Skip to main content Accessibility help

Characterization of a novel spore wall protein NbSWP16 with proline-rich tandem repeats from Nosema bombycis (microsporidia)

  • YING WANG (a1), XIAOQUN DANG (a1) (a2), QIANG MA (a1), FANGYAN LIU (a1), GUOQING PAN (a1), TIAN LI (a1) and ZEYANG ZHOU (a1) (a2)...


Nosema bombycis, a pathogen of silkworm pebrine, is an obligate unicellular eukaryotic parasite. It is reported that the spore wall proteins have essential functions in the adherence and infection process of microsporidia. To date, the information related to spore wall proteins from microsporidia is still limited. Here, a 44 kDa spore wall protein NbSWP16 was characterized in N. bombycis. In NbSWP16, a 25 amino acids signal peptide and 3 heparin binding motifs were predicted. Interestingly, a region that contains 3 proline-rich tandem repeats lacking homology to any known protein was also present in this protein. The immunofluorescence analysis (IFA) demonstrated that distinct fluorescent signals were detected both on the surface of mature spores and the germinated spore coats. Immunolocation by electron microscopy revealed that NbSWP16 localized on the exospore regions. Finally, spore adherence analysis indicated that spore adherence to host cell was decreased more than 20% by anti-NbSWP16 blocking compared with the negative control in vitro. In contrast with anti-NbSWP16, no remarkable decrement inhibition was detected when antibodies of NbSWP16 and NbSWP5 were used simultaneously. Collectively, these results suggest that NbSWP16 is a new exospore protein and probably be involved in spore adherence of N. bombycis.


Corresponding author

* Corresponding author. State Key Laboratory of Silkworm genome Biology, Southwest University, Chongqing 400716, China. E-mail:


