Microsporidian Spore Germination: History
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Qingyuan Huang
,
Jie Chen
,
Qing Lv
,
Mengxian Long
,
Guoqing Pan
,
Zeyang Zhou

Microsporidia are a large group of mysterious obligate intracellular eukaryotic parasites. The microsporidian spore can survive in the absence of nutrients for years under harsh conditions and germinate within seconds under the stimulation of environmental changes like pH and ions. During germination, microsporidia experience an increase in intrasporal osmotic pressure, which leads to an influx of water into the spore, followed by swelling of the polaroplasts and posterior vacuole, which eventually fires the polar filament (PF). Infectious sporoplasm was transported through the extruded polar tube (PT) and delivered into the host cell. 

  • microsporidia
  • germination
  • spore wall proteins
  • polar tube
  • receptors

1. Activation of Spore Germination

Activators for spore germination differ greatly among different species of microsporidia [1][2][3]. In vitro germination of microsporidian spores has been extensively studied in the past few decades. Germination of spores is commonly activated by external pH changes, alkali metal ions, anions, and temperatures. Additionally, a significant difference was found between the germination conditions of two strains of microsporidia belonging to the same genus (Trachipleistophora) [4]. For many species of microsporidia, a shift in external pH to acidic or alkaline triggers germination [2][5][6][7][8]. When the spore is activated, some spore wall proteins (SWPs) can be shed, which may increase the permeability of the spore wall, reduce the rigidity of the spore apex, and lead to the ejection of the polar tube (PT). For instance, SWP30 (SWP1) of Nosema bombycis was displayed both in the alkali-soluble proteins that were extracted from frozen spores and in proteins dissolved in 0.1 mol/L K2CO3 during germination, which was stimulated by the solution [9][10]. The protein was one of the main components of endospores, and its function is still unknown [9][11]. Although 36 SWPs (Table 1) have been identified so far, a large number of microsporidia SWPs have not been discovered [12][13]. Further studies of the diversity of these proteins can significantly improve our understanding of spore activation and invasion. Research on the proteins will enable us to deeper understand the mechanisms of spore wall assembly and the orderly arrangement of polar tubes, the molecular pathogenesis of microsporidian infection, and develop effective strategies to control microsporidiosis [14]. In addition, pH is studied in conjunction with other activators in order to gain a better understanding of how it affects germination. The spore wall functions as a barrier to prevent larger molecules from passing through, but alkali metal cations appear to pass freely through the spore wall and plasma membrane [15]. During germination, the smaller cations (e.g., Na+, and K+, which have been shown to trigger spore germination in Nosema) appear to be more efficient [2][15][16][17]. Spores of diverse microsporidia reacted differently to Na+, K+, and other cations during germination. The spore germination rate of Antonospora locustae (formerly Nosema locustae) has also been increased with LiCl, RbCl, and CsCl [2]. The germination of spores is also influenced by anions. The germination rate of spores was nearly 70% in 0.1 M NaCl or NaNO3, but reduced to 1% in Na2SO4 and Na2HPO4 [15]. Other anions have been used to promote PF discharge, including bromide, iodide, and fluoride [18]. The dehydration of some microsporidia followed by rehydration by hyperosmotic solutions has been found to be effective in promoting spore germination [2]. Low doses of ultraviolet radiation can trigger germination by disrupting the barriers between trehalose and trehalase [19]. Furthermore, microsporidian spores can germinate in response to changes in calcium ion concentrations, the osmotic pressure of the external medium, or in vivo host environments [8][20][21]. Intriguingly, studies have found that calcium chloride (0.001~0.1 mol/L) inhibits spore germination, whereas 0.2 M CaCl2 at pH 9.0 and 1 mM CaCl2 as well as calcium ionophore A23187 promote PF discharge [5][7][8][20][22][23][24][25][26][27][28]. It has been suggested that the displacement of calcium between the membrane and matrix of the polaroplast might be responsible for polaroplast swelling and the subsequent PF discharge [20][29]. According to this theory, the calcium ionophore A23187 triggers polaroplast swelling and discharge of PF, whereas calcium chloride inhibits it [29]. Calcium seems to be an essential component in regulating germination [22].
