1887

Microbiology Society logo

Volume 160, Issue 2

Commitment to cyst formation in Free

Abstract

trophozoites differentiate into infectious cysts (encystment) in response to physiological stimuli; encystment is crucial for ’s transmission, survival and pathogenesis. , encysts when bile sequesters lipids necessary for this lipid auxotroph, and they encyst to infect new hosts. In this study, we investigated, for the first time, commitment to encystment in using both molecular and cellular techniques. We show that after 3–6 h in inducing conditions, encysting trophozoites continue to encyst regardless of whether the inducing stimulus remains. We propose that a trophozoite’s inability to revert to a growing or dividing trophozoite represents a commitment to encystment. The onset of commitment correlated with the appearance of encystment specific vesicles (ESVs) and encystment specific protein synthesis. These observations suggest the involvement of regulatory pathways with the ability to ‘remember’ a transient signal long after its removal; a property that enables encysting trophozoites to complete the encystment process should the unfavourable triggering condition(s) change. The ability to form cysts in response to transient signals or, as we have highlighted in this paper, the ability of a small percentage of the population to form cysts without an inducer is vital for the maintenance of infection within populations.

  • Received:
  • Accepted:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.072405-0
2014-02-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/2/330.html?itemId=/content/journal/micro/10.1099/mic.0.072405-0&mimeType=html&fmt=ahah