Hide All
Becnel, J. and Andreadis, T. G. (1999). Microsporidia in insects. In The Microsporidia and Microsporidiosis (ed. Wittner, M. and Weiss, L. M.), pp. 447501. ASM Press, Washington, DC, USA.
Bohne, W., Ferguson, D. J., Kohler, K. and Gross, U. (2000). Developmental expression of a tandemly repeated, glycine-and serine-rich spore wall protein in the microsporidian pathogen Encephalitozoon cuniculi . Infection and Immunity 68, 22682275.
Cai, S. F., Lu, X. M., Qiu, H. H., Li, M. Q. and Feng, Z. Z. (2011). Identification of a Nosema bombycis (Microsporidia) spore wall protein corresponding to spore phagocytosis. Parasitology 138, 11021109.
Chen, J., Long, M. X., Li, T., Geng, L. N., Li, Z., Yang, D. L., Ma, C., Wu, H. J., Ma, Z. G., Li, C. F., Pan, G. Q. and Zhou, Z. Y. (2013). Identification of a novel chitin-binding spore wall protein (NbSWP12) with a BAR-2 domain from Nosema bombycis (microsporidia). Parasitology 140, 13941402.
Corradi, N., Gangaeva, A. and Keeling, P. J. (2008). Comparative profiling of overlapping transcription in the compacted genomes of microsporidia Antonospora locustae and Encephalitozoon cuniculi . Genomics 91, 388393.
Didier, E., Snowden, K. and Shadduck, J. (1998). Biology of microsporidian species infecting mammals. Advances in Parasitology 40, 283320.
Gemayel, R., Cho, J., Boeynaems, S. and Verstrepen, K. J. (2012). Beyond junk-variable tandem repeats as facilitators of rapid evolution of regulatory and coding sequences. Genes 3, 461480.
Hayman, J. R., Hayes, S. F., Amon, J. and Nash, T. E. (2001). Developmental expression of two spore wall proteins during maturation of the microsporidian Encephalitozoon intestinalis . Infection and Immunity 69, 70577066.
Hayman, J. R., Southern, T. R. and Nash, T. E. (2005). Role of sulfated glycans in adherence of the microsporidian Encephalitozoon intestinalis to host cells in vitro . Infection and Immunity 73, 841848.
Julenius, K., Mølgaard, A., Gupta, R. and Brunak, S. (2005). Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15, 153164.
Katinka, M. D. (2001). Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi . Nature 414, 450453.
Katti, M. V., Sami-Subbu, R., Ranjekar, P. K. and Gupta, V. S. (2000). Amino acid repeat patterns in protein sequences: their diversity and structural-functional implications. Protein Science 9, 12031209.
Li, Y. H., Wu, Z. L., Pan, G. Q., He, W. W., Zhang, R. Z., Hu, J. H. and Zhou, Z. Y. (2009). Identification of a novel spore wall protein (SWP26) from microsporidia Nosema bombycis . International Journal for Parasitology 39, 391398.
Li, Z., Pan, G. Q., Li, T., Huang, W., Chen, J., Geng, L. N., Yang, D. L., Wang, L. L. and Zhou, Z. Y. (2012). SWP5, a spore wall protein, interacts with polar tube proteins in the parasitic microsporidian Nosema bombycis . Eukaryotic cell 11, 229237.
Nageli, K. (1857). Uber die neue Krankheit der Seidenraupe und verwandte Organismen. Bot Z 15, 760761.
Pan, G. Q., Xu, J. S., Li, T., Xia, Q. Y., Liu, S. L., Zhang, G. J., Li, S. G., Li, C. F., Liu, H. D., Yang, L., Liu, T., Zhang, X., Wu, Z. L., Fan, W., Dang, X. Q., Xiang, H., Tao, M. L., Li, Y. H., Hu, J. H., Li, Z., Lin, L. P., Luo, J., Geng, L. N., Wang, L. L., Long, M. X., Wan, Y. J., He, N. J., Zhang, Z., Lu, C., Patrick, J. K. et al. (2013). Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation. BMC genomics 14, 186.
Peuvel-Fanget, I., Polonais, V., Brosson, D., Texier, C., Kuhn, L., Peyret, P., Vivarè, C., Delbac, F. (2006). EnP1 and EnP2, two proteins associated with the Encephalitozoon cuniculi endospore, the chitin-rich inner layer of the microsporidian spore wall. International Journal for Parasitology 36, 309318.
Shadduck, J. A. and Polley, M. B. (1978). Some factors influencing the in vitro infectivity and replication of Encephalitozoon cuniculi . Journal of Eukaryotic Microbiology 25, 491496.
Smith, G. A., Theriot, J. A. and Portnoy, D. A. (1996). The tandem repeat domain in the Listeria monocytogenes ActA protein controls the rate of actin-based motility, the percentage of moving bacteria, and the localization of vasodilator-stimulated phosphoprotein and profilin. Journal of Cell Biology 135, 647660.
Southern, T. R., Jolly, C. E. and Russell Hayman, J. (2006). Augmentation of microsporidia adherence and host cell infection by divalent cations. FEMS Microbiology Letters 260, 143149.
Southern, T. R., Jolly, C. E., Lester, M. E. and Hayman, J. R. (2007). EnP1, a microsporidian spore wall protein that enables spores to adhere to and infect host cells in vitro . Eukaryotic Cell 6, 13541362.
Verstrepen, K. J., Jansen, A., Lewitter, F. and Fink, G. R. (2005). Intragenic tandem repeats generate functional variability. Nature Genetics 37, 986990.
Weidner, E. and Halonen, S. K. (1993). Microsporidian spore envelope keratins phosphorylate and disassemble during spore activation. Journal of Eukaryotic Microbiology 40, 783788.
Weidner, E., Avila, J. and Harris, J. (1992). Cytoskeletal proteins expressed by microsporidian parasites. Subcellular biochemistry. Intracellular Parasites 18, 385399.
Wu, Z. L., Li, Y. H., Pan, G. Q., Tan, X. H., Hu, J. H., Zhou, Z. Y. and Xiang, Z. (2008). Proteomic analysis of spore wall proteins and identification of two spore wall proteins from Nosema bombycis (Microsporidia). Proteomics 8, 24472461.
Xu, Y. J., Peter, T., Ann, C., Wang, F., Zhang, H., George, O., Louis, M. W. (2006). Identification of a new spore wall protein from Encephalitozoon cuniculi . Infection and Immunity 74, 239247.
Yang, D. L., Dang, X. Q., Tian, R., Long, M. X., Li, C. F., Li, T., Chen, J., Li, Z., Pan, G. Q. and Zhou, Z. Y. (2014). Development of an approach to analyze the interaction between Nosema bombycis (microsporidia) deproteinated chitin spore coats and spore wall proteins. Journal of Invertebrate Pathology 115, 17.


Type Description Title
Supplementary materials

Wang Supplementary Material
Supplementary Material

 Unknown (14 KB)
14 KB


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed