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United States Department of Agriculture

Agricultural Research Service


item Becnel, James

Submitted to: Society for Invertebrate Pathology Annual Meeting Proceedings
Publication Type: Proceedings
Publication Acceptance Date: August 18, 2002
Publication Date: August 18, 2002

Technical Abstract: Nosema bombycis, the first described species of microsporidia and etiological agent of Pebrine disease in silkworms, was originally identified as yeast and placed in the Schizomycetes (Naegeli, 1857). Balbiani (1882), after a series of studies on this organism, decided that it lacked essential characters of the Schizomycetes but had affinities to the Sporozoa Leuckart, 1879. He established the taxon "Microsporidies" for N. bombycis and the few known but unnamed species of microsporidia and the group has not been considered related to the Fungi since that time. Recent molecular analyses, however, have determined that the group possesses several gene sequences that suggest this group is closely related to the Fungi (Keeling, 2001; Hirt et al., 1999). Since then, other biological features of the microsporidia and fungi have been analyzed to determine common traits or distinct differences that may provide additional insight on this relationship. However, these comparisons are confounded by widespread convergence and rapid divergence of these groups. Therefore, the following discussion is an attempt, in a very general way, to examine some of the similarities and differences between microsporidia and fungi. It is hoped this will stimulate investigations on both groups to help clarify the many points where information is unclear or lacking. The microsporidia are a large group of strictly obligate, intracellular parasites that infect most animal groups (from Protists to Man) but are not known to infect plants or fungi (Becnel and Andreadis, 1999; Vavra and Larsson, 1999). Only the spores of microsporidia are walled and spores examined thus far contain large amounts of trehalose. Vegetative growth is by non-motile amoeba-like stages (often multinucleate) with simple plasma membranes. Although variable is some respects, all microsporidian spores are definitively and uniquely characterized by containing a coiled polar filament. At germination, the polar filament is inverted to become a tube for transport of the sporoplasm into the host cell. The fungi constitute an extremely large and diverse group of heterotrophic organisms devoid of chlorophyll, have a cell wall, are non-motile (some species have motile reproductive cells) and reproduce by means of a tremendous variety of spore types (Alexopoulos et al., 1996). Fungi are usually filamentous and multicellular and glycogen is the primary carbohydrate storage product (trehalose in yeast and lichens). Obligate parasitic fungi infect plants, animals and in some cases even other fungi. Cytological Structures: Mitochondria, perixosomes, and lysosomes have not been identified in microsporidia but are known to occur in the fungi. Both groups contain paramural bodies. The Golgi apparatus of microsporidia are said to be of a special type mainly consisting of a vesicular meshwork without stacked cisternae. While some fungi possess typical stacked cisternae, most groups have Golgi which consists of a single cisternal element (Alexopoulos et al., 1996). Centrioles are absent in all microsporidia and most fungi. In microsporidia, spindle fiber attachment is to a spindle plaque located on the nuclear envelope with small associated polar bodies often connected to the spindle plaque by filaments. In the fungi, centrioles are present only in the Chytridomycota and are composed of nine triplets. In most true fungi, centrioles are replaced by spindle pole bodies (SPB) and multivesicular bodies. Ribosomes of the fungi are of the typical eukaryotic size of 80S while the ribosomes in the microsporidia are prokaryote-size (70S) consisting of a large (23S) and small (16S) subunits. They lack the 5.8S subunit but a homologuous region is found at beginning of the 23S subunit(Vossbrinck and Woese 1986). Invasion: Spores in both microsporidia and fungi initiate infection in a host. Some microsporidia are characterized by only one type of spore while others form up to four types of spores during the course of the life cycle. Fungal species can also form up to four different spore types generally characterized into sexual (oospores, zygospores, ascospores, basidiospores) and asexual (conidia or sporangiospores) forms. The mechanisms for invasion are distinctly different for microsporidia and fungi. Fungal spores attach to the host surface and produce a penetration germ tube that gains access through enzymatic and mechanical activity. All microsporidian spores contain a polar filament that, on appropriate environmental stimulation, rapidly discharges the filament, which everts to become a hollow tube. The tremendous pressure within the spore at discharge (up to about 60 atm) propels the sporoplasm through the tube (which can reach lengths of up to 500µm in length!) into a host cell thus avoiding host defense systems. Replication: Many microsporidia and most fungi have uninucleate cells and both have cells with 2 nuclei. In the microsporidia this arrangement is called a diplokaryon and is a stable arrangement of paired, haploid nuclei. In fungi, this arrangement is called a dikaryon and represents 2 unpaired haploid nuclei. Mitosis in both microsporidia and fungi is intranuclear, meaning that the nuclear envelopes do not break down during division as occurs in most eukaryotic cells. Both groups contain species with documented meiosis with comparable types of synaptonemal complexes formed in the prophase meiotic nucleus. Vegetative multiplication in microsporidia is by binary and/or multiple fission of wall-less plasmodia. In fungi, walled hyphae develop by apical growth, in yeast by budding or binary fission. Sporulation in microsporidia varies from bisporous sporogony that produces 2 spores from each sporont to polysporous sporogony producing many spores. This process can involve meiosis or nuclear dissociation of diplokarya. Sporulation in fungi is highly variable (see Alexopoulos et al., 1996). Reproduction: Both fungi and microsporidia reproduce both sexually and asexually, although not necessarily at the same time. Asexual species of microsporidia are of two basic forms: one is uninucleate (haploid) throughout development and produces uninucleate spores while the other is diplokaryotic (diploid) throughout development and produces diplokaryotic spores. Asexual fungi are uninucleate (haploid) throughout development producing uninucleate spores. Sexual forms of microsporidia typically have an alternation of uninucleate development producing haploid spores (some sequences involve meiosis) and diplokaryotic development producing diplokaryotic spores. Some involve an obligate intermediate host. Sexual forms of fungi have an alternation of haploid and diploid cell states, which usually involves meiosis and produces only uninucleate spores. Some involve an intermediate host. Biochemical: Trehalose is a major reserve carbohydrate in all species of microsporidia tested while glycogen is the major reserve carbohydrate in fungi. Trehalose is a reserve disaccharide of some fungi especially yeast and lichens. The cell and spore walls of fungi contain chitin while chitin is known to occur only in the endospore of microsporidian spores. Others Features: All known microsporidia are obligate, intracellular parasites while parasitic fungi can be either facultative or obligate. Microsporida infect only animals, from protests to man, while parasitic fungi infect plants, animals and other fungi. Viruses and other fungi attack fungi but there is no conclusive documentation for any pathogens of microsporidia.

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