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Taxonomy and Species Delimitation in Cryptosporidium

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Taxonomy and Species Delimitation in Cryptosporidium Experimental Parasitology 124 (2010) 90–97 Contents lists available at ScienceDirect Experimental Parasitology journal homepage: www.elsevier.com/locate/yexpr Taxonomy and species delimitation in Cryptosporidium Ronald Fayer Agricultural Research Service, United States Department of Agriculture, Beltsville, MD 20705, USA article info abstract Article history: Amphibians, reptiles, birds and mammals serve as hosts for 19 species of Cryptosporidium. All 19 species Received 24 November 2008 have been confirmed by morphological, biological, and molecular data. Fish serve as hosts for three addi- Received in revised form 20 February 2009 tional species, all of which lack supporting molecular data. In addition to the named species, gene Accepted 6 March 2009 sequence data from more than 40 isolates from various vertebrate hosts are reported in the scientific lit- Available online 18 March 2009 erature or are listed in GenBank. These isolates lack taxonomic status and are referred to as genotypes based on the host of origin. Undoubtedly, some will eventually be recognized as species. For them to Keywords: receive taxonomic status sufficient morphological, biological, and molecular data are required and names Cryptosporidium must comply with the rules of the International Code for Zoological Nomenclature (ICZN). Because the Taxonomy Species ICZN rules may be interpreted differently by persons proposing names, original names might be improp- Fish erly assigned, original literature might be overlooked, or new scientific methods might be applicable to Amphibians determining taxonomic status, the names of species and higher taxa are not immutable. The rapidly Reptiles evolving taxonomic status of Cryptosporidium sp. reflects these considerations. Birds Published by Elsevier Inc. Mammals International Code of Zoological Nomenclature (ICZN) 1. Introduction 2. Standards for taxonomic status in the genus Cryptosporidium Cryptosporidium species infect humans and a wide variety of A taxon is the formal unit and name in taxonomic classification vertebrate animals. Because the oocyst stage responsible for trans- such as a phylum, class, order, family, genus, and species. Rules mission is ubiquitous in the environment cryptosporidiosis can be governing the application of scientific names, at the level of family acquired through several routes: person-to-person contact, contact and below, for all organisms considered animals, which includes with companion and farm animals, and ingestion of contaminated species of Cryptosporidium, are published in the ICZN. Guidelines food, drinking water and recreational water (Beach, 2008; Griffiths, in addition to the Code can be helpful for naming species of Cryp- 1998; MacKenzie et al., 1994; Nichols, 2008; Ortega and Cama, tosporidium. Egyed et al. (2003) proposed that the only acceptable 2008; Tangermann et al., 1991). Because this stage lacks distinctive Cryptosporidium species should be those fully polyphasically char- morphologic features to clearly differentiate Cryptosporidium spe- acterized, including morphologic, biologic and genetic information. cies, identification by microscopy is problematic for determining Xiao et al. (2004b) published a consensus for minimal require- the species infecting humans or animals, the burden of disease ments for new species of Cryptosporidium that included morpho- attributable to different species, and the role of individual species metric data for oocysts, genetic characterization (including in disease or transmission (Fall et al., 2003). Consequently, molec- multilocus characterizations when possible), identification of nat- ular tools are recognized as essential for determining Cryptospori- ural and experimentally infected hosts, and adherence to ICZN dium taxonomy which in turn underlies our ability to understand rules. Jirku et al. (2008) summarized recommendations for naming the biology, epidemiology, and health related importance of vari- new species as those in compliance with ICZN rules and having (i) a ous Cryptosporidium species and those populations referred to as robust description of the oocyst and developmental stages accom- genotypes that have not received recognition as species. The fol- panied by deposition of preserved infected tissue, (ii) biological lowing review addresses taxonomic issues related to organisms characterization, (iii) differential diagnosis supported, if possible, in this genus. by (iv) genetic characterization accompanied by deposit of se- quences and material for further DNA characterization with all deposited material available in a museum or academic institution. Aforementioned guidelines are important for establishing a solid E-mail address: [email protected] taxonomic foundation for Cryptosporidium species to benefit not 0014-4894/$ - see front matter Published by Elsevier Inc. doi:10.1016/j.exppara.2009.03.005 R. Fayer / Experimental Parasitology 124 (2010) 90–97 91 only specialists working with organisms in this genus but also phy- provided evidence that these two routes of infection for humans sicians, veterinarians, sanitarians, and others concerned with food, were related to two genotypes- the ‘‘human genotype” transmitted water and environmental safety issues. from human to human and the ‘‘bovine genotype” transmitted from animals to humans, with cattle as the primary reservoir. 