Table 1. The identified microsporidian spore wall proteins.
Species Protein/UniProtKB Number of Amino Acids PI Mainly Location Features Mw (kDa) References
Encephalitozoon cuniculi EcSWP1/Q9XZV1 450 4.96 Exospore glycine- and serine-rich repeats 51 Bohne et al., 2000 [30]
  EcEnP1/Q8SWL3 357 9.07 Endospore HBM 40.5 Southern et al., 2007 [31]
Peuvel et al., 2006 [32]
  EcEnP2/EcSWP3/Q8SWI4 221 8.42 Endospore glycosylphosphatidylinositol (GPI) anchored and O-glycosylation sites 22 Peuvel et al., 2007 [32]
Xu et al., 2006 [33]
  EcCDA/Q8SU65 254 4.43 Endospore,plasma membrane Glycoside hydrolase and deacetylase 28.1 Brosson et al., 2005 [34]
Encephalitozoon intestinalis EiSWP1/Q95WA3 388 4.78 Exospore - 41 Hayman et al., 2001 [35]
  EiSWP2/Q95WA4 1002 3.68 Exospore Repeating of amino-acid units 107 Hayman et al., 2001 [35]
  EiEnP1/A7TZU4 348 8.84 Exospore,endospore and polar membrane layer HBM 39.1 Southern et al., 2007 [31]
Encephalitozoon hellem EhSWP1a/C3VJR1 509 4.30 Exospore - 55 Polonais et al., 2010 [36]
  EhSWP1b/C3VJR2 533 4.64 Exospore - 60 Polonais et al., 2010 [36]
Nosema bombycis NbSWP1/B3STN5 278 7.95 Endospore - 30.4 Wu et al., 2008 [11]
  NbSWP2/B3STN6 268 8.45 Endospore HBM 25.3 Wu et al., 2008 [11]
  NbSWP3/B3STN7 316 7.29 Exospore - 32.7 Wu et al., 2008 [11]
  NbSWP5/G0Z414 186 4.39 Endospore and PT Interacts with PTP2 and PTP3 20.3 Li et al., 2012 [37][38]
  NbSWP7/B3STP1 287 4.78 Exospore and endospore Interacts with NbSWP9 32.8 Yang et al., 2015 [39]
  NbSWP9/R0MLT0 367 8.32 Exospore, endospore and PT Interacts with PTP1, PTP2 and NbSWP9 42.8 Yang et al., 2015 [39]
  NbSWP11/B3STP5 446 9.27 Exospore and endospore DnaJ domain and HBM 52.3 Yang et al., 2014 [40]
  NbSWP12/B3STP6 228 6.78 Exospore, endospore, membrane of meront BAR-2 domain and HBM 26.6 Chen et al., 2013 [41][42][43]
  NbSWP16/R0MN98 211 8.42 Exospore HBM and proline-rich tandem repeats 44 Wang et al., 2015 [44]
  NbSWP26/B9UJ97 223 5.09 Exospore HBM and N-glycosylation sites 25.7 Li et al., 2009 [45]
  Unnamed/EOB13250 244 10.24 Endospore Transmembrane domain 28 Wang et al., 2020 [46]
Nosema ceranae Unnamed/A0A0F9WE74 226 6.84 Endospore - 26.19 Liang et al., 2021 [47]
  NcSWP8/A0A0F9WIV3 172 4.00 - Promote proliferation 19.5 He et al., 2021 [48]
  NcSWP12/A0A0F9WTX8 229 7.88 - Promote proliferation 26.7 He et al., 2021 [48]
Enterocytozoon hepatopenaei EhSWP1/A0A1W0E3P7 228 8.45 Exospore and endospore Exospore and endospore 27 Jaroenlak et al., 2018 [49]
  EhSWP2/A0A1W0E3S3 228 5.12 - MICSWaP domains 25.7 Li et al., 2021 [50]
  EhSWP3/A0A1W0E914 249   Exospore and endospore transmembrane domains 27.1 Fan et al., 2022 [51]
  EhSWP7/A0A1W0E705 250 5.04 - - 25.3 Li et al., 2021 [50]
  EhEnp1/A0A1W0E696 333 8.86 - - 38.3 Li et al., 2021 [50]
Antonospora locustae (formerly Nosema locustae) AlocSWP2/A0A1W0E3S3 222 5.16 Exospore and endospore HBM 25 Chen et al., 2017 [52]
  EbSWP1/B7XHM5 228 7.06 - O-linked glycosylation site 26.8 Meng et al., 2022 [53]
Enterocytozoon bieneusi EbSWP2/B7XJH4 247 9.46 - N-linked glycosylation sites 29.2 Meng et al., 2022 [53]
  EbSWP3/B7XHL8 229 5.15 - N-linked glycosylation sites 25.9 Meng et al., 2022 [53]
  NpSWP1/A0A060A4C2 278 7.02 Endospore Transmembrane 32 Zhu et al., 2014 [54]
Nosema pernyi NpSWP9/A0A0N7AC01 317 5.75 - - 37.16 Ma et al., 2017 [55]
  NpSWP12/A0A0S2EGT8 228 5.96 - BAR domain 26.6 Feng et al., 2015 [56]
Nosema antheraeae NaSWP8/G3CU65 161 4.802 - HBM 18.4 Xi et al., 2010 [57]

