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Abstract Parasitic fungi produce proteins that modulate virulence, alter host physiology, and trigger host responses. These proteins, classified as a type of “effector,” often act via protein–protein interactions (PPIs). The fungal parasiteOphiocordyceps camponoti-floridani(zombie ant fungus) manipulatesCamponotus floridanus(carpenter ant) behavior to promote transmission. The most striking aspect of this behavioral change is a summit disease phenotype where infected hosts ascend and attach to an elevated position. Plausibly, interspecific PPIs drive aspects ofOphiocordycepsinfection and host manipulation. Machine learning PPI predictions offer high-throughput methods to produce mechanistic hypotheses on how this behavioral manipulation occurs. Using D-SCRIPT to predict host–parasite PPIs, we found ca. 6000 interactions involving 2083 host proteins and 129 parasite proteins, which are encoded by genes upregulated during manipulated behavior. We identified multiple overrepresentations of functional annotations among these proteins. The strongest signals in the host highlighted neuromodulatory G-protein coupled receptors and oxidation–reduction processes. We also detectedCamponotusstructural and gene-regulatory proteins. In the parasite, we found enrichment ofOphiocordycepsproteases and frequent involvement of novel small secreted proteins with unknown functions. From these results, we provide new hypotheses on potential parasite effectors and host targets underlying zombie ant behavioral manipulation.
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Hijacking time: How Ophiocordyceps fungi could be using ant host clocks to manipulate behavior
Abstracts Ophiocordycepsfungi manipulate ant behaviour as a transmission strategy. Conspicuous changes in the daily timing of disease phenotypes suggest thatOphiocordycepsand other manipulators could be hijacking the host clock. We discuss the available data that support the notion thatOphiocordycepsfungi could be hijacking ant host clocks and consider how altering daily behavioural rhythms could benefit the fungal infection cycle. By reviewing time‐course transcriptomics data for the parasite and the host, we argue thatOphiocordycepshas a light‐entrainable clock that might drive daily expression of candidate manipulation genes. Moreover, ant rhythms are seemingly highly plastic and involved in behavioural division of labour, which could make them susceptible to parasite hijacking. To provisionally test whether the expression of ant behavioural plasticity and rhythmicity genes could be affected by fungal manipulation, we performed a gene co‐expression network analysis on ant time‐course data and linked it to available behavioural manipulation data. We found that behavioural plasticity genes reside in the same modules as those affected during fungal manipulation. These modules showed significant connectivity with rhythmic gene modules, suggesting thatOphiocordycepscould be indirectly affecting the expression of those genes as well.
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- Award ID(s):
- 1941546
- PAR ID:
- 10367795
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Parasite Immunology
- Volume:
- 44
- Issue:
- 3
- ISSN:
- 0141-9838
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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