Frequent occurrence of mixed enterocytozoon bieneusi infections in humans

Applied and Environmental Microbiology

Volumn 79, Issue 17, 2013, Pages 5357-5362

  Widmer, Giovanni ^a   Dilo, Julia ^a   Tumwine, James K ^b   Tzipori, Saul ^a   Akiyoshi, Donna E ^a  

^a TUFTS UNIVERSITY   (United States)

^b MAKERERE UNIVERSITY COLLEGE OF HEALTH SCIENCES   (Uganda)

Author keywords

[No Author keywords available]

Indexed keywords

GENOTYPING METHODS; HUMAN PATHOGENS; INTERNAL TRANSCRIBED SPACERS; KAMPALA , UGANDA; MICRO SATELLITE; MICROSATELLITE MARKERS; MULTIPLE SEQUENCES; SIMPLE SEQUENCE REPEATS;

CLONING; DNA SEQUENCES; GENES;

POLYMERASE CHAIN REACTION;

DISEASE PREVALENCE; EPIDEMIOLOGY; GENETIC MARKER; GENOME; GENOTYPE; HEALTH RISK; HETEROGENEITY; HOST RANGE; HUMAN GEOGRAPHY; INFECTIOUS DISEASE; POLYMERASE CHAIN REACTION; POLYMORPHISM; SAMPLING;

KAMPALA; UGANDA;

EID: 84884276377     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01260-13     Document Type: Article

References (30)

1. Cali A, Owen RL. 1990. Intracellular development of Enterocytozoon, a unique microsporidian found in the intestine of AIDS patients. J. Protozool. 37:145-155.
2. 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 Encephalitozoon cuniculi. Nature 414:450-453.
3. 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.
4. van Gool T, Hollister WS, Schattenkerk WE, Van den Bergh Weerman MA, Terpstra WJ, van Ketel RJ, Reiss P, Canning EU. 1990. Diagnosis of Enterocytozoon bieneusi microsporidiosis in AIDS patients by recovery of spores from faeces. Lancet 336:697-698.
5. Zhu X, Wittner M, Tanowitz HB, Cali A, Weiss LM. 1994. Ribosomal RNAsequences of Enterocytozoon bieneusi, Septata intestinalis and Ameson michaelis: phylogenetic construction and structural correspondence. J. Eukaryot. Microbiol. 41:204-209.
6. Santin M, Fayer R. 2009. Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. J. Eukaryot. Microbiol. 56:34-38.
7. Widmer G, Akiyoshi DE. 2010. Host-specific segregation of ribosomal nucleotide sequence diversity in the microsporidian Enterocytozoon bieneusi. Infect. Genet. Evol. 10:122-128.
8. Henriques-Gil N, Haro M, Izquierdo F, Fenoy S, del Aguila C. 2010. Phylogenetic approach to the variability of the microsporidian Enterocytozoon bieneusi and its implications for inter- and intrahost transmission. Appl. Environ. Microbiol. 76:3333-3342.
9. Li W, Kiulia NM, Mwenda JM, Nyachieo A, Taylor MB, Zhang X, Xiao L. 2011. Cyclospora papionis, Cryptosporidium hominis, and humanpathogenic Enterocytozoon bieneusi in captive baboons in Kenya. J. Clin. Microbiol. 49:4326-4329.
10. Sulaiman IM, Fayer R, Lal AA, Trout JM, Schaefer FW, III, Xiao L. 2003. Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as humanpathogenic Enterocytozoon bieneusi. Appl. Environ. Microbiol. 69:4495- 4501.
11. Thellier M, Breton J. 2008. Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite 15:349-358.
12. Li N, Xiao L, Wang L, Zhao S, Zhao X, Duan L, Guo M, Liu L, Feng Y. 2012. Molecular surveillance of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi by genotyping and subtyping parasites in wastewater. PLoS Negl. Trop. Dis. 6:e1809. doi:10.1371/journal.pntd .0001809.
13. Akiyoshi DE, Morrison HG, Lei S, Feng X, Zhang Q, Corradi N, Mayanja H, Tumwine JK, Keeling PJ, Weiss LM, Tzipori S. 2009. Genomic survey of the non-cultivatable opportunistic human pathogen, Enterocytozoon bieneusi. PLoS Pathog. 5:e1000261. doi:10.1371/journal .ppat.1000261.
14. Feng Y, Li N, Dearen T, Lobo ML, Matos O, Cama V, Xiao L. 2011. Development of a multilocus sequence typing tool for high resolution genotyping of Enterocytozoon bieneusi. Appl. Environ. Microbiol. 77: 4822-4828.
15. Li W, Cama V, Feng Y, Gilman RH, Bern C, Zhang X, Xiao L. 2012. Population genetic analysis of Enterocytozoon bieneusi in humans. Int. J. Parasitol. 42:287-293.
16. Tumwine JK, Kekitiinwa A, Nabukeera N, Akiyoshi DE, Buckholt MA, Tzipori S. 2002. Enterocytozoon bieneusi among children with diarrhea attending Mulago Hospital in Uganda. Am. J. Trop. Med. Hyg. 67:299- 303.
17. Colwell RK. 2005. EstimateS: statistical estimation of species richness and shared species from samples. Version 7.5. http://purl.oclc.org/estimates.
18. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
19. Li W, Cama V, Akinbo FO, Ganguly S, Kiulia NM, Zhang X, Xiao L. 2013. Multilocus sequence typing of Enterocytozoon bieneusi: lack of geographic segregation and existence of genetically isolated sub-populations. Infect. Genet. Evol. 14:111-119.
20. Peakall R, Smouse PE. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537-2539.
21. Mantel N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Res. 27:209-220.
22. Nielsen K, Yohalem DS. 2001. Origin of a polyploid Botrytis pathogen through interspecific hybridization between Botrytis aclada and B. byssoidea. Mycologia 93:1064-1071.
23. Albertin W, Marullo P. 2012. Polyploidy in fungi: evolution after wholegenome duplication. Proc. Biol. Sci. 279:2497-2509.
24. Gordon JL, Wolfe KH. 2008. Recent allopolyploid origin of Zygosaccharomyces rouxii strain ATCC 42981. Yeast 25:449-456.
25. Dang XQ, Pan GQ, Li T, Lin LP, Ma Q, Geng LN, He YL, Zhou ZY. 2013. Characterization of a subtilisin-like protease with apical localization from microsporidian Nosema bombycis. J. Invertebr. Pathol. 112:166- 174.
26. 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.
27. Nkhoma SC, Nair S, Al-Saai S, Ashley E, McGready R, Phyo AP, Nosten F, Anderson TJ. 2013. Population genetic correlates of declining transmission in a human pathogen. Mol. Ecol. 22:273-285.
28. Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman AH, Nosten F, Ferreira MU, Day KP. 2000. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol. Biol. Evol. 17:1467- 1482.
29. Tanriverdi S, Grinberg A, Chalmers RM, Hunter PR, Petrovic Z, Akiyoshi DE, London E, Zhang L, Tzipori S, Tumwine JK, Widmer G. 2008. Inferences about the global population structures of Cryptosporidium parvum and Cryptosporidium hominis. Appl. Environ. Microbiol. 74:7227-7234.
30. Tumwine JK, Kekitiinwa A, Bakeera-Kitaka S, Ndeezi G, Downing R, Feng X, Akiyoshi DE, Tzipori S. 2005. Cryptosporidiosis and microsporidiosis in Ugandan children with persistent diarrhea with and without concurrent infection with the human immunodeficiency virus. Am. J. Trop. Med. Hyg. 73:921-925.