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Host-Microsporidia Interactions in , a Model Nematode Host

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  • Author: Emily R. Troemel1
  • Editors: Joseph Heitman2, Timothy Y. James3, Pedro W. Crous4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Division of Biological Sciences, Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, CA 92093; 2: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 3: Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109-1048; 4: CBS-KNAW Fungal Diversity Centre, Royal Dutch Academy of Arts and Sciences, Utrecht, The Netherlands
  • Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0003-2016
  • Received 02 March 2016 Accepted 02 June 2016 Published 21 October 2016
  • E. R. Troemel, etroemel@ucsd.edu
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  • Abstract:

    Microsporidia comprise a phylum of obligate intracellular pathogens related to fungi that infect virtually all animals. Recently, the nematode has been developed as a convenient model for studying microsporidia infection in a whole-animal host through the identification and characterization of a natural microsporidian pathogen of this commonly studied laboratory organism. The natural microsporidian pathogen is named , and it causes a lethal intestinal infection in . Comparison of the genomes of and its closely related species sp. 1, together with the genomes of other microsporidian species, has provided insight into the evolutionary events that led to the emergence of the large, specialized microsporidia phylum. Cell biology studies of infection in have shown how restructures host intestinal cells and, in particular, how it hijacks host exocytosis for nonlytic exit to facilitate transmission. Recent results also show how the host responds to infection with ubiquitin-mediated responses, and how a natural variant of is able to clear infection, but only during early life. Altogether, these studies provide insight into the mechanisms of microsporidia pathogenesis using a whole-animal host.

  • Citation: Troemel E. 2016. Host-Microsporidia Interactions in , a Model Nematode Host. Microbiol Spectrum 4(5):FUNK-0003-2016. doi:10.1128/microbiolspec.FUNK-0003-2016.

Key Concept Ranking

Single Nucleotide Polymorphism
0.4463501
Nematocida parisii
0.43627453
0.4463501

References

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5. Bakowski MA, Luallen RJ, Troemel ER. 2014. Microsporidia infections in Caenorhabditis elegans and other nematodes, p 341–356. In Weiss LM, Becnel JJ (ed), Microsporidia: Pathogens of Opportunity. Wiley-Blackwell, Hoboken, NJ.
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8. Williams BA. 2009. Unique physiology of host-parasite interactions in microsporidia infections. Cell Microbiol 11:1551–1560 http://dx.doi.org/10.1111/j.1462-5822.2009.01362.x. [PubMed][CrossRef]
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11. Corradi N, Pombert JF, Farinelli L, Didier ES, Keeling PJ. 2010. The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis. Nat Commun 1:77 http://dx.doi.org/10.1038/ncomms1082. [CrossRef]
12. Luallen RJ, Bakowski MA, Troemel ER. 2015. Characterization of microsporidia-induced developmental arrest and a transmembrane leucine-rich repeat protein in Caenorhabditis elegans. PLoS One 10:e0124065 http://dx.doi.org/10.1371/journal.pone.0124065. [CrossRef]
13. Bakowski MA, Priest M, Young S, Cuomo CA, Troemel ER. 2014. Genome sequence of the microsporidian species Nematocida sp1 strain ERTm6 (ATCC PRA-372). Genome Announc 2:e00905-14 doi:11.1128/genomeA.00905-14 [PubMed]
14. Selman M, Sak B, Kvac M, Farinelli L, Weiss LM, Corradi N. 2013.Extremely reduced levels of heterozygosity in the vertebrate pathogen Encephalitozoon cuniculi. Eukaryot Cell 12:496–502. doi:10.1128/EC.00307-12. PubMed PMID: 23376943; PubMed Central PMCID: PMCPMC3623448. [PubMed]
15. Ni M, Feretzaki M, Sun S, Wang X, Heitman J. 2011. Sex in fungi. Annu Rev Genet 45:405–430 http://dx.doi.org/10.1146/annurev-genet-110410-132536. [PubMed][CrossRef]
16. Tsaousis AD, Kunji ER, Goldberg AV, Lucocq JM, Hirt RP, Embley TM. 2008. A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453:553–556 http://dx.doi.org/10.1038/nature06903. [PubMed][CrossRef]
17. Katinka MD, Duprat S, Cornillot E, Méténier G, Thomarat F, Prensier G, Barbe V, Peyretaillade E, Brottier P, Wincker P, Delbac F, El Alaoui H, Peyret P, Saurin W, Gouy M, Weissenbach J, Vivarès CP. 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450–453 http://dx.doi.org/10.1038/35106579. [PubMed][CrossRef]
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21. Szumowski SC, Estes KA, Troemel ER. 2012. Preparing a discreet escape: microsporidia reorganize host cytoskeleton prior to non-lytic exit from C. elegans intestinal cells. Worm 1:207–211 http://dx.doi.org/10.4161/worm.20501. [CrossRef]
22. Estes KA, Szumowski SC, Troemel ER. 2011. Non-lytic, actin-based exit of intracellular parasites from C. elegans intestinal cells. PLoS Pathog 7:e1002227. doi:10.1371/journal.ppat.1002227 PPATHOGENS-D-11-00634 [pii]. PubMed PMID: 21949650; PubMed Central PMCID: PMC3174248. [PubMed][CrossRef]
23. Szumowski SC, Botts MR, Popovich JJ, Smelkinson MG, Troemel ER. 2014. The small GTPase RAB-11 directs polarized exocytosis of the intracellular pathogen N. parisii for fecal-oral transmission from C. elegans. Proc Natl Acad Sci USA 111:8215–8220 http://dx.doi.org/10.1073/pnas.1400696111. [CrossRef]
24. Szumowski SC, Estes KA, Popovich JJ, Botts MR, Sek G, Troemel ER. 2015. Small GTPases promote actin coat formation on microsporidian pathogens traversing the apical membrane of Caenorhabditis elegans intestinal cells. Cell Microbiol 18:30–45 doi:10.1111/cmi.12481. [CrossRef]
25. Bakowski MA, Desjardins CA, Smelkinson MG, Dunbar TL, Lopez-Moyado IF, Rifkin SA, Cuomo CA, Troemel ER. 2014. Ubiquitin-mediated response to microsporidia and virus infection in C. elegans. PLoS Pathog 10:e1004200 (Erratum 10:e1004371) http://dx.doi.org/10.1371/journal.ppat.1004200. [PubMed]
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27. Balla KM, Andersen EC, Kruglyak L, Troemel ER. 2015. A wild C. elegans strain has enhanced epithelial immunity to a natural microsporidian parasite. PLoS Pathog 11:e1004583 http://dx.doi.org/10.1371/journal.ppat.1004583. [CrossRef]
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2016-10-21
2017-09-25

