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Protistology Overview of Microsporidia and Microsporidiosis 1 Protistology 5 (4), 243–255 (2008) Protistology Overview of microsporidia and microsporidiosis 1 Elizabeth S. Didier 1 and Louis M. Weiss 2 1 Division of Microbiology, Tulane National Primate Research Center, Covington, LA, U.S.A. 2 Departments of Medicine and Pathology, Albert Einstein College of Medicine, Bronx, NY, U.S.A. Summary Microsporidia infections occur in virtually all invertebrate and vertebrate hosts, including mammals. In humans these small single-celled eukaryotic organisms have been recognized as emerging and opportunistic pathogens associated with a wide range of clinical syndromes in persons with HIV/AIDS, travelers, children, organ transplant recipients, and the elderly. The most common microsporidia infecting humans are Enterocytozoon bieneusi and members of the Encephalitozoonidae. These infections are often overlooked due to the small size of the infectious agents. Albendazole is effective for treating infections by Encephalitozoon spp., but no effective drug has been identified for treating E. bieneusi infections. Furthermore, it is dif- ficult to study E. bieneusi because tissue culture and small animal models that simulate human infections are lacking. There is still debate about whether microsporidian infections remain persistent in asymptomatic immune-competent individuals, reactivate during conditions of immune-compromise, or are transmitted to other people under risk circumstances such as pregnancy or organ donation. Reliable serological diagnostic methods are needed to supple- ment PCR or histochemistry when spore shedding may be sporadic. The microsporidia have also generated much interest because of their reduced and compact genomes, and comparative molecular and phylogenetic studies continue to support a relationship between the microspo- ridia and fungi. Key words: Microsporidia, Enterocytozoon, Encephalitozoon, opportunistic infection, emerg- ing infection, therapeutics, diagnostic testing, genomics, proteomics Introduction species have been identified as infectious agents of humans (Table 1). Enterocytozoon bieneusi and the The phylum Microsporidia comprises nearly 1200 Encephalitozoon spp. are the most prevalent micro- species of single-celled, obligate intracellular, eukary- sporidia identified in humans (Weber et al., 2000; otic parasites that infect animals of virtually all ani- Didier, 2005; Didier and Weiss, 2006). Molecular mal phyla, particularly fish and insects (Canning et epidemiology studies are generating a broader un- al., 1986; Larsson, 2005; Vossbrinck and Debrunner- derstanding about the wide demographic, geo- Vossbrinck, 2005). Since they were discovered to be graphic, zoonotic, and environmental range of the a cause of persistent diarrhea and systemic disease microsporidia that infect humans, and the detection in persons with AIDS, the interest of the biomedi- of human-infecting microsporidia in water sources cal community in these organisms has grown tre- led to their inclusion into the NIH Category B list mendously (Desportes et al., 1985). Currently, 14 of biodefense pathogens and the EPA microbial con- 1 Materials presented on the V European Congress of Protistology (July 23–27, 2007, St. Petersburg, Russia). © 2008 by Russia, Protistology 244 • Elizabeth S. Didier and Louis M. Weiss Table 1. Species of microsporidia infecting humans Microsporidia species Sites of infection a Anncaliia (syns. Nosema and Brachiola) algerae Eye, muscle Anncaliia (syns. Nosema and Brachiola) connori Systemic Anncaliia (syns. Nosema-like and Brachiola) vesicularum Muscle a Encephalitozoon (syn. Nosema) cuniculi Systemic, eye, respiratory tract, urinary tract, liver, peritoneum, brain a Encephalitozoon hellem Eye, respiratory tract, urinary tract, systemic a Encephalitozoon (syn. Septata) intestinalis Intestine, biliary tract, respiratory tract, bone, skin, systemic Enterocytozoon bieneusi Intestine, biliary tract, respiratory tract Microsporidium africanum (syn. Nosema sp.) Eye Microsporidium ceylonensis (syn. Nosema sp.) Eye Nosema ocularum Eye Pleistophora ronneafiei (syn. Pleistophora sp.) Muscle a Trachipleistophora anthropopthera Systemic, eye a Trachipleistophora hominis Muscle, eye a Vittaforma corneae (syn. Nosema corneum) Eye, urinary tract a - Species that can be grown in long-term culture. taminant candidates list of concern for waterborne 2007). The cytoplasm of a microsporidian spore con- transmission (Didier and Weiss, 2006). Completion sists of a nucleus in a monokaryon or diplokaryon of the Encephalitozoon cuniculi genome (Katinka arrangement, an anterior anchoring disk, a membra- et al., 2001) and the ongoing genome projects on nous lamellar polaroplast that appears to include an Anncaliia (syn. Brachiola, Nosema) algerae, Spraguea atypical Golgi apparatus, polar vesicles that are likely lophii, Antonospora (syn. Nosema) locustae, and E. to be reduced mitochondria called mitosomes, endo- bieneusi are offering new insights into the genom- plasmic reticulum, ribosomes, and a poster vacuole ics, proteomics, and basic biology of the microspo- (Vavra and Larsson, 1999; Vivares et al., 2002; Vavra, ridia (Keeling et al., 2005; Texier et al., 2005; Tzipori, 2005; Burri et al., 2006; Beznoussenko et al., 2007). 