Host-dependent impairment of parasite development and reproduction in the acanthocephalan model

Publikationstyp:
Zeitschriftenaufsatz
Metadaten:
Autoren
  • Hanno Schmidt
  • Katharina Mauer
  • Thomas Hankeln
  • Holger Herlyn
Autoren-URL
https://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=fis-test-1&SrcAuth=WosAPI&KeyUT=WOS:000804043700006&DestLinkType=FullRecord&DestApp=WOS_CPL
DOI
10.1186/s13578-022-00818-2
eISSN
2045-3701
Externe Identifier
  • Clarivate Analytics Document Solution ID: 1S4TD
  • PubMed Identifier: 35642000
Ausgabe der Veröffentlichung
1
Zeitschrift
CELL AND BIOSCIENCE
Schlüsselwörter
  • Gene expression
  • Reproduction
  • Energy metabolism
  • Immune response
  • Eel
  • Barbel
  • RNA-Seq
  • Schistosoma
  • Nematoda
  • Cestoda
Artikelnummer
ARTN 75
Datum der Veröffentlichung
2022
Status
Published
Titel
Host-dependent impairment of parasite development and reproduction in the acanthocephalan model
Sub types
  • Article
Ausgabe der Zeitschrift
12

Datenquelle: Web of Science (Lite)

Andere Metadatenquellen:
Abstract
<jats:title>Abstract</jats:title><jats:sec> <jats:title>Background</jats:title> <jats:p>A central question in parasitology is why parasites mature and reproduce in some host species but not in others. Yet, a better understanding of the inability of parasites to complete their life cycles in less suitable hosts may hold clues for their control. To shed light on the molecular basis of parasite (non-)maturation, we analyzed transcriptomes of thorny-headed worms (Acanthocephala: <jats:italic>Pomphorhynchus laevis</jats:italic>), and compared developmentally arrested worms excised from European eel (<jats:italic>Anguilla anguilla</jats:italic>) to developmentally unrestricted worms from barbel (<jats:italic>Barbus barbus</jats:italic>).</jats:p> </jats:sec><jats:sec> <jats:title>Results</jats:title> <jats:p>Based on 20 RNA-Seq datasets, we demonstrate that transcriptomic profiles are more similar between <jats:italic>P. laevis</jats:italic> males and females from eel than between their counterparts from barbel. Impairment of sexual phenotype development was reflected in gene ontology enrichment analyses of genes having differential transcript abundances. Genes having reproduction- and energy-related annotations were found to be affected by parasitizing either eel or barbel. According to this, the molecular machinery of male and female acanthocephalans from the eel is less tailored to reproduction and more to coping with the less suitable environment provided by this host. The pattern was reversed in their counterparts from the definitive host, barbel.</jats:p> </jats:sec><jats:sec> <jats:title>Conclusions</jats:title> <jats:p>Comparative analysis of transcriptomes of developmentally arrested and reproducing parasites elucidates the challenges parasites encounter in hosts which are unsuitable for maturation and reproduction. By studying a gonochoric species, we were also able to highlight sex-specific traits. In fact, transcriptomic evidence for energy shortage in female acanthocephalans associates with their larger body size. Thus, energy metabolism and glycolysis should be promising targets for the treatment of acanthocephaliasis. Although inherently enabling a higher resolution in heterosexuals, the comparison of parasites from definitive hosts and less suitable hosts, in which the parasites merely survive, should be applicable to hermaphroditic helminths. This may open new perspectives in the control of other helminth pathogens of humans and livestock.</jats:p> </jats:sec>
Autoren
  • Hanno Schmidt
  • Katharina Mauer
  • Thomas Hankeln
  • Holger Herlyn
DOI
10.1186/s13578-022-00818-2
eISSN
2045-3701
Ausgabe der Veröffentlichung
1
Zeitschrift
Cell &amp; Bioscience
Sprache
en
Artikelnummer
75
Online publication date
2022
Status
Published online
Herausgeber
Springer Science and Business Media LLC
Herausgeber URL
http://dx.doi.org/10.1186/s13578-022-00818-2
Datum der Datenerfassung
2022
Titel
Host-dependent impairment of parasite development and reproduction in the acanthocephalan model
Ausgabe der Zeitschrift
12

