Three-dimensional visualization and a deep-learning model reveal complex fungal parasite networks in behaviorally manipulated ants

Maridel A. Fredericksen, Yizhe Zhang, Missy L. Hazen, Raquel G. Loreto, Colleen A. Mangold, Danny Z. Chen, David P. Hughes

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

Some microbes possess the ability to adaptively manipulate host behavior. To better understand how such microbial parasites control animal behavior, we examine the cell-level interactions between the species-specific fungal parasite Ophiocordyceps unilateralis sensu lato and its carpenter ant host (Camponotus castaneus) at a crucial moment in the parasite’s lifecycle: when the manipulated host fixes itself permanently to a substrate by its mandibles. The fungus is known to secrete tissue-specific metabolites and cause changes in host gene expression as well as atrophy in the mandible muscles of its ant host, but it is unknown how the fungus coordinates these effects to manipulate its host’s behavior. In this study, we combine techniques in serial block-face scanning-electron microscopy and deep-learning–based image segmentation algorithms to visualize the distribution, abundance, and interactions of this fungus inside the body of its manipulated host. Fungal cells were found throughout the host body but not in the brain, implying that behavioral control of the animal body by this microbe occurs peripherally. Additionally, fungal cells invaded host muscle fibers and joined together to form networks that encircled the muscles. These networks may represent a collective foraging behavior of this parasite, which may in turn facilitate host manipulation.

Original languageEnglish (US)
Pages (from-to)12590-12595
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number47
DOIs
StatePublished - Nov 21 2017

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Ants
Parasites
Fungi
Learning
Mandible
Muscles
Communicable Disease Control
Animal Behavior
Aptitude
Cell Communication
Electron Scanning Microscopy
Atrophy
Gene Expression
Brain

All Science Journal Classification (ASJC) codes

  • General

Cite this

Fredericksen, Maridel A. ; Zhang, Yizhe ; Hazen, Missy L. ; Loreto, Raquel G. ; Mangold, Colleen A. ; Chen, Danny Z. ; Hughes, David P. / Three-dimensional visualization and a deep-learning model reveal complex fungal parasite networks in behaviorally manipulated ants. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 47. pp. 12590-12595.
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Three-dimensional visualization and a deep-learning model reveal complex fungal parasite networks in behaviorally manipulated ants. / Fredericksen, Maridel A.; Zhang, Yizhe; Hazen, Missy L.; Loreto, Raquel G.; Mangold, Colleen A.; Chen, Danny Z.; Hughes, David P.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 47, 21.11.2017, p. 12590-12595.

Research output: Contribution to journalArticle

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