The microsporidian polar tube: origin, structure, composition, function, and application

Abstract

Microsporidia are a class of obligate intracellular parasitic unicellular eukaryotes that infect a variety of hosts, even including humans. Although different species of microsporidia differ in host range and specificity, they all share a similar infection organelle, the polar tube, which is also defined as the polar filament in mature spores. In response to the appropriate environmental stimulation, the spore germinates with the polar filament everted, forming a hollow polar tube, and then the infectious cargo is transported into host cells via the polar tube. Hence, the polar tube plays a key role in microsporidian infection. Here, we review the origin, structure, composition, function, and application of the microsporidian polar tube, focusing on the origin of the polar filament, the structural differences between the polar filament and polar tube, and the characteristics of polar tube proteins. Comparing the three-dimensional structure of PTP6 homologous proteins provides new insight for the screening of additional novel polar tube proteins with low sequence similarity in microsporidia. In addition, the interaction of the polar tube with the spore wall and the host are summarized to better understand the infection mechanism of microsporidia. Due to the specificity of polar tube proteins, they are also used as the target in the diagnosis and prevention of microsporidiosis. With the present findings, we propose a future study on the polar tube of microsporidia.

Keywords: Diagnosis; Interaction; Microsporidia; Polar filament; Polar tube; Polar tube proteins; Structure.

Fig. 1

The hypothesis of the formation process of the microsporidian polar filament. A In the early proliferate stages, the GC-like structure (G) is considered as clusters of vesicles derived from the nucleus (N) and endoplasmic reticulum (ER). B The GC-like structure gradually appears as tubules. C With the tubular network (TN) formed, the PTPs are concentrated and modified in the TN and gradually accumulate at its edge. D With the assembly of PTPs, the core and envelope of the polar filaments are first formed. E, F They further develop into layers to develop mature polar filaments

Fig. 2

Comparison of the predicted PTP6 protein structure among different species of microsporidia by AlphaFold2. A Amino acid sequence alignment was generated with ClustalW (https://www.genome.jp/tools-bin/clustalw) and colored by ESPript 3.0 (https://espript.ibcp.fr/ESPript/cgi-bin/ESPript.cgi). B The PTP6 protein structure model of Enc. cuniculi (GenBank No. AGE95102.1), Enc. hellem (GenBank no. AFM98867.1), Enc. intestinalis (GenBank no. ADM12100.1), N. bombycis (GenBank no. EOB11485.1), and N. ceranae (GenBank no. EEQ82670.1) were predicted by AlphaFold2. The highlighted fluorescent green is the overlap region of PTP6 in different species of microsporidia produced by Chimera 1.16

Fig. 3

Summary. In response to external environmental stimulation, the spore germinates with the polar filament everted, forming a hollow polar tube, and then the infectious cargo is transported to inject into host cells through the polar tube. During this process, the polar tube interacts with both the microsporidian spore wall proteins and host receptors, and there are still many unknown aspects that need to be solved. PT polar tube, PF polar filament, PP polaroplast, PV posterior vacuole, Sp sporoplasm, TfR1 transferrin receptor 1