2. Energy of Germination

The first observation of the Microsporidia spore structure was made by Thélohan in 1894 [58]. In the years following the initial observations, studies have been conducted to define the internal structure of the spores. It is now generally accepted that in the phylum Microsporidia, spores can take a wide variety of shapes, from spherical to rodlike, and range in size from 1 to 40 μm [59][60]. In the anterior part of the spore, there is a system of membrane-limited cavities called polaroplasts. Typically, this structure occupies one-third to one-half of the spore volume, surrounds the straight part of the polar filament, and terminates at the level of the anterior polar filament coils. In mature spores, polaroplasts vary in shape but are usually lamellar [12][61]. And the posterior vacuole is a membrane-lined area filled with clear or spongy content [61]. The spatial relationship between polar filaments and posterior vacuoles is poorly understood. Different opinions exist regarding whether the filament enters or terminates at the vacuole. An image of the three-dimensional organization of the microsporidian shows the vacuole membrane interdigitating with the PF, cueing an interaction between these two organelles [62]. When microsporidia are exposed to activators, polaroplasts and posterior vacuoles appear to play an important role in the process of germination [16][17][21]. Hydrostatic pressure is now generally accepted as the reason for microsporidian spore germination. Pressure is due to an increase in water permeability or an increase in solute concentration [63]. Interestingly, the way osmotic pressure increases within species differs from species to species [64][65]. The decomposition of trehalose into glucose by trehalase in Nosema algerae can rapidly increase the intrasporal hydrostatic pressure inside the spore, which triggers spore germination [16][21]. Thus, aquatic microsporidia have been hypothesized to germinate through an increase in intrasporal osmotic pressure caused by trehalose degradation [66]. For terrestrial microsporidia, no changes in sugar content were observed after germination, so an alternative explanation is needed [66]. Studies indicated the presence of two crucial components of peroxisomal enzymes, catalase and acyl-CoA oxidase (ACOX), in the posterior vacuole of Spraguea lophii [67][68]. In the β-oxidation of the very long chain fatty acid (VLCFA) nervonic acid, the catalase and ACOX can convert H2O2 into water and oxygen [67][69]. As a result of the oxidation of long chain fatty acids and the subsequent production of molecular oxygen and water, the posterior vacuole may experience rapid swelling and cause germination [67]. Water inflow through aquaporins appears to be crucial to germination [70]. Recently, studies have shown that several aquaporins are located on the spore wall layer of N. bombycis and Encephalitozoon cuniculi. Moreover, the polyamine transporters or permeases encoded by some microsporidia may contribute to germination by absorbing sugars, cations, and nicotinic acids [71][72]. Altogether, increasing osmotic pressure induces spores to absorb water through functional aquaporins, resulting in swelling of the polaroplast and posterior vacuole [17][20][73]. The spore wall withstands osmotic pressure for some time but eventually ruptures at the apex, where it is thin, eventually leading to polar filament discharge [61].