Datenquelle: Crossref

Abstract
<h4>Background</h4>A central question in parasitology is why parasites mature and reproduce in some host species but not in others. Yet, a better understanding of the inability of parasites to complete their life cycles in less suitable hosts may hold clues for their control. To shed light on the molecular basis of parasite (non-)maturation, we analyzed transcriptomes of thorny-headed worms (Acanthocephala: Pomphorhynchus laevis), and compared developmentally arrested worms excised from European eel (Anguilla anguilla) to developmentally unrestricted worms from barbel (Barbus barbus).<h4>Results</h4>Based on 20 RNA-Seq datasets, we demonstrate that transcriptomic profiles are more similar between P. laevis males and females from eel than between their counterparts from barbel. Impairment of sexual phenotype development was reflected in gene ontology enrichment analyses of genes having differential transcript abundances. Genes having reproduction- and energy-related annotations were found to be affected by parasitizing either eel or barbel. According to this, the molecular machinery of male and female acanthocephalans from the eel is less tailored to reproduction and more to coping with the less suitable environment provided by this host. The pattern was reversed in their counterparts from the definitive host, barbel.<h4>Conclusions</h4>Comparative analysis of transcriptomes of developmentally arrested and reproducing parasites elucidates the challenges parasites encounter in hosts which are unsuitable for maturation and reproduction. By studying a gonochoric species, we were also able to highlight sex-specific traits. In fact, transcriptomic evidence for energy shortage in female acanthocephalans associates with their larger body size. Thus, energy metabolism and glycolysis should be promising targets for the treatment of acanthocephaliasis. Although inherently enabling a higher resolution in heterosexuals, the comparison of parasites from definitive hosts and less suitable hosts, in which the parasites merely survive, should be applicable to hermaphroditic helminths. This may open new perspectives in the control of other helminth pathogens of humans and livestock.
Addresses
  • Anthropology, Institute of Organismic and Molecular Evolution (iomE), Johannes Gutenberg University Mainz, Mainz, Germany. hannoschmidt@gmx.de.
Autoren
  • Hanno Schmidt
  • Katharina Mauer
  • Thomas Hankeln
  • Holger Herlyn
DOI
10.1186/s13578-022-00818-2
eISSN
2045-3701
Externe Identifier
  • PubMed Identifier: 35642000
  • PubMed Central ID: PMC9153150
Funding acknowledgements
  • Deutsche Forschungsgemeinschaft: HE 3487/5-1
  • Deutsche Forschungsgemeinschaft: HE 3487/5–1
  • Johannes Gutenberg-Universität Mainz:
Open access
true
ISSN
2045-3701
Ausgabe der Veröffentlichung
1
Zeitschrift
Cell & bioscience
Sprache
eng
Medium
Electronic
Online publication date
2022
Open access status
Open Access
Paginierung
75
Datum der Veröffentlichung
2022
Status
Published
Publisher licence
CC BY
Datum der Datenerfassung
2022
Titel
Host-dependent impairment of parasite development and reproduction in the acanthocephalan model.
Sub types
  • research-article
  • Journal Article
Ausgabe der Zeitschrift
12

Files

https://cellandbioscience.biomedcentral.com/counter/pdf/10.1186/s13578-022-00818-2 https://europepmc.org/articles/PMC9153150?pdf=render