2007). This review summarizes recent research on Polar tube: Microsporidia possess a unique the microsporidia and microsporidiosis with an em- structure, the polar tube, which infects the host cell phasis on infections of humans. during germination (Keohane and Weiss, 1999). The coiled polar tube emanates from the anchoring disk The microsporidian spore and coils numerous times within the posterior region of the spore. A change in osmotic pressure results in General features. Unlike bacterial spores that are swelling of the posterior vacuole and causes the polar generated in response to environmentally stressful tube to evert, followed by transfer of the cytoplasmic conditions, microsporidia spores develop as the ma- contents through the 50–500 µM-long polar tube in- ture and infectious stage of the life cycle. Similarly to to the host cell (Weidner et al., 1994; Frixione et al., bacterial spores, microsporidian spores are resistant 1997) (Figure 1). The mechanism(s) of germination and survive for long periods of time in the environ- and polar tube formation remain to be determined. ment (Fayer, 2004). Spores of the microsporidian In addition, the mechanism by which the sporoplasm species that infect mammals are relatively small, penetrates its host cell has not been resolved. At measuring 1.0-3.0 µM by 1.5-4.0 µM. Spores are lease five polar tube proteins have been identified as surrounded by a glycoprotein outer layer and a chi- components of the microsporidian polar tube using tinous inner layer (Vavra et al., 1993; Metenier and proteomic approaches (Polonais et al., 2007, Weiss et Vivares, 2001; Southern et al., 2007). Several proteins al., unpublished data). These proteins appear to be have been identified in the spore wall and endospore partially conserved among the microsporidia species including SWP1, SWP2, SWP3 (EnP2) and EnP1 studied to date but share little or no homology with (Peuvel-Fanget et al., 2006, Xu et al., 2006). Some of other proteins researched through various databases, these proteins (i.e. EnP1) may be involved in spore suggesting that the polar tube proteins define a novel wall adhesion to host cells or mucin, thereby play- family of proteins (Polonais et al., 2005). Ptp1, which ing a role in the process of invasion (Southern et al., is the most abundant component of the polar tube, is Protistology • 245 Fig. 1. Life cycle of Encephalitozoon and Enterocytozoon species of microsporidia in humans. The majority of infections are believed to occur by ingestion or inhalation of infectious microsporidia spores which are the mature stages of these organisms. Infections are believed to occasionally occur by direct contact or trauma. Vertical transmission in humans has not been reported to occur. Spores are typically shed with the feces, urine, and possibly with respiratory secretions and mucus. This image is reprinted with permission from the DPDx website of the Centers for Disease Control and Prevention (http://www.dpd.cdc.gov/dpdx/). 246 • Elizabeth S. Didier and Louis M. Weiss modified by the addition of O-linked mannose resi- overlapping coding regions (Vivares et al., 2002; dues, which probably play a role in the adhesion of Keeling et al., 2005; Texier et al., 2005; Williams et the polar tube to host cells (Xu et al., 2003; Peek et al., al., 2005). The genome sizes of the Microsporidia are 2005). Ptp1 and ptp2 both contain cysteine residues currently estimated to range from 2.3 Mb on 11 chro- and appear to interact with each other. Ptp4 local- mosomes for E. intestinalis to 19.5 Mb on 16 chromo- izes to the end of the polar tube and may have a role somes for Glugea atherinae (Metenier and Vivares, in adherence to the host cell or in the final process of 2001). Microsporidia lack many of the genes encod- invasion (Polonais et al., 2005; Polonais et al., 2007). ing proteins in metabolic and regulatory pathways, Serum from patients known to have been infected and retain those related to transport of energy sourc- with microsporidia express antibodies which bind es and metabolites, presumably as a consequence of to the polar tube, suggesting that ptps may serve as host cell dependence (Vivares et al., 2002; Keeling serological diagnostic antigens (van Gool et al., 2004; and Slamovits, 2004, 2005; Texier et al., 2005). In Peek et al., 2005). addition, sporoblast
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