3. Polar Tube and Eversion Process during Germination

When the microsporidia spore activates, accompanied by swelling of the polaroplast and posterior vacuole, the polar filament (PF) is fired from the mushroom-shaped anchoring disk (AD) and forms a hollow tube as an “everting finger of a glove” [17][74]. According to several studies, the everting PT is filled with electron-dense materials, which may be unpolymerized PTPs or tightly folded membranes [75][76][77][78]. Additionally, stretchability is a feature of the PT; the sporoplasm is transported through the PT into the host cell, and the diameter increases from 100 to 600 nm [62][74][78][79][80]. In spores, PF forms a right-handed helix, but the number of coils varies from species to species [62][81][82]. In N. bombycis, the structures of PF and PT have distinct structures; 881 and 1216 proteins have been identified from them, respectively [83]. Despite this, the structure and protein composition of the PF and PT remain a mystery. As of yet, according to research on the composition of the PT, six distinct PTPs (PTP1-PTP6) have been expressed and analyzed from different microsporidia (Table 2) [84]. PTP1, a proline-rich component of PT, has high tensile strength and elasticity. Consequently, it plays a crucial role in the discharge and passage of sporoplasm through narrow PT [85][86][87]. Moreover, as an O-linked mannosylated protein, PTP1 is capable of interacting with mannose-binding receptors on the cell membranes of its host [88][89][90][91]. According to further studies of PTPs, PTP2 is commonly found in various microsporidia at the same genomic locus as PTP1 and is more conserved than PTP1 [87]. PTP3, which can interact with other PTPs, might be a scaffold protein that contributes to the formation of PT [91][92]. PTP4 is found near the tip of the PT in A. locustae [84][93]. Subsequently, The PTP4 of Encephalitozoon hellem showed a similar location to the front of the PT, and immunoprecipitation analysis of PTP4 bound to host cell membranes identified transferrin receptor 1 (TfR1) as a host cell interacting partner for PTP4 [94]. In the genome, PTP4 and PTP5 are usually clustered, suggesting that they may have been linked in either evolution or expression [84][94]. A novel PT protein, NbPTP6, with cell-binding properties, was identified in N. bombycis. NbPTP6 was rich in histidine and serine, as well as having 6 O-glycosylation sites and 1 N-glycosylation site [95]. PTP6 homologs can be found in the genomes of other microsporidia [84]. In addition, ten potential novel PTPs in N. bombycis were screened [83]. Several NbPTPs were reported to interact with the spore wall proteins NbSWP5, NbSWP7, and NbSWP9 [37][39].
Many of the microsporidia proteins involved in spore firing are unknown. The anchoring disk is where the polar tube attaches to the spore wall, and it can rupture for PT discharge [96]. E. cuniculi spore wall protein EnP1 is embedded in the spore wall and abundant in the polar sac/anchoring disk region [31]. The homologous spore wall and anchoring disk complex protein NbSWP16 was identified in N. bombycis [44]. These proteins may play a role in the structural composition of the anchor disk and may also serve as substrates for proteases that promote the breakdown of the polar sac-anchor disk complex. NbSLP1, a subtilisin-like protease that localizes to both poles of the spore from N. bombycis, has been implicated in germination. NbSLP1 is active only at the apex of the spore, where the PT exits [97]. In further studies, intramolecular proteolysis has been shown to be necessary for NbSLP1 maturation, which undergoes a series of sequential cleavages at its N-terminus. The catalytic triad of NbSLP1 is crucial to its self-activation, as with Bacillus amyloliquefaciens, Vibrio cholerae, and other subtilisin-like enzymes [98][99][100]. Chitin is a major component of the endospore, which provides rigidity to the spore [12]. It has been demonstrated that the chitinase NbchiA from N. bombycis mainly hydrolyzes the second glycosidic linkage from the reducing end of (GlcNAc) 3–5, which may contribute to the discharge of polar filaments [101]. In teleost serum, chitinolytic and proteolytic activities may contribute to the defense against microsporidian infection [102].
