Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation.
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.
Institute of Medical Psychology, Faculty of Medicine, Ludwig-Maximilians-University Munich, Goethestrasse 31, 80336, Munich, Germany. charissa.debekker@med.uni-muenchen.de.|Department of Entomology and Department of Biology, Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, State College, Pennsylvania, 16802, PA, USA. charissa.debekker@med.uni-muenchen.de.
Charissa
C
de Bekker
Microbiology, Faculty of Science, Utrecht University, Padualaan 8, 3584, CH, Utrecht, The Netherlands.
Robin A
RA
Ohm
Department of Entomology and Department of Biology, Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, State College, Pennsylvania, 16802, PA, USA.|CAPES Foundation, Ministry of Education of Brazil, Brasília, 70040-020, DF, Brazil.
Raquel G
RG
Loreto
Bioinformatics Consulting Center, Pennsylvania State University, University Park, State College, Pennsylvania, 16802, PA, USA.
Aswathy
A
Sebastian
Bioinformatics Consulting Center, Pennsylvania State University, University Park, State College, Pennsylvania, 16802, PA, USA.|Department of Biochemistry and Molecular Biology, The Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, State College, Pennsylvania, 16802, PA, USA.
Istvan
I
Albert
Institute of Medical Psychology, Faculty of Medicine, Ludwig-Maximilians-University Munich, Goethestrasse 31, 80336, Munich, Germany.
Martha
M
Merrow
Faculty of Biology, Section Genetics, Ludwig-Maximilians-University Munich, Grosshaderner Strasse 2-4, 82152, Martinsried, Germany.
Andreas
A
Brachmann
Department of Entomology and Department of Biology, Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, State College, Pennsylvania, 16802, PA, USA. dhughes@psu.edu.
David P
DP
Hughes
D000818:Animals; D001000:Ants / Q000235:genetics* / Q000382:microbiology*; D001522:Behavior, Animal / Q000502:physiology*; D020869:Gene Expression Profiling / Q000379:methods; D005786:Gene Expression Regulation; D016681:Genome, Fungal; D049750:Genome, Insect; D054884:Host-Pathogen Interactions; D010802:Phylogeny; D004718:Saccharomycetales / Q000235:genetics / Q000502:physiology*; D017423:Sequence Analysis, RNA / Q000379:methods*