References

  1. Adam R. D. ( 2001). Biology of Giardia lamblia . Clin Microbiol Rev 14:447–475 [View Article][PubMed]
     [Google Scholar]
  2. Bagowski C. P., Ferrell J. E. Jr ( 2001). Bistability in the JNK cascade. Curr Biol 11:1176–1182 [View Article][PubMed]
     [Google Scholar]
  3. Bradford M. M. ( 1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 [View Article][PubMed]
     [Google Scholar]
  4. Cotton J. A., Beatty J. K., Buret A. G. ( 2011). Host parasite interactions and pathophysiology in Giardia infections. Int J Parasitol 41:925–933 [View Article][PubMed]
     [Google Scholar]
  5. Davids B. J., Mehta K., Fesus L., McCaffery J. M., Gillin F. D. ( 2004). Dependence of Giardia lamblia encystation on novel transglutaminase activity. Mol Biochem Parasitol 136:173–180 [View Article][PubMed]
     [Google Scholar]
  6. Dubnau D., Losick R. ( 2006). Bistability in bacteria. Mol Microbiol 61:564–572 [CrossRef]
     [Google Scholar]
  7. Dworkin J., Losick R. ( 2005). Developmental commitment in a bacterium. Cell 121:401–409 [View Article][PubMed]
     [Google Scholar]
  8. Ellis J. G. IV, Davila M., Chakrabarti R. ( 2003). Potential involvement of extracellular signal-regulated kinase 1 and 2 in encystation of a primitive eukaryote, Giardia lamblia. Stage-specific activation and intracellular localization. J Biol Chem 278:1936–1945 [View Article][PubMed]
     [Google Scholar]
  9. Erlandsen S. L., Macechko P. T., van Keulen H., Jarroll E. L. ( 1996). Formation of the Giardia cyst wall: studies on extracellular assembly using immunogold labeling and high resolution field emission SEM. J Eukaryot Microbiol 43:416–430 [View Article][PubMed]
     [Google Scholar]
  10. Faubert G., Reiner D. S., Gillin F. D. ( 1991). Giardia lamblia: regulation of secretory vesicle formation and loss of ability to reattach during encystation in vitro. Exp Parasitol 72:345–354 [View Article][PubMed]
     [Google Scholar]
  11. Ferrell J. E. Jr ( 2002). Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr Opin Cell Biol 14:140–148 [View Article][PubMed]
     [Google Scholar]
  12. Ferrell J. Jr, Xiong W. ( 2001). Bistability in cell signaling: How to make continuous processes discontinuous, and reversible processes irreversible. Chaos 11:221–236[PubMed] [CrossRef]
     [Google Scholar]
  13. Gerwig G. J., van Kuik J. A., Leeflang B. R., Kamerling J. P., Vliegenthart J. F. G., Karr C. D., Jarroll E. L. ( 2002). The Giardia intestinalis filamentous cyst wall contains a novel beta(1-3)-N-acetyl-D-galactosamine polymer: a structural and conformational study. Glycobiology 12:499–505 [View Article][PubMed]
     [Google Scholar]
  14. Gillin F. D., Boucher S. E., Rossi S. S., Reiner D. S. ( 1989). Giardia lamblia: the roles of bile, lactic acid, and pH in the completion of the life cycle in vitro. Exp Parasitol 69:164–174 [View Article][PubMed]
     [Google Scholar]
  15. Hehl A. B., Marti M., Köhler P. ( 2000). Stage-specific expression and targeting of cyst wall protein-green fluorescent protein chimeras in Giardia. . Mol Biol Cell 11:1789–1800 [View Article][PubMed]
     [Google Scholar]
  16. Huang Y. C., Su L. H., Lee G. A., Chiu P. W., Cho C. C., Wu J. Y., Sun C. H. ( 2008). Regulation of cyst wall protein promoters by Myb2 in Giardia lamblia. . J Biol Chem 283:31021–31029 [View Article][PubMed]
     [Google Scholar]
  17. Katoh M., Chen G., Roberge E., Shaulsky G., Kuspa A. ( 2007). Developmental commitment in Dictyostelium discoideum . . Eukaryot Cell 6:2038–2045 [View Article][PubMed]
     [Google Scholar]
  18. Keister D. B. ( 1983). Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 77:487–488 [View Article][PubMed]
     [Google Scholar]
  19. Lopez A. B., Sener K., Jarroll E. L., van Keulen H. ( 2003). Transcription regulation is demonstrated for five key enzymes in Giardia intestinalis cyst wall polysaccharide biosynthesis. Mol Biochem Parasitol 128:51–57 [View Article][PubMed]
     [Google Scholar]
  20. Luján H. D. ( 2011). Mechanisms of adaptation in the intestinal parasite Giardia lamblia. . Essays Biochem 51:177–191[PubMed]
     [Google Scholar]
  21. Lujan H. D., Touz M. C. ( 2003). Protein trafficking in Giardia lamblia. . Cell Microbiol 5:427–434 [View Article][PubMed]
     [Google Scholar]
  22. Macechko P. T., Steimle P. A., Lindmark D. G., Erlandsen S. L., Jarroll E. L. ( 1992). Galactosamine-synthesizing enzymes are induced when Giardia encyst. Mol Biochem Parasitol 56:301–309 [View Article][PubMed]
     [Google Scholar]
  23. Mowatt M. R., Luján H. D., Cotten D. B., Bowers B., Yee J., Nash T. E., Stibbs H. H. ( 1995). Developmentally regulated expression of a Giardia lamblia cyst wall protein gene. Mol Microbiol 15:955–963 [View Article][PubMed]
