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Microsporidia: Obligate Intracellular Pathogens Within the Fungal Kingdom

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  • Authors: Bing Han1, Louis M. Weiss2
  • Editors: Joseph Heitman4, Eva Holtgrewe Stukenbrock5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Pathology, Division of Tropical Medicine and Parasitology; 2: Department of Pathology, Division of Tropical Medicine and Parasitology; 3: Department of Medicine, Division of Infectious Diseases, Albert Einstein College of Medicine, Bronx, NY 10461; 4: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 5: Environmental Genomics, Christian-Albrechts University of Kiel, Kiel, Germany, and Max Planck Institute for Evolutionary Biology, Plön, Germany
  • Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0018-2016
  • Received 27 June 2016 Accepted 12 December 2016 Published 10 March 2017
  • Louis M. Weiss, louis.weiss@einstein.yu.edu
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  • Abstract:

    Microsporidia are obligate intracellular pathogens related to Fungi. These organisms have a unique invasion organelle, the polar tube, which upon appropriate environmental stimulation rapidly discharges out of the spore, pierces a host cell’s membrane, and serves as a conduit for sporoplasm passage into the host cell. Phylogenetic analysis suggests that microsporidia are related to the Fungi, being either a basal branch or sister group. Despite the description of microsporidia over 150 years ago, we still lack an understanding of the mechanism of invasion, including the role of various polar tube proteins, spore wall proteins, and host cell proteins in the formation and function of the invasion synapse. Recent advances in ultrastructural techniques are helping to better define the formation and functioning of the invasion synapse. Over the past 2 decades, proteomic approaches have helped define polar tube proteins and spore wall proteins as well as the importance of posttranslational modifications such as glycosylation in the functioning of these proteins, but the absence of genetic techniques for the manipulation of microsporidia has hampered research on the function of these various proteins. The study of the mechanism of invasion should provide fundamental insights into the biology of these ubiquitous intracellular pathogens that can be integrated into studies aimed at treating or controlling microsporidiosis.

  • Citation: Han B, Weiss L. 2017. Microsporidia: Obligate Intracellular Pathogens Within the Fungal Kingdom. Microbiol Spectrum 5(2):FUNK-0018-2016. doi:10.1128/microbiolspec.FUNK-0018-2016.

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Infection and Immunity
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RNA Polymerase II
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/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0018-2016
2017-03-10
2017-07-20

Abstract:

Microsporidia are obligate intracellular pathogens related to Fungi. These organisms have a unique invasion organelle, the polar tube, which upon appropriate environmental stimulation rapidly discharges out of the spore, pierces a host cell’s membrane, and serves as a conduit for sporoplasm passage into the host cell. Phylogenetic analysis suggests that microsporidia are related to the Fungi, being either a basal branch or sister group. Despite the description of microsporidia over 150 years ago, we still lack an understanding of the mechanism of invasion, including the role of various polar tube proteins, spore wall proteins, and host cell proteins in the formation and function of the invasion synapse. Recent advances in ultrastructural techniques are helping to better define the formation and functioning of the invasion synapse. Over the past 2 decades, proteomic approaches have helped define polar tube proteins and spore wall proteins as well as the importance of posttranslational modifications such as glycosylation in the functioning of these proteins, but the absence of genetic techniques for the manipulation of microsporidia has hampered research on the function of these various proteins. The study of the mechanism of invasion should provide fundamental insights into the biology of these ubiquitous intracellular pathogens that can be integrated into studies aimed at treating or controlling microsporidiosis.

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Figures

Image of FIGURE 1
FIGURE 1

Microsporidian life cycles. The initial phase of infection involves spores being exposed to the proper environmental conditions that cause germination of the spores and polar tube extrusion. The polar tube pierces the plasma membrane (solid black line) of the host cell, and the sporoplasm travels through the polar tube into the host cell. The sporoplasm then divides during the proliferative phase, and the morphology of this division is used for determination of microsporidian genera. The sporoplasm on the left is uninucleate, and the cells that are produced from it represent the developmental patterns of several microsporidia with isolated nuclei. The sporoplasm on the right is diplokaryotic, and it similarly produces the various diplokaryotic developmental patterns. Cells containing either type of nucleation will produce one of three basic developmental forms. Some cycles have cells that divide immediately after karyokinesis by binary fission (e.g., ). A second type forms elongated moniliform multinucleate cells that divide by multiple fission (e.g., some species). The third type forms rounded plasmodial multinucleate cells that divide by plasmotomy (e.g., species). Cells may repeat their division cycles one to several times in the proliferative phase. The intracellular stages in this phase are usually in direct contact with the host cell cytoplasm or closely abutted to the host endoplasmic reticulum; however, the proliferative cells of (and probably ) are surrounded by a host-formed parasitophorous vacuole throughout their development, and the proliferative plasmodium of the genus is surrounded by a thick layer of parasite secretions that becomes the sporophorous vesicle in the sporogonic phase. The sporogonic phase is illustrated below the dashed line. Some of the microsporidian genera maintain direct contact with the host cell cytoplasm during sporogony, i.e., , , , , and probably . The remaining genera form a sporophorous vesicle as illustrated by the circles around developing sporogonial stages. It should be noted that in the cycle and the -like part of the cycle, the diplokarya separate and continue their development as cells with isolated nuclei. Adapted with permission from reference 70 .

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0018-2016
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Image of FIGURE 2
FIGURE 2

Diagram of a microsporidian spore. Spores range in size from 1 to 10 μm. The spore coat consists of an electron-dense exospore (Ex), an electron-lucent endospore (En), and a plasma membrane (Pm). It is thinner at the anterior end of the spore. The sporoplasm (Sp) contains a single nucleus (Nu), the posterior vacuole (PV), and ribosomes. The polar filament is attached to the anterior end of the spore by an anchoring disc (AD) and is divided into two regions: the manubroid, or straight portion (M), and the posterior region forming five coils (PT) around the sporoplasm. The manubroid polar filament is surrounded by the lamellar polaroplast (Pl) and vesicular polaroplast (VPl). The insert depicts a cross section of the polar tube coils (five coils in this spore), demonstrating the various concentric layers of different electron density and electron-dense core present in such cross sections. Reprinted with permission from reference 70 .

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0018-2016
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Image of FIGURE 3
FIGURE 3

Scanning electron micrograph of microsporidia infection of a host cell shows the extruded polar tube of a spore of piercing and infecting Vero E6 green monkey kidney cells in tissue culture. Reprinted with permission from reference 70 and with the kind permission of N. P. Kock, C. Schmetz, and J. Schottelius, Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany; published in Kock NP. 1998. Diagnosis of human pathogen microsporidia (dissertation).

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0018-2016
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Tables

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TABLE 1

Species of microsporidia infecting humans

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0018-2016

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