Germination of Microsporidian Spores: The Known and Unknown
Abstract
:1. Infectious Parasites: Microsporidia
2. Known about Microsporidian Spore Germination
2.1. Activation of Spore Germination
2.2. Energy of Germination
2.3. Polar Tube and Eversion Process during Germination
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 [113] Bouzahzah et al., 2010 [114] Delbac et al., 1998 [125] |
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 [111] Peuvel et al., 2002 [116] | |
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 [116] | |
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 [114] Peuvel et al., 2002 [116] |
EiPTP2/P0CAT4 | 275 | lysine-rich, RGD motif, N-glycosylation and signal peptide | 30 | Peuvel et al., 2002 [116] | |
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 [110] Xu et al., 2004 [113] Peuvel et al., 2002 [116], |
EhPTP2/P0CAT5 | 272 | lysine-rich, N-glycosylation, RGN motif and signal peptide, localized on the whole polar | 30 | Peuvel et al., 2002 [116] | |
EhPTP4/I6UDI1 | 278 | signal peptide, located at the tip of the PT, N-, O-glycosylation | 36 | Han et al., 2017 [22] | |
Nosema bombycis | NbPTP1/R0MQM8 | 409 | signal peptide, O-glycosylation, phosphorylation, localized on the whole PT | 55 | Wu et al., 2014 [126] |
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 [67] Wang et al., 2007 [127] Yi et al., 2019 [128] | |
NbPTP3/J7EQ15 | 1370 | PI = 6.73, interacted with SWP5, localized on the whole PT | 150 | Li et al., 2012 [67] Wang et al., 2007 [127] | |
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 [129] | |
NbPTP5/R0KWI6 | 271 | PI = 8.68, located at the front end of the PT and around the anchor disk | 32.5 | Liu, 2019 [129] | |
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 [117] | |
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 [67,68] | |
NbSWP7/B3STP1 | 287 | PI = 4.78, located in the PT and spore wall. | 32.8 | Yang et al., 2015 [69] | |
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 [69] | |
Enterocytozoon hepatopenaei | EhpPTP2/A0A1W0E7X7 | 284 | PI = 8.8, rich in lysine, super family domain (pfam17022), O-glycosylation | 32 | Wang et al., 2021 [130] |
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 [131] |
AlPTP2/C8CG41 | 287 | PI = 9.1, signal peptide, O-glycosylation, rich in lysine, localized on the whole PT | 29 | Polonais et al., 2005 [131], | |
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 [132] | |
AlPTP2c/C8CG43 | 599 | signal peptide, PI = 8.7, O-glycosylation, rich glycine and serine, b-turn structures | 56 | Polonais et al., 2013 [132] | |
Paranosema grylli | PgPTP1/- | 351 | PI = 5.2, acidic and proline-rich, N-glycosylation, interact with the ConA | 33 | Polonais et al., 2005 [131] |
PgPTP2/- | 287 | PI = 8.9, rich in lysine | 29 | Polonais et al., 2005 [131] | |
Nosema pernyi | NpPTP1/A0A482G4U9 | 394 | PI = 5.82, signal peptide | 39.16 | Wang et al., 2019 [133] |
NpPTP2/A0A482G3T3 | 277 | PI = 9.39, signal peptide | 30.8 | Wang et al., 2019 [133] | |
NpPTP3/A0A0N7ABT9 | 1370 | PI = 6.52, localized on the whole polar | 148.56 | Wang et al., 2019 [133] |
