Extremely reduced levels of heterozygosity in the vertebrate pathogen Encephalitozoon cuniculi

Eukaryotic Cell

Volumn 12, Issue 4, 2013, Pages 496-502

  Selman, Mohammed ^a   Sak, Bohumil ^b   Kváč, Martin ^b   Farinelli, Laurent ^c   Weiss, Louis M ^d   Corradi, Nicolas ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b INSTITUTE OF PARASITOLOGY   (Czech Republic)

^c Fasteris   (Switzerland)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ARTICLE; CLASSIFICATION; DNA SEQUENCE; ENCEPHALITOZOON CUNICULI; FUNGAL GENOME; GENETIC VARIABILITY; GENETICS; HETEROZYGOTE; HOMOZYGOTE; MAMMAL; MICROBIOLOGY; PATHOGENICITY; PHYLOGENY; PLOIDY; SELF FERTILIZATION;

ANIMALS; ENCEPHALITOZOON CUNICULI; GENETIC VARIATION; GENOME, FUNGAL; HETEROZYGOTE; HOMOZYGOTE; MAMMALS; PHYLOGENY; PLOIDIES; SELF-FERTILIZATION; SEQUENCE ANALYSIS, DNA;

ENCEPHALITOZOON; ENCEPHALITOZOON CUNICULI; MICROSPORIDIA; VERTEBRATA;

EID: 84875492810     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00307-12     Document Type: Article

References (41)

1. Keeling PJ, Fast NM. 2002. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu. Rev. Microbiol. 56:93-116.
2. Corradi N, Keeling PJ. 2009. Microsporidia: a journey through radical taxonomical revisions. Fungal Biol. Rev. 23:1-8.
3. Cuomo CA, Desjardins CA, Bakowski MA, Goldberg J, Ma AT, Becnel JJ, Didier ES, Fan L, Heiman DI, Levin JZ, Young S, Zeng Q, Troemel ER. 2012. Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res. 22:2478-2488.
4. Capella-Gutierrez S, Marcet-Houben M, Gabaldon T. 2012. Phylog-enomics supports microsporidia as the earliest diverging clade of se-quenced fungi. BMC Biol. 10:47.
5. Lee SC, Corradi N, Byrnes EJ, III, Torres-Martinez S, Dietrich FS, Keeling PJ, Heitman J. 2008. Microsporidia evolved from ancestral sexual fungi. Curr. Biol. 18:1675-1679.
6. Lee SC, Corradi N, Doan S, Dietrich FS, Keeling PJ, Heitman J. 2010. Evolution of the sex-related locus and genomic features shared in microspo-ridia and fungi. PLoS One 5:e10539. doi:10.1371/journal.pone.0010539.
7. Keeling PJ. 2003. Congruent evidence from alpha-tubulin and beta-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genet. Biol. 38:298-309.
8. Akiyoshi DE, Morrison HG, Lei S, Feng X, Zhang Q., Corradi N, Mayanja H, Tumwine JK, Keeling PJ, Weiss LM and Tzipori S. 2009. Genomic survey of the non-cultivatable opportunistic human pathogen, Enterocytozoon bieneusi. PLoS Pathog. 5:e1000261. doi:10.1371/journal.ppat.1000261.
9. Corradi N, Haag KL, Pombert JF, Ebert D, Keeling PJ. 2009. Draft genome sequence of the Daphnia pathogen Octosporea bayeri: insights into the gene content of a large microsporidian genome and a model for host-parasite interactions. Genome Biology 10:R106.
10. Keeling PJ, Corradi N, Morrison HG, Haag KL, Ebert D, Weiss LM, Akiyoshi DE, Tzipori S. 2010. The reduced genome of the parasitic microsporidian Enterocytozoon bieneusi lacks genes for core carbon metabolism. Genome Biol. Evol. 2:304-309.
11. Pombert JF, Selman M, Burki F, Bardell FT, Farinelli L, Solter LF, Whitman DW, Weiss LM, Corradi N, Keeling PJ. 2012. Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. Proc. Natl. Acad. Sci. U. S. A. 109:12638-12643.
12. Katinka MD, Duprat S, Cornillot E, Metenier 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, Vivares CP. 2001. Genome sequence and gene compaction of the eukaryote parasite Enceph-alitozoon cuniculi. Nature 414:450-453.
13. Corradi N, Pombert JF, Farinelli L, Didier ES, Keeling PJ. 2010. The complete sequence of the smallest known nuclear genome from the mi-crosporidian Encephalitozoon intestinalis. Nat. Commun. 1:77.
14. Selman M, Pombert JF, Solter L, Farinelli L, Weiss LM, Keeling P, Corradi N. 2011. Acquisition of an animal gene by microsporidian intra-cellular parasites. Curr. Biol. 21:R576-R577.
15. Selman M, Corradi N. 2011. Microsporidia: horizontal gene transfers in vicious parasites. Mob Genet. Elements 1:251-255.
16. Schottelius J, Schmetz C, Kock NP, Schuler T, Sobottka I, Fleischer B. 2000. Presentation by scanning electron microscopy of the life cycle of mi-crosporidia of the genus Encephalitozoon. Microbes Infect. 2:1401-1406.
17. Bigliardi E, Sacchi L. 2001. Cell biology and invasion of the microspo-ridia. Microbes Infect. 3:373-379.
18. Biderre C, Mathis A, Deplazes P, Weber R, Metenier G and Vivares CP. 1999. Molecular karyotype diversity in the microsporidian Encephalito-zoon cuniculi. Parasitology 118:439-445.
19. Biderre C, Pages M, Metenier G, Canning EU, Vivares CP. 1995. Evidence for the smallest nuclear genome (2.9 Mb) inthe microsporidium Encephalitozoon cuniculi. Mol. Biochem. Parasitol. 74:229-231.
20. Brugere JF, Cornillot E, Metenier G, Bensimon A and Vivares CP. 2000. Encephalitozoon cuniculi (Microspora) genome: physical map and evidence for telomere-associated rDNA units on all chromosomes. Nucleic Acids Res. 28:2026-2033.
21. Ni M, Feretzaki M, Sun S, Wang X, Heitman J. 2011. Sex in fungi. Annu. Rev. Genet. 45:405-430.
22. Billiard S, Lopez-Villavicencio M, Hood ME, Giraud T. 2012. Sex, outcrossing and mating types: unsolved questions in fungi and beyond. J. Evol. Biol. 25:1020-1038.
23. Didier ES, Vossbrinck CR, Baker MD, Rogers LB, Bertucci DC, Shad-duck JA. 1995. Identification and characterization of three Encephalito-zoon cuniculi strains. Parasitology 111:411- 421.
24. Shadduck JA. 1969. Nosema cuiculi: in vitro isolation. Science 166:516- 517.
25. Vavra J, Bedrnik P, Cinatl J. 1972. Isolation and in vitro cultivation of the mammalian microsporidian Encephalitozoon cuniculi. Folia Parasitol. 19: 349-354.
26. Shadduck JA, Bendele R, Robinson GT. 1978. Isolation of the causative organism of canine encephalitozoonosis. Vet. Pathol. 15:449-460.
27. Aurrecoechea C, Barreto A, Brestelli J, Brunk BP, Caler EV, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Iodice J, Kissinger JC, Kraemer ET, Li W, Nayak V, Pennington C, Pinney DF, Pitts B, Roos DS, Srinivasamoorthy G, Stoeckert CJ, Jr, Treatman C, Wang H. 2011. AmoebaDB and MicrosporidiaDB: functional genomic resources for Amoe-bozoa and Microsporidia species. Nucleic Acids Res. 39:D612-D619.
28. Pombert J-F, Xu J, Smith DR, Heiman D, Young S, Cuomo CA, Weiss LM, Keeling PJ. 2013. Complete genome sequences from three genetically distinct strains reveal high intraspecies genetic diversity in the microspo-ridian Encephalitozoon cuniculi. Eukaryot. Cell 12:496-504.
29. Koudela B, Vítovec J, Kuc ̌erová Z, Ditrich O, Trávnic ̌ek J. 1993. The severe combined immunodeficient mouseasamodel for Encephalitozoon cuniculi microsporidiosis. Folia Parasitol. 40:279 -286.
30. Gerke J, Lorenz K, Cohen B. 2009. Genetic interactions between transcription factors cause natural variation in yeast. Science 323:498-501.
31. Idnurm A. 2011. Sex determination in the first-described sexual fungus. Eukaryot. Cell 10:1485-1491.
32. Wong Sak Hoi J, Dumas B. 2010. Ste12 and Ste12-like proteins, fungal transcription factors regulating development and pathogenicity. Eu-karyot. Cell 9:480-485.
33. Xu X, Sun J, Zhang J, Wellems D, Qing X, McCutchan T, Pan W. 2012. Having a pair: the key to immune evasion for the diploid pathogen Schis-tosoma japonicum. Sci. Rep. 2:346.
34. Heitman J. 2006. Sexual reproduction and the evolution of microbial pathogens. Curr. Biol. 16:R711-R725.
35. Heitman J. 2010. Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host Microbe 8:86-99.
36. Barraclough TG, Birky CW, Jr, Burt A. 2003. Diversification in sexual and asexual organisms. Evolution 57:2166-2172.
37. Balloux F, Lehmann L, de Meeus T. 2003. The population genetics of clonal and partially clonal diploids. Genetics 164:1635-1644.
38. Balloux F, Amos W, Coulson T. 2004. Does heterozygosity estimate inbreeding in real populations? Mol. Ecol. 13:3021-3031.
39. De Meeus T, Lehmann L, Balloux F. 2006. Molecular epidemiology of clonal diploids: a quick overview and a short DIY (do it yourself) notice. Infect. Genet. Evol. 6:163-170.
40. Billiard S, Lopez-Villavicencio M, Devier B, Hood ME, Fairhead C, Giraud T. 2011. Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biol. Rev. Camb. Philos. Soc. 86:421- 442.
41. Kondrashov AS. 1994. The asexual ploidy cycle and the origin of sex. Nature 370:213-216.