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

Journal: Proceedings of the National Academy of Sciences of the United States of America
Published Date:

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 and its carpenter ant host () 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.

Authors

  • Maridel A Fredericksen
    Department of Entomology, Pennsylvania State University, University Park, PA 16802.
  • Yizhe Zhang
    Department of Computer Science and Engineering, University of Notre Dame, Notre Dame, IN 46556.
  • Missy L Hazen
    Huck Institutes of the Life Sciences Microscopy and Cytometry Facility, Pennsylvania State University, University Park, PA 16802.
  • Raquel G Loreto
    Department of Entomology, Pennsylvania State University, University Park, PA 16802.
  • Colleen A Mangold
    Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, PA 16802.
  • Danny Z Chen
    Department of Computer Science and Engineering, University of Notre Dame, Notre Dame, IN 46556.
  • David P Hughes
    Department of Entomology, Pennsylvania State University, University Park, PA 16802; dhughes@psu.edu.