3. Spore Germination: Major Unanswered Questions
3.1. What Is the Initial Germination Signal and Receptor of Microsporidia?
3.2. How Do the Germination Signals Stimulate Microsporidian Polar Filament to Eject?
3.3. How Do Polar Tube Ejections Happen and Where Does the Energy Come from?
3.4. How Do Nuclei Pass through the PT?
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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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 [60] |
EcEnP1/Q8SWL3 | 357 | 9.07 | Endospore | HBM | 40.5 | Southern et al., 2007 [61] Peuvel et al., 2006 [62] | |
EcEnP2/EcSWP3/Q8SWI4 | 221 | 8.42 | Endospore | glycosylphosphatidylinositol (GPI) anchored and O-glycosylation sites | 22 | Peuvel et al., 2007 [62] Xu et al., 2006 [63] | |
EcCDA/Q8SU65 | 254 | 4.43 | Endospore,plasma membrane | Glycoside hydrolase and deacetylase | 28.1 | Brosson et al., 2005 [64] | |
Encephalitozoon intestinalis | EiSWP1/Q95WA3 | 388 | 4.78 | Exospore | - | 41 | Hayman et al., 2001 [65] |
EiSWP2/Q95WA4 | 1002 | 3.68 | Exospore | Repeating of amino-acid units | 107 | Hayman et al., 2001 [65] | |
EiEnP1/A7TZU4 | 348 | 8.84 | Exospore,endospore and polar membrane layer | HBM | 39.1 | Southern et al., 2007 [61] | |
Encephalitozoon hellem | EhSWP1a/C3VJR1 | 509 | 4.30 | Exospore | - | 55 | Polonais et al., 2010 [66] |
EhSWP1b/C3VJR2 | 533 | 4.64 | Exospore | - | 60 | Polonais et al., 2010 [66] | |
Nosema bombycis | NbSWP1/B3STN5 | 278 | 7.95 | Endospore | - | 30.4 | Wu et al., 2008 [45] |
NbSWP2/B3STN6 | 268 | 8.45 | Endospore | HBM | 25.3 | Wu et al., 2008 [45] | |
NbSWP3/B3STN7 | 316 | 7.29 | Exospore | - | 32.7 | Wu et al., 2008 [45] | |
NbSWP5/G0Z414 | 186 | 4.39 | Endospore and PT | Interacts with PTP2 and PTP3 | 20.3 | Li et al., 2012 [67,68] | |
NbSWP7/B3STP1 | 287 | 4.78 | Exospore and endospore | Interacts with NbSWP9 | 32.8 | Yang et al., 2015 [69] | |
NbSWP9/R0MLT0 | 367 | 8.32 | Exospore, endospore and PT | Interacts with PTP1, PTP2 and NbSWP9 | 42.8 | Yang et al., 2015 [69] | |
NbSWP11/B3STP5 | 446 | 9.27 | Exospore and endospore | DnaJ domain and HBM | 52.3 | Yang et al., 2014 [70] | |
NbSWP12/B3STP6 | 228 | 6.78 | Exospore, endospore, membrane of meront | BAR-2 domain and HBM | 26.6 | Chen et al., 2013 [71,72,73] | |
NbSWP16/R0MN98 | 211 | 8.42 | Exospore | HBM and proline-rich tandem repeats | 44 | Wang et al., 2015 [74] | |
NbSWP26/B9UJ97 | 223 | 5.09 | Exospore | HBM and N-glycosylation sites | 25.7 | Li et al., 2009 [75] | |
Unnamed/EOB13250 | 244 | 10.24 | Endospore | Transmembrane domain | 28 | Wang et al., 2020 [76] | |
Nosema ceranae | Unnamed/A0A0F9WE74 | 226 | 6.84 | Endospore | - | 26.19 | Liang et al., 2021 [77] |
NcSWP8/A0A0F9WIV3 | 172 | 4.00 | - | Promote proliferation | 19.5 | He et al., 2021 [78] | |
NcSWP12/A0A0F9WTX8 | 229 | 7.88 | - | Promote proliferation | 26.7 | He et al., 2021 [78] | |
Enterocytozoon hepatopenaei | EhSWP1/A0A1W0E3P7 | 228 | 8.45 | Exospore and endospore | Exospore and endospore | 27 | Jaroenlak et al., 2018 [79] |
EhSWP2/A0A1W0E3S3 | 228 | 5.12 | - | MICSWaP domains | 25.7 | Li et al., 2021 [80] | |