3. Historical perspective regarding species names The former genotype was eventually named Cryptosporidium hom- inis (Morgan-Ryan et al., 2002) and the latter continued to be iden- Ernest Edward Tyzzer named the genus Cryptosporidium and de- tified as C. parvum. When biological and genetic data for other scribed the type species, Cryptosporidium muris, found in gastric genotypes accumulated to the point that they were recognized as glands of laboratory mice, in a two page report (Tyzzer, 1907). unique and distinct they also acquired species names and status. He later published a more detailed description of the life-cycle The canine genotype became Cryptosporidium canis, pig genotype including drawings and photomicrographs and noted that he had I became Cryptosporidium suis, bovine B genotype became Cryptos- observed similar organisms attached to epithelium of the small poridium bovis, and the deer-like genotype became Cryptosporidium intestine of rabbits (Tyzzer, 1910). He observed similar stages in ryanae. This trend, strongly supported by genetic data is expected the intestine of mice and named them Cryptosporidium parvum to continue. (Tyzzer, 1912). This species differed from the type species because it infected the small intestine rather than the stomach, and because 4. Species in fish the oocysts were smaller (Tyzzer, 1912). Characteristics used to identify and name species of Apicom- Studies with wild caught fish present difficulties with regard to plexa traditionally have been based on host specificity, location naming parasites. With little biological data, extremely little of endogenous stages, and morphology of endogenous or exoge- molecular data, and no museum specimens available, there is little nous stages. The characteristic of host specificity was applied to information to provide a clear understanding of the taxonomic sta- the naming of species of Cryptosporidium. For example, oocysts tus of Cryptosporidium infecting fish. Despite this dearth of data, found in sheep feces were named Cryptosporidium agni (Barker two species from fish were given names: Cryptosporidium molnari and Carbonell, 1974), others in human feces were named Cryptos- and Cryptosporidium scophthalmi based on microscopic observa- poridium garnhami (Bird, 1981)orCryptosporidium enteriditis tions of developmental stages in tissue sections. However, because (Qadripur and Klose, 1985), but because these and several other of the lack of both molecular data and museum specimens these named species lacked taxonomic data that could clearly distin- species should be regarded as nomena nudum (Table 1). guish these species from all others (morphological, biological, Cryptosporidium molnari was reported as infecting gilthead sea and/or molecular data) they became nonvalid names. Morphologi- bream (Sparus auratus) and European sea bass (Dicentrarchus labrax) cal characteristics of the exogenous stage (the oocyst) were insuf- primarily in the stomach and seldom in the intestine (Alvarez-Pelli- ficient to distinguish one species from another except for those tero and Sitjà-Bobadilla, 2002). Because neither data nor specimens with ‘‘large” oocysts and those with ‘‘small” oocysts. During much of C. molnari are available for genetic studies, it cannot be confirmed of the 1970s through the 1990s only a single species, Cryptospori- if the isolate identified as C. molnari-like (Ryan et al., 2004a), based dium muris, was thought to parasitize the gastric mucosa of mam- on morphology and location, is the same organism as C. molnari re- mals and that was a species with large oocysts, whereas another ported by Alvarez-Pellitero and Sitjà-Bobadilla (2002). Cryptospori- species, Cryptosporidium parvum, with the small oocysts, was dium scophthalmi was reported as infecting turbot (Psetta maxima) thought to parasitize the intestine of all mammals (Tzipori et al., with stages located mainly in the intestinal epithelium and very sel- 1980). During this time, oocysts from many different animal spe- dom in the stomach (Alvarez-Pellitero et al., 2004). cies including humans were identified and published as C. parvum, The first report of Cryptosporidium in fish described illness in a C. parvum-like or simply
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