Microsporidia dressing up: the spore polaroplast transport through the polar tube and transformation into the sporoplasm membrane

Abstract

Microsporidia are obligate intracellular parasites that infect a wide variety of hosts, including humans. Microsporidian spores possess a unique, highly specialized invasion apparatus involving the polar filament, polaroplast and posterior vacuole. During spore germination, the polar filament is discharged out of the spore forming the hollow polar tube that transports the sporoplasm components including nucleus into the host cell to achieve the invasion. Due to the complicated topological changes occurring in this process, the formation of sporoplasm is unclear. Here, electron microscopy observation and DiI staining confirmed that during spore germination, a large number of vesicles derived from the polaroplast, nucleus and other cytoplasm were transported out via the polar tube. Meanwhile, the posterior vacuole and plasma membrane remained in the empty spore coat. In addition, there was no DiI-labeled membrane around the nucleus in mature spores, whereas a DiI-labeled limit membrane wrapping nucleus was found at the tip of the extruded polar tube, suggesting that the membrane of sporoplasm was formed outside the mature spore. TwoNosema bombycissporoplasm surface proteins (NbTMP1 and NoboABCG1.1) were located at the polaroplast in mature spores, in the extruded polar tube and on the sporoplasm membrane, which indicated that the polaroplast transported via the polar tube finally became the limiting membrane of the sporoplasm. Golgi-tracker green and Golgi marker protein syntaxin 6 were also found the same model, which was consistent with the transported polaroplast derived from Golgi transformed into the novel sporoplasm membrane during spore germination.

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

“…Some fine fibers were observed on the outermost layer of the polar tubes, which might be the glycosylated PTPs. At the tip of the extruded polar tube of A. algerae, a "J"-shaped hook existed [31,68], which was also found in the extruded polar tube of N. bombycis [70]. During the process of germination, the polar tube first elongated to its maximum length , and then rapidly shortened once the sporoplasm was released [31].…”

“…Live-cell imaging of nuclei transport through the A. algerae polar tube showed that the nuclei were elongated, then recovered a globular shape after exiting the polar tube [31]. Lv et al labeled the diplokaryons of N. bombycis and also found that they were elongated for transport in the polar tube [70]. However, Takvorian et al [68] observed some circular diplokaryons surrounded by a membrane forming the oval or sperm-head-shaped structures in the A. algerae polar tube.…”

Ultrastructural insights into the microsporidian infection apparatus reveal the kinetics and morphological transitions of polar tube and cargo during host cell invasion

“…These events, including tube eversion and passage of sporoplasm cargo through this constricted tube, are extremely fast and occur within 2 s [ 25 ]. To achieve successful firing, sporoplasm delivery, and host infection, the polar tube and the cargo undergo drastic remodeling during this discharge [ 25 , 27 , 28 ]. These swift ultrastructure changes in the polar tube evince its extraordinary mechanical properties likely conferred by its components, the PTPs.…”

“…These swift ultrastructure changes in the polar tube evince its extraordinary mechanical properties likely conferred by its components, the PTPs. However, the mechanisms driving polar tube firing, sporoplasm discharge, and the dynamics of polar tube eversion are not well understood [25,[28][29][30]. Further, the swift nature of germination events creates challenges in capturing polar tube dynamics and contributes to the generally understudied nature of these parasites.…”