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Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation.

ABSTRACT: BACKGROUND:Adaptive 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. RESULTS:We 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. CONCLUSIONS:Our 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.

SUBMITTER: de Bekker C

PROVIDER: S-EPMC4545319 | biostudies-literature | 2015 Aug

REPOSITORIES: biostudies-literature

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Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation.

de Bekker Charissa C Ohm Robin A RA Loreto Raquel G RG Sebastian Aswathy A Albert Istvan I Merrow Martha M Brachmann Andreas A Hughes David P DP

BMC genomics 20150819

<h4>Background</h4>Adaptive 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 d ...[more]

PMID: 26285697

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Project description:BackgroundParasites that manipulate host behavior can provide prominent examples of extended phenotypes: parasite genomes controlling host behavior. Here we focus on one of the most dramatic examples of behavioral manipulation, the death grip of ants infected by Ophiocordyceps fungi. We studied the interaction between O. unilateralis s.l. and its host ant Camponotus leonardi in a Thai rainforest, where infected ants descend from their canopy nests down to understory vegetation to bite into abaxial leaf veins before dying. Host mortality is concentrated in patches (graveyards) where ants die on sapling leaves ca. 25 cm above the soil surface where conditions for parasite development are optimal. Here we address whether the sequence of ant behaviors leading to the final death grip can also be interpreted as parasite adaptations and describe some of the morphological changes inside the heads of infected workers that mediate the expression of the death grip phenotype.ResultsWe found that infected ants behave as zombies and display predictable stereotypical behaviors of random rather than directional walking, and of repeated convulsions that make them fall down and thus precludes returning to the canopy. Transitions from erratic wandering to death grips on a leaf vein were abrupt and synchronized around solar noon. We show that the mandibles of ants penetrate deeply into vein tissue and that this is accompanied by extensive atrophy of the mandibular muscles. This lock-jaw means the ant will remain attached to the leaf after death. We further present histological data to show that a high density of single celled stages of the parasite within the head capsule of dying ants are likely to be responsible for this muscular atrophy.ConclusionsExtended phenotypes in ants induced by fungal infections are a complex example of behavioral manipulation requiring coordinated changes of host behavior and morphology. Future work should address the genetic basis of such extended phenotypes.

Project description:BACKGROUND: A compelling demonstration of adaptation by natural selection is the ability of parasites to manipulate host behavior. One dramatic example involves fungal species from the genus Ophiocordyceps that control their ant hosts by inducing a biting behavior. Intensive sampling across the globe of ants that died after being manipulated by Ophiocordyceps suggests that this phenomenon is highly species-specific. We advance our understanding of this system by reconstructing host manipulation by Ophiocordyceps parasites under controlled laboratory conditions and combining this with field observations of infection rates and a metabolomics survey. RESULTS: We report on a newly discovered species of Ophiocordyceps unilateralis sensu lato from North America that we use to address the species-specificity of Ophiocordyceps-induced manipulation of ant behavior. We show that the fungus can kill all ant species tested, but only manipulates the behavior of those it infects in nature. To investigate if this could be explained at the molecular level, we used ex vivo culturing assays to measure the metabolites that are secreted by the fungus to mediate fungus-ant tissue interactions. We show the fungus reacts heterogeneously to brains of different ant species by secreting a different array of metabolites. By determining which ion peaks are significantly enriched when the fungus is grown alongside brains of its naturally occurring host, we discovered candidate compounds that could be involved in behavioral manipulation by O. unilateralis s.l.. Two of these candidates are known to be involved in neurological diseases and cancer. CONCLUSIONS: The integrative work presented here shows that ant brain manipulation by O. unilateralis s.l. is species-specific seemingly because the fungus produces a specific array of compounds as a reaction to the presence of the host brain it has evolved to manipulate. These studies have resulted in the discovery of candidate compounds involved in establishing behavioral manipulation by this specialized fungus and therefore represent a major advancement towards an understanding of the molecular mechanisms underlying this phenomenon.

Project description:Some Ophiocordyceps species infecting ants are able to manipulate the host behavior. The hosts are manipulated in order to move to location that are advantageous for fungal spore transmission. Ophiocordyceps species that are able to manipulate the ant's behavior are called "zombie-ant fungi". They are widespread within tropical forests worldwide, with relatively few reports from subtropical monsoon evergreen broad-leaf forest. Zombie-ant fungi have been described and reported in different countries worldwide. However, there were a few reports from China. This study proposed six new species of zombie-ant fungi from China based on multi-gene (SSU, LSU, TEF, RPB1 and RPB2) phylogenetic analyses and morphological characteristics. Six novel species of Ophiocordyceps from China were identified as the Ophiocordyceps unilateralis core clade, forming a separate lineage with other species. Six novel species of Ophiocordyceps with hirsutella-like asexual morphs exclusively infecting ants were presented herein, namely, Ophiocordyceps acroasca, Ophiocordyceps bifertilis, Ophiocordyceps subtiliphialida, Ophiocordyceps basiasca, Ophiocordyceps nuozhaduensis and Ophiocordyceps contiispora. Descriptions and illustrations for six taxon were provided. Five of these species were collected from the subtropical monsoon evergreen broad-leaf forest, and one was collected from the rainforest and subtropical monsoon evergreen broad-leaf forest. This work proposes that the same host of Camponotus can be infected by multiple ant pathogenic fungi, while multiple ants of Polyrhachis can be infected by the same pathogenic fungi at the same time. This study contributes towards a better understanding of the evolutionary relationship between hosts and fungi, and provides novel insights into the morphology, distribution, parasitism, and ecology of Ophiocordyceps unilateralis sensu lato. We have provided a method for obtaining living cultures of Ophiocordyceps unilateralis complex species and their asexual morphs based on the living cultures, which is of significant value for further studies of Ophiocordyceps unilateralis complex species in the future.

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Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation.

Publications

Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation.

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