3-Dimensional organization and dynamics of the microsporidian polar tube invasion machinery

Autor: Michael Cammer, Damian C. Ekiert, Feng-Xia Liang, Mahrukh Usmani, Pattana Jaroenlak, Alina Davydov, Gira Bhabha, Joseph Sall
Jazyk: angličtina
Rok vydání: 2020
Předmět:
Pulmonology
Pathology and Laboratory Medicine
Medical Conditions
0302 clinical medicine
Cell polarity
Medicine and Health Sciences
Biology (General)
Fungal Pathogens
Microscopy
0303 health sciences
biology
Chemistry
030302 biochemistry & molecular biology
Dynamics (mechanics)
Cell Polarity
Spores
Fungal
Entry into host
In Vivo Imaging
Infectious Diseases
Aspect Ratio
medicine.anatomical_structure
Medical Microbiology
030220 oncology & carcinogenesis
Microsporidia
Physical Sciences
Cellular Structures and Organelles
Pathogens
Research Article
Cell Physiology
Materials science
Imaging Techniques
QH301-705.5
Immunology
Geometry
Mycology
Opportunistic Infections
Research and Analysis Methods
Microbiology
Fungal Proteins
Respiratory Disorders
03 medical and health sciences
Virology
Anncaliia algerae
Organelle
Genetics
medicine
Molecular Biology
Microbial Pathogens
030304 developmental biology
Organelles
fungi
Biology and Life Sciences
Cell Biology
RC581-607
biology.organism_classification
Vacuoles
Respiratory Infections
Polar tube
Biophysics
Parasitology
Immunologic diseases. Allergy
Nucleus
Mathematics
Zdroj: PLoS Pathogens, Vol 16, Iss 9, p e1008738 (2020)
PLoS Pathogens
ISSN: 1553-7374
1553-7366
Popis: Microsporidia, a divergent group of single-celled eukaryotic parasites, harness a specialized harpoon-like invasion apparatus called the polar tube (PT) to gain entry into host cells. The PT is tightly coiled within the transmissible extracellular spore, and is about 20 times the length of the spore. Once triggered, the PT is rapidly ejected and is thought to penetrate the host cell, acting as a conduit for the transfer of infectious cargo into the host. The organization of this specialized infection apparatus in the spore, how it is deployed, and how the nucleus and other large cargo are transported through the narrow PT are not well understood. Here we use serial block-face scanning electron microscopy to reveal the 3-dimensional architecture of the PT and its relative spatial orientation to other organelles within the spore. Using high-speed optical microscopy, we also capture and quantify the entire PT germination process of three human-infecting microsporidian species in vitro: Anncaliia algerae, Encephalitozoon hellem and E. intestinalis. Our results show that the emerging PT experiences very high accelerating forces to reach velocities exceeding 300 μm⋅s-1, and that firing kinetics differ markedly between species. Live-cell imaging reveals that the nucleus, which is at least 7 times larger than the diameter of the PT, undergoes extreme deformation to fit through the narrow tube, and moves at speeds comparable to PT extension. Our study sheds new light on the 3-dimensional organization, dynamics, and mechanism of PT extrusion, and shows how infectious cargo moves through the tube to initiate infection.
Author summary Microsporidia infect a wide range of hosts: from economically important invertebrates such as silkworms and honey bees, to vertebrates including humans, where infection in immunocompromised patients can be fatal. In order to infect the host, microsporidia utilize a unique harpoon-like invasion organelle called the polar tube (PT), which serves as a pathway for transport of infectious cargo to the host. Knowledge of how the long PT is packaged in the spore, the kinetics of its firing and how the cargo is transported through the PT are still poorly understood. We use electron microscopy techniques to generate 3D reconstructions of intact spores, which reveal the configuration of the PT and other organelles within. Using high-speed live-cell imaging, we capture and quantify the kinetics of PT firing, and how cargo is deformed during transport through the narrow PT. Our study provides new insights into architecture and dynamics of the PT, which serve as foundations for our understanding of microsporidia infection.
Databáze: OpenAIRE
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