Datenquelle: Europe PubMed Central

Abstract
BACKGROUND: A central question in parasitology is why parasites mature and reproduce in some host species but not in others. Yet, a better understanding of the inability of parasites to complete their life cycles in less suitable hosts may hold clues for their control. To shed light on the molecular basis of parasite (non-)maturation, we analyzed transcriptomes of thorny-headed worms (Acanthocephala: Pomphorhynchus laevis), and compared developmentally arrested worms excised from European eel (Anguilla anguilla) to developmentally unrestricted worms from barbel (Barbus barbus). RESULTS: Based on 20 RNA-Seq datasets, we demonstrate that transcriptomic profiles are more similar between P. laevis males and females from eel than between their counterparts from barbel. Impairment of sexual phenotype development was reflected in gene ontology enrichment analyses of genes having differential transcript abundances. Genes having reproduction- and energy-related annotations were found to be affected by parasitizing either eel or barbel. According to this, the molecular machinery of male and female acanthocephalans from the eel is less tailored to reproduction and more to coping with the less suitable environment provided by this host. The pattern was reversed in their counterparts from the definitive host, barbel. CONCLUSIONS: Comparative analysis of transcriptomes of developmentally arrested and reproducing parasites elucidates the challenges parasites encounter in hosts which are unsuitable for maturation and reproduction. By studying a gonochoric species, we were also able to highlight sex-specific traits. In fact, transcriptomic evidence for energy shortage in female acanthocephalans associates with their larger body size. Thus, energy metabolism and glycolysis should be promising targets for the treatment of acanthocephaliasis. Although inherently enabling a higher resolution in heterosexuals, the comparison of parasites from definitive hosts and less suitable hosts, in which the parasites merely survive, should be applicable to hermaphroditic helminths. This may open new perspectives in the control of other helminth pathogens of humans and livestock.
Date of acceptance
2022
Autoren
  • Hanno Schmidt
  • Katharina Mauer
  • Thomas Hankeln
  • Holger Herlyn
Autoren-URL
https://www.ncbi.nlm.nih.gov/pubmed/35642000
DOI
10.1186/s13578-022-00818-2
Externe Identifier
  • PubMed Central ID: PMC9153150
Funding acknowledgements
  • Deutsche Forschungsgemeinschaft: HE 3487/5-1
ISSN
2045-3701
Ausgabe der Veröffentlichung
1
Zeitschrift
Cell Biosci
Schlüsselwörter
  • Barbel
  • Cestoda
  • Eel
  • Energy metabolism
  • Gene expression
  • Immune response
  • Nematoda
  • RNA-Seq
  • Reproduction
  • Schistosoma
Sprache
eng
Country
England
Paginierung
75
PII
10.1186/s13578-022-00818-2
Datum der Veröffentlichung
2022
Status
Published online
Titel
Host-dependent impairment of parasite development and reproduction in the acanthocephalan model.
Sub types
  • Journal Article
Ausgabe der Zeitschrift
12

Datenquelle: PubMed

Author's licence
CC-BY
Autoren
  • Hanno Schmidt
  • Katharina Mauer
  • Thomas Hankeln
  • Holger Herlyn
Hosting institution
Universitätsbibliothek Mainz
Sammlungen
  • DFG-491381577-G
Resource version
Published version
DOI
10.1186/s13578-022-00818-2
Funding acknowledgements
  • Gefördert durch die Deutsche Forschungsgemeinschaft (DFG) - Projektnummer 491381577
File(s) embargoed
false
Open access
true
ISSN
2045-3701
Zeitschrift
Cell & bioscience
Schlüsselwörter
  • 570 Biowissenschaften
  • 570 Life sciences
Sprache
eng
Open access status
Open Access
Paginierung
75
Datum der Veröffentlichung
2022
Public URL
https://openscience.ub.uni-mainz.de/handle/20.500.12030/8185
Herausgeber
BioMed Central
Datum der Datenerfassung
2022
Datum, an dem der Datensatz öffentlich gemacht wurde
2022
Zugang
Public
Titel
Host-dependent impairment of parasite development and reproduction in the acanthocephalan model
Ausgabe der Zeitschrift
12

Files

hostdependent_impairment__of_-20221025122817664.pdf

Datenquelle: OPENSCIENCE.UB

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