Long live the host! Proteomic analysis reveals possible strategies for parasitic manipulation of its social host

Publication type:
Journal article
Metadata:
Autoren
  • Juliane Hartke
  • Alejandro Ceron-Noriega
  • Marah Stoldt
  • Tom Sistermans
  • Marion Kever
  • Jenny Fuchs
  • Falk Butter
  • Susanne Foitzik
Autoren-URL
https://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=fis-test-1&SrcAuth=WosAPI&KeyUT=WOS:001119318900001&DestLinkType=FullRecord&DestApp=WOS_CPL
DOI
10.1111/mec.17155
eISSN
1365-294X
Externe Identifier
  • Clarivate Analytics Document Solution ID: LH6B5
  • PubMed Identifier: 37795937
ISSN
0962-1083
Ausgabe der Veröffentlichung
21
Zeitschrift
MOLECULAR ECOLOGY
Schlüsselwörter
  • ageing
  • antioxidants
  • cestode
  • intermediate host
  • lifespan
  • parasite
Paginierung
5877 - 5889
Datum der Veröffentlichung
2023
Status
Published
Titel
Long live the host! Proteomic analysis reveals possible strategies for parasitic manipulation of its social host
Sub types
  • Article
Ausgabe der Zeitschrift
32

Data source: Web of Science (Lite)

Other metadata sources:
Abstract
<jats:title>Abstract</jats:title><jats:p>Parasites with complex life cycles often manipulate the phenotype of their intermediate hosts to increase the probability of transmission to their definitive hosts. Infection with <jats:italic>Anomotaenia brevis</jats:italic>, a cestode that uses <jats:italic>Temnothorax nylanderi</jats:italic> ants as intermediate hosts, leads to a multiple‐fold extension of host lifespan and to changes in behaviour, morphology and colouration. The mechanisms behind these changes are unknown, as is whether the increased longevity is achieved through parasite manipulation. Here, we demonstrate that the parasite releases proteins into its host with functions that might explain the observed changes. These parasitic proteins make up a substantial portion of the proteome of the hosts' haemolymph, and thioredoxin peroxidase and superoxide dismutase, two antioxidants, exhibited the highest abundances among them. The largest part of the secreted proteins could not be annotated, indicating they are either novel or severely altered during recent coevolution to function in host manipulation. We also detected shifts in the hosts' proteome with infection, in particular an overabundance of vitellogenin‐like A in infected ants, a protein that regulates division of labour in <jats:italic>Temnothorax</jats:italic> ants, which could explain the observed behavioural changes. Our results thus suggest two different strategies that might be employed by this parasite to manipulate its host: secreting proteins with immediate influence on the host's phenotype and altering the host's translational activity. Our findings highlight the intricate molecular interplay required to influence the phenotype of a host and point to potential signalling pathways and genes involved in parasite–host communication.</jats:p>
Autoren
  • Juliane Hartke
  • Alejandro Ceron‐Noriega
  • Marah Stoldt
  • Tom Sistermans
  • Marion Kever
  • Jenny Fuchs
  • Falk Butter
  • Susanne Foitzik
DOI
10.1111/mec.17155
eISSN
1365-294X
ISSN
0962-1083
Ausgabe der Veröffentlichung
21
Zeitschrift
Molecular Ecology
Sprache
en
Online publication date
2023
Paginierung
5877 - 5889
Datum der Veröffentlichung
2023
Status
Published
Herausgeber
Wiley
Herausgeber URL
http://dx.doi.org/10.1111/mec.17155
Datum der Datenerfassung
2023
Titel
Long live the host! Proteomic analysis reveals possible strategies for parasitic manipulation of its social host
Ausgabe der Zeitschrift
32

Data source: Crossref

Abstract
Parasites with complex life cycles often manipulate the phenotype of their intermediate hosts to increase the probability of transmission to their definitive hosts. Infection with Anomotaenia brevis, a cestode that uses Temnothorax nylanderi ants as intermediate hosts, leads to a multiple-fold extension of host lifespan and to changes in behaviour, morphology and colouration. The mechanisms behind these changes are unknown, as is whether the increased longevity is achieved through parasite manipulation. Here, we demonstrate that the parasite releases proteins into its host with functions that might explain the observed changes. These parasitic proteins make up a substantial portion of the proteome of the hosts' haemolymph, and thioredoxin peroxidase and superoxide dismutase, two antioxidants, exhibited the highest abundances among them. The largest part of the secreted proteins could not be annotated, indicating they are either novel or severely altered during recent coevolution to function in host manipulation. We also detected shifts in the hosts' proteome with infection, in particular an overabundance of vitellogenin-like A in infected ants, a protein that regulates division of labour in Temnothorax ants, which could explain the observed behavioural changes. Our results thus suggest two different strategies that might be employed by this parasite to manipulate its host: secreting proteins with immediate influence on the host's phenotype and altering the host's translational activity. Our findings highlight the intricate molecular interplay required to influence the phenotype of a host and point to potential signalling pathways and genes involved in parasite-host communication.
Addresses
  • Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Mainz, Germany.
Autoren
  • Juliane Hartke
  • Alejandro Ceron-Noriega
  • Marah Stoldt
  • Tom Sistermans
  • Marion Kever
  • Jenny Fuchs
  • Falk Butter
  • Susanne Foitzik
DOI
10.1111/mec.17155
eISSN
1365-294X
Externe Identifier
  • PubMed Identifier: 37795937
Funding acknowledgements
  • Deutsche Forschungsgemeinschaft: GRK2526/1
Open access
false
ISSN
0962-1083
Ausgabe der Veröffentlichung
21
Zeitschrift
Molecular ecology
Schlüsselwörter
  • Animals
  • Ants
  • Cestoda
  • Parasites
  • Proteome
  • Proteomics
  • Host-Parasite Interactions
Sprache
eng
Medium
Print-Electronic
Online publication date
2023
Paginierung
5877 - 5889
Datum der Veröffentlichung
2023
Status
Published
Publisher licence
CC BY-NC-ND
Datum der Datenerfassung
2023
Titel
Long live the host! Proteomic analysis reveals possible strategies for parasitic manipulation of its social host.
Sub types
  • Journal Article
Ausgabe der Zeitschrift
32