Abstract:

Microsporidia comprise a phylum of obligate intracellular pathogens related to fungi that infect virtually all animals. Recently, the nematode has been developed as a convenient model for studying microsporidia infection in a whole-animal host through the identification and characterization of a natural microsporidian pathogen of this commonly studied laboratory organism. The natural microsporidian pathogen is named , and it causes a lethal intestinal infection in . Comparison of the genomes of and its closely related species sp. 1, together with the genomes of other microsporidian species, has provided insight into the evolutionary events that led to the emergence of the large, specialized microsporidia phylum. Cell biology studies of infection in have shown how restructures host intestinal cells and, in particular, how it hijacks host exocytosis for nonlytic exit to facilitate transmission. Recent results also show how the host responds to infection with ubiquitin-mediated responses, and how a natural variant of is able to clear infection, but only during early life. Altogether, these studies provide insight into the mechanisms of microsporidia pathogenesis using a whole-animal host.

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Figures

Image of FIGURE 1
FIGURE 1

microsporidia infecting the intestine at the meront stage. meronts are labeled with a fluorescent probe for rRNA in red, the intestine is labeled with cytoplasmic GFP in green, and DNA is labeled with DAPI in blue. DAPI, 4′,6-diamidino-2-phenylindole; GFP, green fluorescent protein. (Image credit Susannah Szumowski.)

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0003-2016
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Image of FIGURE 2
FIGURE 2

restructures intestinal cells and exits via RAB-11-directed apical exocytosis. exit from intestinal cells is a two-phase process. Phase 1: When replicates as a meront inside intestinal cells, the actin isoform ACT-5 is no longer restricted to just the apical side and instead appears to be ectopically expressed on the basolateral side of the cell. This relocalization may trigger gaps in the terminal web that occur just as spores begin to form in the intestinal cell. Phase 2: spores are found in separate membrane-bound compartments, become coated in the host small GTPase RAB-11, which is required for spore-containing compartments to fuse with the apical membrane and allow spores to exit into the lumen.

Source: microbiolspec October 2016 vol. 4 no. 5 doi:10.1128/microbiolspec.FUNK-0003-2016
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