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

Abstract 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...

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Main Authors: Kathryn M. Huson, Russell M. Morphew, Nathan R. Allen, Matthew J. Hegarty, Hillary J. Worgan, Susan E. Girdwood, Eleanor L. Jones, Helen C. Phillips, Martin Vickers, Martin Swain, Daniel Smith, Alison H. Kingston-Smith, Peter M. Brophy
Format: Article
Language:English
Published: BMC 2018-12-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-018-3225-6
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language English
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author Kathryn M. Huson
Russell M. Morphew
Nathan R. Allen
Matthew J. Hegarty
Hillary J. Worgan
Susan E. Girdwood
Eleanor L. Jones
Helen C. Phillips
Martin Vickers
Martin Swain
Daniel Smith
Alison H. Kingston-Smith
Peter M. Brophy
spellingShingle Kathryn M. Huson
Russell M. Morphew
Nathan R. Allen
Matthew J. Hegarty
Hillary J. Worgan
Susan E. Girdwood
Eleanor L. Jones
Helen C. Phillips
Martin Vickers
Martin Swain
Daniel Smith
Alison H. Kingston-Smith
Peter M. Brophy
Polyomic tools for an emerging livestock parasite, the rumen fluke Calicophoron daubneyi; identifying shifts in rumen functionality
Parasites & Vectors
Calicophoron daubneyi
Transcriptome
Paramphistome
Proteomics
In vitro
Rumen fermentation
author_facet Kathryn M. Huson
Russell M. Morphew
Nathan R. Allen
Matthew J. Hegarty
Hillary J. Worgan
Susan E. Girdwood
Eleanor L. Jones
Helen C. Phillips
Martin Vickers
Martin Swain
Daniel Smith
Alison H. Kingston-Smith
Peter M. Brophy
author_sort Kathryn M. Huson
title 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_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_sort polyomic tools for an emerging livestock parasite, the rumen fluke calicophoron daubneyi; identifying shifts in rumen functionality
publisher BMC
series Parasites & Vectors
issn 1756-3305
publishDate 2018-12-01
description Abstract 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.
topic Calicophoron daubneyi
Transcriptome
Paramphistome
Proteomics
In vitro
Rumen fermentation
url http://link.springer.com/article/10.1186/s13071-018-3225-6
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spelling doaj-d85a5d9391ba4d0fa0f277680a2ae7bb2020-11-25T01:27:48ZengBMCParasites & Vectors1756-33052018-12-0111112210.1186/s13071-018-3225-6Polyomic tools for an emerging livestock parasite, the rumen fluke Calicophoron daubneyi; identifying shifts in rumen functionalityKathryn M. Huson0Russell M. Morphew1Nathan R. Allen2Matthew J. Hegarty3Hillary J. Worgan4Susan E. Girdwood5Eleanor L. Jones6Helen C. Phillips7Martin Vickers8Martin Swain9Daniel Smith10Alison H. Kingston-Smith11Peter M. Brophy12Institute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisInstitute of Biological, Environmental & Rural Sciences (IBERS), Aberystwyth University, PenglaisAbstract 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.http://link.springer.com/article/10.1186/s13071-018-3225-6Calicophoron daubneyiTranscriptomeParamphistomeProteomicsIn vitroRumen fermentation