Data source: Europe PubMed Central

Abstract
Parasites with complex life cycles often manipulate the phenotype of their intermediate hosts to increase the probability of transmission to their definitive hosts. Infection with Anomotaenia brevis, a cestode that uses Temnothorax nylanderi ants as intermediate hosts, leads to a multiple-fold extension of host lifespan and to changes in behaviour, morphology and colouration. The mechanisms behind these changes are unknown, as is whether the increased longevity is achieved through parasite manipulation. Here, we demonstrate that the parasite releases proteins into its host with functions that might explain the observed changes. These parasitic proteins make up a substantial portion of the proteome of the hosts' haemolymph, and thioredoxin peroxidase and superoxide dismutase, two antioxidants, exhibited the highest abundances among them. The largest part of the secreted proteins could not be annotated, indicating they are either novel or severely altered during recent coevolution to function in host manipulation. We also detected shifts in the hosts' proteome with infection, in particular an overabundance of vitellogenin-like A in infected ants, a protein that regulates division of labour in Temnothorax ants, which could explain the observed behavioural changes. Our results thus suggest two different strategies that might be employed by this parasite to manipulate its host: secreting proteins with immediate influence on the host's phenotype and altering the host's translational activity. Our findings highlight the intricate molecular interplay required to influence the phenotype of a host and point to potential signalling pathways and genes involved in parasite-host communication.
Date of acceptance
2023
Autoren
  • Juliane Hartke
  • Alejandro Ceron-Noriega
  • Marah Stoldt
  • Tom Sistermans
  • Marion Kever
  • Jenny Fuchs
  • Falk Butter
  • Susanne Foitzik
Autoren-URL
https://www.ncbi.nlm.nih.gov/pubmed/37795937
DOI
10.1111/mec.17155
eISSN
1365-294X
Funding acknowledgements
  • Deutsche Forschungsgemeinschaft: GRK2526/1
Ausgabe der Veröffentlichung
21
Zeitschrift
Mol Ecol
Schlüsselwörter
  • ageing
  • antioxidants
  • cestode
  • intermediate host
  • lifespan
  • parasite
  • Animals
  • Parasites
  • Host-Parasite Interactions
  • Proteome
  • Proteomics
  • Cestoda
  • Ants
Sprache
eng
Country
England
Paginierung
5877 - 5889
Datum der Veröffentlichung
2023
Status
Published
Datum, an dem der Datensatz öffentlich gemacht wurde
2023
Titel
Long live the host! Proteomic analysis reveals possible strategies for parasitic manipulation of its social host.
Sub types
  • Journal Article
Ausgabe der Zeitschrift
32

Data source: PubMed

Author's licence
CC-BY-NC-ND
Autoren
  • Juliane Hartke
  • Alejandro Ceron-Noriega
  • Marah Stoldt
  • Tom Sistermans
  • Marion Kever
  • Jenny Fuchs
  • Falk Butter
  • Susanne Foitzik
Hosting institution
Universitätsbibliothek Mainz
Sammlungen
  • DFG-491381577-H
Resource version
Published version
DOI
10.1111/mec.17155
File(s) embargoed
false
Open access
true
ISSN
0962-1083
Ausgabe der Veröffentlichung
21
Zeitschrift
Molecular ecology
Schlüsselwörter
  • 570 Biowissenschaften
  • 570 Life sciences
Sprache
eng
Open access status
Open Access
Paginierung
5877 - 5889
Datum der Veröffentlichung
2023
Public URL
https://openscience.ub.uni-mainz.de/handle/20.500.12030/9755
Herausgeber
Wiley-Blackwell
Datum der Datenerfassung
2023
Datum, an dem der Datensatz öffentlich gemacht wurde
2023
Zugang
Public
Titel
Long live the host! Proteomic analysis reveals possible strategies for parasitic manipulation of its social host
Ausgabe der Zeitschrift
32

Files

long_live_the_host_proteomic_-20231201123836363.pdf

Data source: OPENSCIENCE.UB

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