     [Google Scholar]
  24. Paget T. A., Macechko P. T., Jarroll E. L. ( 1998). Metabolic changes in Giardia intestinalis during differentiation. J Parasitol 84:222–226 [View Article][PubMed]
     [Google Scholar]
  25. Pan Y. J., Cho C. C., Kao Y. Y., Sun C. H. ( 2009). A novel WRKY-like protein involved in transcriptional activation of cyst wall protein genes in Giardia lamblia. . J Biol Chem 284:17975–17988 [View Article][PubMed]
     [Google Scholar]
  26. Reiner D. S., McCaffery J. M., Gillin F. D. ( 2001). Reversible interruption of Giardia lamblia cyst wall protein transport in a novel regulated secretory pathway. Cell Microbiol 3:459–472 [View Article][PubMed]
     [Google Scholar]
  27. Reiner D. S., Ankarklev J., Troell K., Palm D., Bernander R., Gillin F. D., Andersson J. O., Svärd S. G. ( 2008). Synchronization of Giardia lamblia: identification of cell cycle stage-specific genes and a differentiation restriction point. Int J Parasitol 38:935–944 [CrossRef]
     [Google Scholar]
  28. Sener K., van Keulen H., Jarroll E. L. ( 2009) Giardan: synthesis, regulation and inhibition. Giardia and Cryptosporidium382–397 Ortega-Pierres G., other editors. Wallingford, UK: CABI Press; [CrossRef]
     [Google Scholar]
  29. Sha W., Moore J., Chen K., Lassaletta A. D., Yi C. S., Tyson J. J., Sible J. C. ( 2003). Hysteresis drives cell-cycle transitions in Xenopus laevis egg extracts. Proc Natl Acad Sci U S A 100:975–980 [View Article][PubMed]
     [Google Scholar]
  30. Smits W. K., Eschevins C. C., Susanna K. A., Bron S., Kuipers O. P., Hamoen L. W. ( 2005). Stripping Bacillus: ComK auto-stimulation is responsible for the bistable response in competence development. Mol Microbiol 56:604–614 [View Article][PubMed]
     [Google Scholar]
  31. Sun C. H., Palm D., McArthur A. G., Svärd S. G., Gillin F. D. ( 2002). A novel Myb-related protein involved in transcriptional activation of encystation genes in Giardia lamblia. . Mol Microbiol 46:971–984 [View Article][PubMed]
     [Google Scholar]
  32. Sun C. H., McCaffery J. M., Reiner D. S., Gillin F. D. ( 2003). Mining the Giardia lamblia genome for new cyst wall proteins. J Biol Chem 278:21701–21708 [View Article][PubMed]
     [Google Scholar]
  33. Sun C. H., Su L. H., Gillin F. D. ( 2006). Novel plant-GARP-like transcription factors in Giardia lamblia. . Mol Biochem Parasitol 146:45–57 [View Article][PubMed]
     [Google Scholar]
  34. Svärd S. G., Hagblom P., Palm J. E. D. ( 2003). Giardia lamblia – a model organism for eukaryotic cell differentiation. FEMS Microbiol Lett 218:3–7[PubMed]
     [Google Scholar]
  35. Touz M. C., Nores M. J., Slavin I., Carmona C., Conrad J. T., Mowatt M. R., Nash T. E., Coronel C. E., Luján H. D. ( 2002). The activity of a developmentally regulated cysteine proteinase is required for cyst wall formation in the primitive eukaryote Giardia lamblia. . J Biol Chem 277:8474–8481 [View Article][PubMed]
     [Google Scholar]
  36. Van Keulen H., Steimle P. A., Bulik D. A., Borowiak R. K., Jarroll E. L. ( 1998). Cloning of two putative Giardia lamblia glucosamine 6-phosphate isomerase genes only one of which is transcriptionally activated during encystment. J Eukaryot Microbiol 45:637–642 [View Article][PubMed]
     [Google Scholar]
  37. Veening J. W., Smits W. K., Kuipers O. P. ( 2008). Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol 62:193–210 [View Article][PubMed]
     [Google Scholar]
  38. Wang X., Hao N., Dohlman H. G., Elston T. C. ( 2006). Bistability, stochasticity, and oscillations in the mitogen-activated protein kinase cascade. Biophys J 90:1961–1978 [View Article][PubMed]
     [Google Scholar]
  39. Wang C. H., Su L. H., Sun C. H. ( 2007). A novel ARID/Bright-like protein involved in transcriptional activation of cyst wall protein 1 gene in Giardia lamblia. . J Biol Chem 282:8905–8914 [View Article][PubMed]
     [Google Scholar]
  40. Wang Y. T., Pan Y. J., Cho C. C., Lin B. C., Su L. H., Huang Y. C., Sun C. H. ( 2010). A novel pax-like protein involved in transcriptional activation of cyst wall protein genes in Giardia lamblia. . J Biol Chem 285:32213–32226 [View Article][PubMed]
     [Google Scholar]
  41. Xiong W., Ferrell J. E. Jr ( 2003). A positive-feedback-based bistable ‘memory module’ that governs a cell fate decision. Nature 426:460–465 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.072405-0
Loading
Commitment to cyst formation in Giardia
Microbiology 160, 330 (2014); https://doi.org/10.1099/mic.0.072405-0
/content/journal/micro/10.1099/mic.0.072405-0
/content/journal/micro/10.1099/mic.0.072405-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error