Table 2. The known proteins localized to the microsporidian polar tube.
Species Protein/UniProtKB Number of Amino Acids Features Mw(kDa) References
Encephalitozoon cuniculi EcPTP1/O76942 395 Acidic proline-rich, hydrophobicity, presence of tandem repeats, mannosylated with O-glycosylation, signal peptide, interact with the Concanavalin A (ConA), localized on the whole PT 37 Xu et al., 2004 [89]
Bouzahzah et al., 2010 [90]
Delbac et al., 1998 [103]
  EcPTP2/Q8SRT0 277 Basic lysine-rich core, acidic tail, can form intermolecular disulfide bridges with PTP1, RGD motif and signal peptide, localized on the whole PT 30 Delbac et al., 2001 [87]
Peuvel et al., 2002 [92]
  EcPTP3/Q8MTP3 1256 Acidic core flanked by highly basic N- and C-termini, lacks cysteine residue, may assist in controlling PT extrusion, signal peptide, localized on the whole PT 150 Peuvel et al., 2002 [92]
Encephalitozoon intestinalis EiPTP1/Q5F2J0 371 proline-rich, presence of tandem repeats, absent tryptophan and arginine, O-glycosylation and signal peptide, interact with the ConA, localized to polar filaments 35 Bouzahzah et al., 2010 [90]
Peuvel et al., 2002 [92]
  EiPTP2/P0CAT4 275 lysine-rich, RGD motif, N-glycosylation and signal peptide 30 Peuvel et al., 2002 [92]
Encephalitozoon hellem EhPTP1/O76273 453 proline-rich, presence of tandem repeats, mannosylated with N-, O-glycosylation, absent tryptophan and arginine, signal peptide, interact with the ConA, localized to polar filaments 43 Keohane et al., 1998 [86]
Xu et al., 2004 [89]
Peuvel et al., 2002 [92],
  EhPTP2/P0CAT5 272 lysine-rich, N-glycosylation, RGN motif and signal peptide, localized on the whole polar 30 Peuvel et al., 2002 [92]
  EhPTP4/I6UDI1 278 signal peptide, located at the tip of the PT, N-, O-glycosylation 36 Han et al., 2017 [94]
Nosema bombycis NbPTP1/R0MQM8 409 signal peptide, O-glycosylation, phosphorylation, localized on the whole PT 55 Wu et al., 2014 [104]
  NbPTP2/R0KY97 277 PI = 9.39, signal peptide, interacted with SWP5, presence in the whole polor tube, phosphorylation, localized on the whole PT 39 Li et al., 2012 [37]
Wang et al., 2007 [105]
Yi et al., 2019 [106]
  NbPTP3/J7EQ15 1370 PI = 6.73, interacted with SWP5, localized on the whole PT 150 Li et al., 2012 [37]
Wang et al., 2007 [105]
  NbPTP4/- 222 PI = 7.56, located at the front end of the PT and around the anchor disk, interact with Bmtubulin-α 25.3 Liu, 2019 [107]
  NbPTP5/R0KWI6 271 PI = 8.68, located at the front end of the PT and around the anchor disk 32.5 Liu, 2019 [107]
  NbPTP6/R0MBR8 247 rich in histidine (H) and serine (S), signal peptide, N-, O-glycosylation, cell-binding ability, localized on the whole PT 28.3 Lv et al., 2020 [95]
  NbSWP5/B3STN9 186 PI = 4.39, localized to the exospore and the region of the PT, interacts with the PT proteins NbPTP2 and NbPTP3 20.3 Li et al., 2012 [37][38]
  NbSWP7/B3STP1 287 PI = 4.78, located in the PT and spore wall. 32.8 Yang et al., 2015 [39]
  NbSWP9/R0MLT0 367 PI = 8.92, located in the spore wall, as well as anchoring disk and the front end of the PT after germination; interacts with NbPTP1 and NbPTP2 42.8 Yang et al., 2015 [39]
Enterocytozoon hepatopenaei EhpPTP2/A0A1W0E7X7 284 PI = 8.8, rich in lysine, super family domain (pfam17022), O-glycosylation 32 Wang et al., 2021 [108]
