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

Charissa de Bekker, Robin A. Ohm, Raquel G. Loreto, Aswathy Sebastian, Istvan Albert, Martha Merrow, Andreas Brachmann, David P. Hughes

Research output: Contribution to journalArticle

45 Citations (Scopus)

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.

Original languageEnglish (US)
Article number620
JournalBMC genomics
Volume16
Issue number1
DOIs
StatePublished - Aug 19 2015

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Behavior Control
Ants
Gene Expression
Parasites
Fungal Genes
Genome
Animal Behavior
Proteins
Genomics
Alkaloids
Fungi
Communication
Observation
RNA
Apoptosis
Genes

All Science Journal Classification (ASJC) codes

  • Biotechnology
  • Genetics

Cite this

de Bekker, Charissa ; Ohm, Robin A. ; Loreto, Raquel G. ; Sebastian, Aswathy ; Albert, Istvan ; Merrow, Martha ; Brachmann, Andreas ; Hughes, David P. / Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. In: BMC genomics. 2015 ; Vol. 16, No. 1.
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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.",
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Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. / de Bekker, Charissa; Ohm, Robin A.; Loreto, Raquel G.; Sebastian, Aswathy; Albert, Istvan; Merrow, Martha; Brachmann, Andreas; Hughes, David P.

In: BMC genomics, Vol. 16, No. 1, 620, 19.08.2015.

Research output: Contribution to journalArticle

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T1 - Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation

AU - de Bekker, Charissa

AU - Ohm, Robin A.

AU - Loreto, Raquel G.

AU - Sebastian, Aswathy

AU - Albert, Istvan

AU - Merrow, Martha

AU - Brachmann, Andreas

AU - Hughes, David P.

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