Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 114, Issue 47, Pages 12590-12595Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.1711673114
Keywords
deep learning; fungal networks; extended phenotype; behavioral manipulation; ants
Categories
Funding
- National Science Foundation [IOS-1558062, CCF-1217906, CNS-1629914, CCF-1617735]
- NIH [R01 GM116927-02]
- Comissao de Aperfeicoamento de Pessoal de Nival Superior-Brazil [6203-10-8]
- American Heart Association [16POST29920001]
- Division of Computing and Communication Foundations
- Direct For Computer & Info Scie & Enginr [1617735, 1217906] Funding Source: National Science Foundation
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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.
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