Abstract
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.
Highlights
Intracellular pathogens use a diverse array of mechanisms to enter and infect new host cells[1,2,3]
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
Our study provides new insights into architecture and dynamics of the polar tube (PT), which serve as foundations for our understanding of microsporidia infection
Summary
Intracellular pathogens use a diverse array of mechanisms to enter and infect new host cells[1,2,3]. Microsporidia are a group of single-celled intracellular parasites that have developed one of the most dramatic, yet poorly understood, mechanisms of host cell invasion. Microsporidia infect a wide range of hosts, including nematodes[6,7], insects[8,9], and vertebrates[10,11,12]. As obligate intracellular parasites with reduced genomes[17], they are dependent on the host for replication[18,19]. Prior to exiting the host cell, microsporidia form spores, which are the only form of the organism that can survive outside of a host
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