Dataset Information

Modulation of Rumen Microbes Through Extracellular Vesicle Released by the Rumen Fluke Calicophoron daubneyi.

ABSTRACT: Parasite derived extracellular vesicles (EVs) have been proposed to play key roles in the establishment and maintenance of infection. Calicophoron daubneyi is a newly emerging parasite of livestock with many aspects of its underpinning biology yet to be resolved. This research is the first in-depth investigation of EVs released by adult C. daubneyi. EVs were successfully isolated using both differential centrifugation and size exclusion chromatography (SEC), and morphologically characterized though transmission electron microscopy (TEM). EV protein components were characterized using a GeLC approach allowing the elucidation of comprehensive proteomic profiles for both their soluble protein cargo and surface membrane bound proteins yielding a total of 378 soluble proteins identified. Notably, EVs contained Sigma-class GST and cathepsin L and B proteases, which have previously been described in immune modulation and successful establishment of parasitic flatworm infections. SEC purified C. daubneyi EVs were observed to modulate rumen bacterial populations by likely increasing microbial species diversity via antimicrobial activity. This data indicates EVs released from adult C. daubneyi have a role in establishment within the rumen through the regulation of microbial populations offering new routes to control rumen fluke infection and to develop molecular strategies to improve rumen efficiency.

SUBMITTER: Allen NR

PROVIDER: S-EPMC8096352 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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Modulation of Rumen Microbes Through Extracellular Vesicle Released by the Rumen Fluke Calicophoron daubneyi.

Allen Nathan R NR Taylor-Mew Aspen R AR Wilkinson Toby J TJ Huws Sharon S Phillips Helen H Morphew Russell M RM Brophy Peter M PM

Frontiers in cellular and infection microbiology 20210420

Parasite derived extracellular vesicles (EVs) have been proposed to play key roles in the establishment and maintenance of infection. Calicophoron daubneyi is a newly emerging parasite of livestock with many aspects of its underpinning biology yet to be resolved. This research is the first in-depth investigation of EVs released by adult C. daubneyi. EVs were successfully isolated using both differential centrifugation and size exclusion chromatography (SEC), and morphologically cha ...[more]

PMID: 33959516

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Project description:BackgroundDiseases caused by parasitic flatworms of rumen tissues (paramphistomosis) are a significant threat to global food security as a cause of morbidity and mortality in ruminant livestock in subtropical and tropical climates. Calicophoron daubneyi is currently the only paramphistome species commonly infecting ruminant livestock in temperate European climates. However, recorded incidences of C. daubneyi infection in European livestock have been increasing over the last decade. Whilst clinical paramphistomosis caused by adult worms has not been confirmed in Europe, fatalities have been attributed to severe haemorrhagic enteritis of the small intestine resulting from the migration of immature paramphistomes. Large numbers of mature adults can reside in the rumen, yet to date, the impact on rumen fermentation, and consequently on productivity and economic management of infected livestock, have not been resolved. Limited publicly available nucleotide and protein sequences for C. daubneyi underpin this lack of biological and economic understanding. Here we present for the first time a de novo assembled transcriptome, with functional annotations, for adult C. daubneyi, which provides a reference database for protein and nucleotide sequence identification to facilitate fundamental biology, anthelmintic, vaccine and diagnostics discoveries.ResultsThis dataset identifies a number of genes potentially unique to C. daubneyi and, by comparison to an existing transcriptome for the related Paramphistomum cervi, identifies novel genes which may be unique to the paramphistome group of platyhelminthes. Additionally, we present the first coverage of the excretory/secretory and soluble somatic proteome profiles for adult C. daubneyi and identify the release of extracellular vesicles from adult C. daubneyi parasites during in vitro, ex-host culture. Finally, we have performed the first analysis of rumen fluke impacting upon rumen fermentation parameters using an in vitro gas production study resulting in a significant increase in propionate production.ConclusionsThe resulting data provide a discovery platform (transcriptome, proteomes, EV isolation pipeline and in vitro fermentation system) to further study C. daubneyi-host interaction. In addition, the acetate: propionate ratio has been demonstrated to decrease with rumen fluke infection suggesting that acidotic conditions in the rumen may occur.