EhSWP3/A0A1W0E914 | 249 | Exospore and endospore | transmembrane domains | 27.1 | Fan et al., 2022 [81] | ||
EhSWP7/A0A1W0E705 | 250 | 5.04 | - | - | 25.3 | Li et al., 2021 [80] | |
EhEnp1/A0A1W0E696 | 333 | 8.86 | - | - | 38.3 | Li et al., 2021 [80] | |
Antonospora locustae (formerly Nosema locustae) | AlocSWP2/A0A1W0E3S3 | 222 | 5.16 | Exospore and endospore | HBM | 25 | Chen et al., 2017 [82] |
EbSWP1/B7XHM5 | 228 | 7.06 | - | O-linked glycosylation site | 26.8 | Meng et al., 2022 [83] | |
Enterocytozoon bieneusi | EbSWP2/B7XJH4 | 247 | 9.46 | - | N-linked glycosylation sites | 29.2 | Meng et al., 2022 [83] |
EbSWP3/B7XHL8 | 229 | 5.15 | - | N-linked glycosylation sites | 25.9 | Meng et al., 2022 [83] | |
NpSWP1/A0A060A4C2 | 278 | 7.02 | Endospore | Transmembrane | 32 | Zhu et al., 2014 [84] | |
Nosema pernyi | NpSWP9/A0A0N7AC01 | 317 | 5.75 | - | - | 37.16 | Ma et al., 2017 [85] |
NpSWP12/A0A0S2EGT8 | 228 | 5.96 | - | BAR domain | 26.6 | Feng et al., 2015 [86] | |
Nosema antheraeae | NaSWP8/G3CU65 | 161 | 4.802 | - | HBM | 18.4 | Xi et al., 2010 [87] |
Germination Stages | Known Information | Information Gaps |
---|---|---|
Activation | Spores may be triggered by pH changes, alkali metal ions (e. g. Na+, K+, Ca2+), anions (e. g. Cl−, CO32−, Br−), and other stimuli | The mechanisms by which receptors are triggered in vivo and the path of signaling in activation. |
Increase of intrasporal osmotic pressure | An increased intrasporal osmotic pressure may be caused by trehalase, acyl-CoA oxidase, catalase, permeases, and some transporters. As soon as the spores absorb water through functional aquaporins, swelling of the polaroplasts and posterior vacuoles occurs. | The main substances that cause changes of intrasporal osmotic pressure. A challenge in understanding osmolarity increases is identifying the signaling pathway. |
PT eversion | The subtilisin-like protease or chitinase may play a key role during the PT firing occurs. | The details of the PT structure, the energy source, and the ejection of the PT are still unclear. |
Sporoplasm passage | As soon as the PT extend a half, the nuclei deform to fit into the PT and exit from the spore coat. Vesicles can be observed in the extruded PT. Sporoplasm returns to a circular shape in the tip of PT. | The sources of energy, regulation of the nuclear phases and deformation of sporoplasm are difficult to understand. |
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Huang, Q.; Chen, J.; Lv, Q.; Long, M.; Pan, G.; Zhou, Z. Germination of Microsporidian Spores: The Known and Unknown. J. Fungi 2023, 9, 774. https://doi.org/10.3390/jof9070774
Huang Q, Chen J, Lv Q, Long M, Pan G, Zhou Z. Germination of Microsporidian Spores: The Known and Unknown. Journal of Fungi. 2023; 9(7):774. https://doi.org/10.3390/jof9070774
Chicago/Turabian StyleHuang, Qingyuan, Jie Chen, Qing Lv, Mengxian Long, Guoqing Pan, and Zeyang Zhou. 2023. "Germination of Microsporidian Spores: The Known and Unknown" Journal of Fungi 9, no. 7: 774. https://doi.org/10.3390/jof9070774