecal-oral spread of coccidia, have a wall that is thought responsible for their survival in the environment and for their transit through the stomach and small intestine. While oocyst walls of Toxoplasma and Eimeria are strengthened by a porous scaffold of fibrils of ?-1,3-glucan and by proteins cross-linked by dityrosines, both are absent from walls of Cryptosporidium. We show here that all oocyst walls are acid fast, have a rigid bilayer, dissolve in organic solvents, and contain a complex set of triglycerides rich in polyhydroxy and long fatty acyl chains that might be synthesized by an abundant polyketide synthase. These results suggest the possibility that coccidia build a waxy coat of acid-fast lipids in the oocyst wall that makes them resistant to environmental stress.

SUBMITTER: Bushkin GG

PROVIDER: S-EPMC3760245 | biostudies-literature | 2013 Sep

REPOSITORIES: biostudies-literature

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Evidence for a structural role for acid-fast lipids in oocyst walls of Cryptosporidium, Toxoplasma, and Eimeria.

Bushkin G Guy GG Motari Edwin E Carpentieri Andrea A Dubey Jitender P JP Costello Catherine E CE Robbins Phillips W PW Samuelson John J

mBio 20130903 5

<h4>Unlabelled</h4>Coccidia are protozoan parasites that cause significant human disease and are of major agricultural importance. Cryptosporidium spp. cause diarrhea in humans and animals, while Toxoplasma causes disseminated infections in fetuses and untreated AIDS patients. Eimeria is a major pathogen of commercial chickens. Oocysts, which are the infectious form of Cryptosporidium and Eimeria and one of two infectious forms of Toxoplasma (the other is tissue cysts in undercooked meat), have ...[more]

PMID: 24003177

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Project description:UnlabelledThe walls of infectious pathogens, which are essential for transmission, pathogenesis, and diagnosis, contain sugar polymers that are defining structural features, e.g., β-1,3-glucan and chitin in fungi, chitin in Entamoeba cysts, β-1,3-GalNAc in Giardia cysts, and peptidoglycans in bacteria. The goal here was to determine in which of three walled forms of Toxoplasma gondii (oocyst, sporocyst, or tissue cyst) is β-1,3-glucan, the product of glucan synthases and glucan hydrolases predicted by whole-genome sequences of the parasite. The three most important discoveries were as follows. (i) β-1,3-glucan is present in oocyst walls of Toxoplasma and Eimeria (a chicken parasite that is a model for intestinal stages of Toxoplasma) but is absent from sporocyst and tissue cyst walls. (ii) Fibrils of β-1,3-glucan are part of a trabecular scaffold in the inner layer of the oocyst wall, which also includes a glucan hydrolase that has a novel glucan-binding domain. (iii) Echinocandins, which target the glucan synthase and kill fungi, arrest development of the Eimeria oocyst wall and prevent release of the parasites into the intestinal lumen. In summary, β-1,3-glucan, which can be targeted by drugs, is an important component of oocyst walls of Toxoplasma but is not a component of sporocyst and tissue cyst walls.ImportanceWe show here that walls of Toxoplasma oocysts, the infectious stage shed by cats, contain β-1,3-glucan, a sugar polymer that is a major component of fungal walls. In contrast to fungi, β-1,3-glucan is part of a trabecular scaffold in the inner layer of the oocyst wall that is independent of the permeability barrier formed by the outer layer of the wall. While glucan synthase inhibitors kill fungi, these inhibitors arrest the development of the oocyst walls of Eimeria (an important chicken pathogen that is a surrogate for Toxoplasma) and block release of oocysts into the intestinal lumen. The absence of β-1,3-glucan in tissue cysts of Toxoplasma suggests that drugs targeted at the glucan synthase might be used to treat Eimeria in chickens but not to treat Toxoplasma in people.

Project description:Simple Summary Neospora caninum, Toxoplasma gondii, Cryptosporidium and Eimeria species are parasites of phylum Apicomplexa, which includes several protozoa affecting animals and humans. In Ecuador, the maintenance of goat health is a matter of utmost importance because it affects the economic welfare of the breeders. N. caninum and T. gondii cause reproductive problems in goats, leading to abortions or weak offspring. Severe diarrhea in kids and delays in growth are due to the Cryptosporidium and Eimeria species. Moreover, T. gondii and Cryptosporidium are zoonotic parasites with serious consequences for human health. The aim of this work was to determine, by serological and parasitological tests, the prevalence of these parasites and the risk factors for goat populations in Southern Ecuador. On some farms, the prevalence of N. caninum and T. gondii reached more than 50%; up to 17% of the kids were positive for Cryptosporidium and 90% of the goats were positive for the Eimeria species. The analysis of risk factors revealed differences according to the parasite species. Considering the zoonotic significance of these results, control and prevention measures are essential and constitute a warning to veterinarians and governmental institutions. Abstract Neospora caninum, Toxoplasma gondii, Cryptosporidium and Eimeria cause severe impacts on the productivity of goat herds. The objectives of the present study were to establish the prevalence of these apicomplexans in goat farms from Ecuador; to evaluate a rapid test for Cryptosporidium diagnosis and to identify the risk factors associated with the infections. A questionnaire was designed to obtain information from 24 goat farms from Zapotillo, Garza Real, Cazaderos, Limones and Paletillas parishes in Ecuador. Blood (n = 388) and feces (n = 391) samples were collected. Indirect ELISA and standard parasitological assays were carried out to evaluate the seroprevalence of N. caninum and T. gondii and to detect oocysts of Cryptosporidium and Eimeria. The overall prevalence values of N. caninum and T. gondii were 12.11% and 18.20%, Cryptosporidium spp. and Eimeria spp. oocysts were detected in 10.49% and 89.51% of the total samples. A low correlation value was found between the results obtained by Ziehl-Nielsen and the rapid test. The multinomial logistic regression analysis revealed that vitamin supplementation, age of diarrhea, frequency of deworming, pasture area, presence of artiodactyls, domestic fowl, administration of sulfas, age group, body condition, abortions, type of pastures and the presence of cattle were risk factors according to the parasite species.

Dataset Information

Evidence for a structural role for acid-fast lipids in oocyst walls of Cryptosporidium, Toxoplasma, and Eimeria.

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Importance

Publications

Evidence for a structural role for acid-fast lipids in oocyst walls of Cryptosporidium, Toxoplasma, and Eimeria.

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