Antonospora locustae (formerly Nosema locustae) AlPTP1/- 355 PI = 5.2, rich in proline and glycine, N-, O-glycosylation, interact with the ConA, localized on the whole PT 34 Polonais et al., 2005 [109]
AlPTP2/C8CG41 287 PI = 9.1, signal peptide, O-glycosylation, rich in lysine, localized on the whole PT 29 Polonais et al., 2005 [109],
  AlPTP2b/C8CG42 568 signal peptide, PI = 8.4, O-glycosylation, rich glycine and serine, b-turn structures, localized on the whole PT 55 Polonais et al., 2013 [110]
  AlPTP2c/C8CG43 599 signal peptide, PI = 8.7, O-glycosylation, rich glycine and serine, b-turn structures 56 Polonais et al., 2013 [110]
Paranosema grylli PgPTP1/- 351 PI = 5.2, acidic and proline-rich, N-glycosylation, interact with the ConA 33 Polonais et al., 2005 [109]
  PgPTP2/- 287 PI = 8.9, rich in lysine 29 Polonais et al., 2005 [109]
Nosema pernyi NpPTP1/A0A482G4U9 394 PI = 5.82, signal peptide 39.16 Wang et al.,
2019 [111]
  NpPTP2/A0A482G3T3 277 PI = 9.39, signal peptide 30.8 Wang et al.,
2019 [111]
  NpPTP3/A0A0N7ABT9 1370 PI = 6.52, localized on the whole polar 148.56 Wang et al.,
2019 [111]
The whole process of PF eversion in E. hellem and E. intestinalis takes less than 500 ms, while that of Anncaliia algerae takes 1.6 s [62]. Generally, the process of PF eversion can be divided into three phases: (i) PT elongation, (ii) a static phase, where the PT length does not change; and (iii) the emergence of cargo at the distal end of the PT [62]. In the initial phase of PF eversion, PT emerges from the apical portion of the spore and elongates to its maximum size [17][62]. PT length and width may differ among species, but the fully extended PT is much longer than the PF that is inside the spore, suggesting that either the PT is stretched or that the protein or stacked membrane subunits that make up the PT undergo a reorganization during eversion, and once the PT has reached 50% extension, sporoplasm transport begins [62][78]. The stationary phase begins after the PT reaches its maximum length. Microsporidia are mainly transporting sporoplasm at this stage, and the rate of transport varies significantly among different species. During this process, the spore nucleus undergoes significant deformation when passing through the tube due to the significant difference in diameter between the nucleus and the PT. Interestingly, a pause in nuclei movement was found approximately three-quarters of the way through the PT [62]. Currently, there are two hypotheses: (i) During extension, the end of the PT may remain closed, and the delay in the opening of the distal end of the PT may be responsible for the observed pausing during nuclear translocation [17]. (ii) PT firing and sporoplasm transport may diminish the driving force, followed by a further increase in force to complete sporoplasm export, suggesting that sporoplasm may be pushed out of the tube by a new force [84]. In phase 3, the sporoplasm is extruded from the PT at the distal end and has an approximate circular shape. The PT components may interact with the sporoplasm in a specific way, or some membrane from the sporoplasm may remain inside the tube to form an adhesion bridge with the PT [62].

This entry is adapted from the peer-reviewed paper 10.3390/jof9070774

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