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Polyomic tools for an emerging livestock parasite, the rumen fluke Calicophoron daubneyi; identifying shifts in rumen functionality

BACKGROUND: 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...

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Autores principales: Huson, Kathryn M., Morphew, Russell M., Allen, Nathan R., Hegarty, Matthew J., Worgan, Hillary J., Girdwood, Susan E., Jones, Eleanor L., Phillips, Helen C., Vickers, Martin, Swain, Martin, Smith, Daniel, Kingston-Smith, Alison H., Brophy, Peter M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6278170/
https://www.ncbi.nlm.nih.gov/pubmed/30509301
http://dx.doi.org/10.1186/s13071-018-3225-6
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author Huson, Kathryn M.
Morphew, Russell M.
Allen, Nathan R.
Hegarty, Matthew J.
Worgan, Hillary J.
Girdwood, Susan E.
Jones, Eleanor L.
Phillips, Helen C.
Vickers, Martin
Swain, Martin
Smith, Daniel
Kingston-Smith, Alison H.
Brophy, Peter M.
author_facet Huson, Kathryn M.
Morphew, Russell M.
Allen, Nathan R.
Hegarty, Matthew J.
Worgan, Hillary J.
Girdwood, Susan E.
Jones, Eleanor L.
Phillips, Helen C.
Vickers, Martin
Swain, Martin
Smith, Daniel
Kingston-Smith, Alison H.
Brophy, Peter M.
author_sort Huson, Kathryn M.
collection PubMed
description BACKGROUND: 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 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. RESULTS: 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. CONCLUSIONS: The 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-018-3225-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-62781702018-12-10 Polyomic tools for an emerging livestock parasite, the rumen fluke Calicophoron daubneyi; identifying shifts in rumen functionality Huson, Kathryn M. Morphew, Russell M. Allen, Nathan R. Hegarty, Matthew J. Worgan, Hillary J. Girdwood, Susan E. Jones, Eleanor L. Phillips, Helen C. Vickers, Martin Swain, Martin Smith, Daniel Kingston-Smith, Alison H. Brophy, Peter M. Parasit Vectors Research BACKGROUND: 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 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. RESULTS: 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. CONCLUSIONS: The 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-018-3225-6) contains supplementary material, which is available to authorized users. BioMed Central 2018-12-04 /pmc/articles/PMC6278170/ /pubmed/30509301 http://dx.doi.org/10.1186/s13071-018-3225-6 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Huson, Kathryn M.
Morphew, Russell M.
Allen, Nathan R.
Hegarty, Matthew J.
Worgan, Hillary J.
Girdwood, Susan E.
Jones, Eleanor L.
Phillips, Helen C.
Vickers, Martin
Swain, Martin
Smith, Daniel
Kingston-Smith, Alison H.
Brophy, Peter M.
Polyomic tools for an emerging livestock parasite, the rumen fluke Calicophoron daubneyi; identifying shifts in rumen functionality
title Polyomic tools for an emerging livestock parasite, the rumen fluke Calicophoron daubneyi; identifying shifts in rumen functionality
title_full Polyomic tools for an emerging livestock parasite, the rumen fluke Calicophoron daubneyi; identifying shifts in rumen functionality
title_fullStr Polyomic tools for an emerging livestock parasite, the rumen fluke Calicophoron daubneyi; identifying shifts in rumen functionality
title_full_unstemmed Polyomic tools for an emerging livestock parasite, the rumen fluke Calicophoron daubneyi; identifying shifts in rumen functionality
title_short Polyomic tools for an emerging livestock parasite, the rumen fluke Calicophoron daubneyi; identifying shifts in rumen functionality
title_sort polyomic tools for an emerging livestock parasite, the rumen fluke calicophoron daubneyi; identifying shifts in rumen functionality
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6278170/
https://www.ncbi.nlm.nih.gov/pubmed/30509301
http://dx.doi.org/10.1186/s13071-018-3225-6
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