Abstract
BackgroundAdaptive manipulation of animal behavior by parasites functions to increase parasite transmission through changes in host behavior. These changes can range from slight alterations in existing behaviors of the host to the establishment of wholly novel behaviors. The biting behavior observed in Carpenter ants infected by the specialized fungus Ophiocordyceps unilateralis s.l. is an example of the latter. Though parasitic manipulation of host behavior is generally assumed to be due to the parasite’s gene expression, few studies have set out to test this.ResultsWe experimentally infected Carpenter ants to collect tissue from both parasite and host during the time period when manipulated biting behavior is experienced. Upon observation of synchronized biting, samples were collected and subjected to mixed RNA-Seq analysis. We also sequenced and annotated the O. unilateralis s.l. genome as a reference for the fungal sequencing reads.ConclusionsOur mixed transcriptomics approach, together with a comparative genomics study, shows that the majority of the fungal genes that are up-regulated during manipulated biting behavior are unique to the O. unilateralis s.l. genome. This study furthermore reveals that the fungal parasite might be regulating immune- and neuronal stress responses in the host during manipulated biting, as well as impairing its chemosensory communication and causing apoptosis. Moreover, we found genes up-regulated during manipulation that putatively encode for proteins with reported effects on behavioral outputs, proteins involved in various neuropathologies and proteins involved in the biosynthesis of secondary metabolites such as alkaloids.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1812-x) contains supplementary material, which is available to authorized users.
Highlights
Adaptive manipulation of animal behavior by parasites functions to increase parasite transmission through changes in host behavior
We found that during manipulated biting, the fungal parasite O. unilateralis s.l. up-regulates genes that putatively encode for proteins involved in oxidation-reduction processes and pathogenicity-related interactions, some of which may have medical or industrial applications
Our transcriptomics data indicate a shift from parasitic to saprophytic activity. This is supported by previous metabolomics analyses, which demonstrated that fungal parasites display vastly different secretomes during growth on live versus dead ant tissues [36]. Related to this shift we found that after manipulation, O. unilateralis s.l. had downregulated an overrepresented amount of genes involved in oxidation-reduction processes, such as cytochrome P450s (CYPs) (Additional file 6: Table S6)
Summary
Adaptive manipulation of animal behavior by parasites functions to increase parasite transmission through changes in host behavior. Many parasites have evolved the ability to manipulate host behavior This can range from alterations of existing behavioral traits to the expression of novel behaviors not present in the normal repertoire [1,2,3]. These changes in host behavior serve to promote completion of the parasite’s life cycle and are generally assumed to be the result de Bekker et al BMC Genomics (2015) 16:620 second mechanism involves expression of the baculovirus gene ecdysteroid uridine 5’-diphosphate (UDP)-glucosyltransferase (egt) that results in a disrupted climbing behavior [9]. The attraction of infected individuals by light, suggests a role for host pathways involved in phototaxis and light perception [17]
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