Project description:Diseases caused by parasitic flatworms of rumen tissues (paramphistomosis) are a significant threat to global food security as a cause of morbidity and mortality in ruminant livestock in subtropical and tropical climates. Calicophoron daubneyi is currently the only paramphistome species commonly infecting livestock species in temperate European climates. However, recorded incidences of C. daubneyi infection in European livestock have been increasing over the last decade. Whilst clinical paramphistomosis caused by adult worms is currently uncommon in Europe, fatalities have been reported in association with severe haemorrhagic enteritis resulting from the migration of immature paramphistomes. Large numbers of mature adults can reside in the rumen, yet to date, the impact on rumen fermentation, and consequently in productivity and economic management of infected livestock have not been resolved. Limited public available nucleotide and protein sequences for C. daubneyi underpin this lack of biological and economic understanding. Here we present for the first time a de novo assembled transcriptome, with functional annotations, for adult C. daubneyi, which provides a reference database for protein and nucleotide sequence identification to facilitate fundamental biology, anthelmintic, vaccine and diagnostics discoveries. This dataset identifies a number of genes potentially unique to C. daubneyi and, by comparison to an existing transcriptome for the related Paramphistomum cervi, identifies novel genes which may be unique to the paramphistome group of platyhelminthes. Additionally, we present the first coverage of the excretory/secretory and soluble somatic proteome profiles for adult C. daubneyi and identify the release of extracellular vesicles from adult C. daubneyi parasites during in vitro, ex-host culture. Finally, we have performed the first analysis of rumen fluke impacting upon rumen fermentation parameters using an in vitro gas production study resulting in a significant increase in propionate production.

Project description:Calicophoron daubneyi infections have increased in Europe, being more frequent than fasciolosis in some areas. Infection occurs once definitive hosts ingest encysted metacercariae present on vegetation. Following excystation, juvenile flukes penetrate the small intestinal mucosa and migrate into the rumen where adults mature. Throughout the somatic migration, juveniles come across different microenvironments and tissues and encounter host leukocytes. Besides phagocytosis, production of reactive oxygen species (ROS) and degranulation, polymorphonuclear neutrophils also cast neutrophil extracellular traps (NETs), which can entrap several parasite species, including the closely related liver fluke Fasciola hepatica. In this study, we analyzed whether in vitro exposure of bovine neutrophils to C. daubneyi antigen (CdAg) and eggs triggered neutrophils activation and NET formation. Results on scanning electron microscopy (SEM) and immunofluorescence analyses show weak formation of short spread NETs upon CdAg stimulation, corroborated by increased extracellular DNA measurements. Likewise, early NETosis was confirmed via nuclear area expansion assays. Bovine neutrophil stimulation with CdAg 100 µg/mL concentration led to a significant increase in oxygen consumption rates (p = 0.0152) and extracellular acidification rates (p = 0.0022), while lower concentrations of CdAg (10 µg/mL) failed to induce neutrophil activation, suggesting a dose dependent response. Both intra- and extracellular ROS production was not affected by any CdAg concentration here studied. Bovine neutrophil total adenosine triphosphate concentration significantly decreased after exposure to CdAg 100 µg/mL, in line to the observed with the positive control (phorbol myristate acetate/ionomycin). In summary, C. daubneyi activates bovine neutrophils with rather weak responses, which might suggest that the release of C. daubneyi-specific molecules (i.e. excretory-secretory antigens, proteases, or nucleases) could interfere with neutrophil-related effector mechanisms. Further ex vivo analyses will clarify if such mechanisms are also involved in pathogenesis of paramphistomosis by demonstrating neutrophil recruitment into affected intestinal mucosa.

Dataset Information

Modulation of Rumen Microbes Through Extracellular Vesicle Released by the Rumen Fluke Calicophoron daubneyi.

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Modulation of Rumen Microbes Through Extracellular Vesicle Released by the Rumen Fluke <i>Calicophoron daubneyi</i>.

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