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

View ORCID ProfileJuliane Hartke, Alejandro Ceron-Noriega, Marah Stoldt, Tom Sistermans, Marion Kever, Jenny Fuchs, Falk Butter, Susanne Foitzik
doi: https://doi.org/10.1101/2022.12.23.521666
Juliane Hartke
1Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Germany
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  • For correspondence: juliane.hartke@gmail.com
Alejandro Ceron-Noriega
2Institute of Molecular Biology, Mainz, Germany
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Marah Stoldt
1Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Germany
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Tom Sistermans
1Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Germany
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Marion Kever
1Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Germany
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Jenny Fuchs
1Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Germany
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Falk Butter
2Institute of Molecular Biology, Mainz, Germany
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Susanne Foitzik
1Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Germany
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Abstract

Parasites with complex lifecycles 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 point at two different strategies likely employed by this parasite to manipulate its host – by secretion of proteins with immediate influence on the host’s phenotype and by altering the host’s translational activity. Our findings reveal the intricate molecular interplay required to influence the phenotype of a host and shed light on potential signalling pathways and genes involved in parasite-host communication.

Competing Interest Statement

The authors have declared no competing interest.

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Posted May 22, 2023.
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Long live the host! Proteomic analysis reveals possible strategies for parasitic manipulation of its social host
Juliane Hartke, Alejandro Ceron-Noriega, Marah Stoldt, Tom Sistermans, Marion Kever, Jenny Fuchs, Falk Butter, Susanne Foitzik
bioRxiv 2022.12.23.521666; doi: https://doi.org/10.1101/2022.12.23.521666
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Long live the host! Proteomic analysis reveals possible strategies for parasitic manipulation of its social host
Juliane Hartke, Alejandro Ceron-Noriega, Marah Stoldt, Tom Sistermans, Marion Kever, Jenny Fuchs, Falk Butter, Susanne Foitzik
bioRxiv 2022.12.23.521666; doi: https://doi.org/10.1101/2022.12.23.521666

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