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In Vivo and in Vitro Development of the Protist Helicosporidium Sp

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In Vivo and in Vitro Development of the Protist Helicosporidium Sp J. Eukaryot. Microbiol., 48(4), 2001 pp. 460±470 q 2001 by the Society of Protozoologists In Vivo and In Vitro Development of the Protist Helicosporidium sp. DRION G. BOUCIAS,a JAMES J. BECNEL,b SUSAN E. WHITEb and MICHEAL BOTT aDepartment of Entomology and Nematology, University of Florida, Gainesville, Florida, 32611 USA, and bCenter for Medical, Agricultural and Veterinary Entomology, USDA, ARS, Gainesville, Florida 32604, USA ABSTRACT. We describe the discovery and developmental features of a Helicosporidium sp. isolated from the black ¯y Simulium jonesi. Morphologically, the helicosporidia are characterized by a distinct cyst stage that encloses three ovoid cells and a single elongate ®lamentous cell. Bioassays have demonstrated that the cysts of this isolate infect various insect species, including the lepidopterans, Helicoverpa zea, Galleria mellonella, and Manduca sexta, and the dipterans, Musca domestica, Aedes taeniorhynchus, Anopheles albimanus, and An. quadrimaculatus. The cysts attach to the insect peritrophic matrix prior to dehiscence, which releases the ®lamentous cell and the three ovoid cells. The ovoid cells are short-lived in the insect gut with infection mediated by the penetration of the ®lamentous cell into the host. Furthermore, these ®lamentous cells are covered with projections that anchor them to the midgut lining. Unlike most entomopathogenic protozoa, this Helicosporidium sp. can be propagated in simple nutritional media under de®ned in vitro conditions, providing a system to conduct detailed analysis of the developmental biology of this poorly known taxon. The morphology and development of the in vitro produced cells are similar to that reported for the achorophyllic algae belonging to the genus Prototheca. Key Words. Black ¯y, entomopathogens, Helicosporidia, Helicosporidium, insect pathogen, pathogenic protist, Simuliidae, Simulium jonesi. ELICOSPORIDIUM parasiticum, a pathogenic protist de- per os. The ability to produce quantities of this pathogen in a H tected initially in a ceratopogonid (Diptera), was de- lab insect provided an opportunity to conduct a series of labo- scribed and named by Keilin (1921) and was subsequently ratory experiments. We present data on the discovery, host placed in a separate order, Helicosporidia, within the Cnidios- range, and in vivo development of this Helicosporidium sp. and pora (Kudo 1966). Weiser (1970) examined both the type ma- provide new evidence on the invasion process. We also dem- terial and a new isolate from a hepialid larva, and proposed that onstrate that this pathogen has very simple nutritional require- this organism be transferred to the Ascomycetes. Later work by ments and can be cultivated in vitro on a wide range of media Kellen and Lindegren (1974) described the life cycle of a Hel- and maintain infectivity for insect hosts. icosporidium sp. [isolated originally from Carpophilus mutila- tus (Nitidulidae, Coleoptera) Kellen and Lindegren 1973] in a MATERIALS AND METHODS lepidopteran host, the navel orangeworm Paramyelois transi- Insect methods. The test insects, including various dipteran tella, and agreed that this organism belonged with the primitive and lepidopteran hosts, were accessed from established lab col- ascomycete group. Kellen and Lindegren (1974), conducting onies and were maintained according to standard protocols as lab transmission studies, reported that cysts ingested by host previously described (Avery and Undeen 1987a, 1987b). navel orangeworm released the cyst contents into the gut lumen; Field isolation. Black ¯y larvae were collected from Hatchet both sporoplasms (ovoid cells) and ®laments were found in the Creek, Alachua County, Florida (N 298 439 50.499,W828 149 lumen at 3 h post-infection. Elongate cells 11.5 3 3.5 mm, 56.699) in the fall of 1998. Larvae from the sample were ex- believed to develop from the released sporoplasms, were de- amined for signs of infection and for species identi®cation. The tected in the hemocoel at 24 h post-challenge. These cells di- total number of larvae and the prevalence of infection was es- vided to form 4 daughter cells within a pellicle. By 72 h, spher- timated from the samples. ical cells 3.5 mm in diam. were observed in the hemolymph. In vivo propagation of the Helicosporidium sp. Cysts of Between d 3±6 these cells divided and developed into additional the Helicosporidium sp., extracted from infected black ¯ies Si- spherical cells. After this, the daughter cells underwent sporog- mulium jonesi, were fed per os to second and third instar corn ony, secreted a thick spore wall (or pellicle) and differentiated earworm Helicoverpa zea larva. Eight test larvae, initially into the cassette of a ®lament and three sporoplasms. Lindegren starved for 24 h prior, were each allowed to imbibe a 10 ml and Hoffman (1976) proposed that the developmental stages of droplet containing 4 3 105 cysts. Treated larvae were placed in this organism placed it closer to the Protozoa than to the Fungi. individual cups containing arti®cial diet and incubated at 26 8C Because of this uncertain taxonomic status, the helicosporidia under a 16-h light:8-h dark period. At 10±14 d post-challenge, have not appeared in classi®cation systems of either the Pro- cream-colored hemolymph was harvested from infected larvae tozoa or the Fungi and have been unclassi®ed since 1931 (Cav- and subjected to several cycles of low-speed centrifugation (600 alier-Smith 1998; Patterson 1999). Fukuda et al. (1976) isolated g, 1±2 min). Cysts, located in the pellets, were suspended in 50 a Helicosporidium sp. from the mosquito Culex territans and determined that larvae were infected per os and that the disease mM Tris-HCl buffer pH 8.0 and puri®ed on a linear gradient may persist though adult eclosion. Additional helicosporidia of Ludox (DuPont Chemical, Boston, MA) following Undeen have been detected in mites, cladocerans, trematodes, collem- and Vavra (1998). The band containing the cysts was collected, bolans, and pond water samples (Avery and Undeen 1987a; diluted in 10 vols. of water, and subjected to several cycles of Pekkarinen 1993; Purrini 1984; Sayre and Clark 1978). low-speed centrifugation to remove residual gradient material. Recently, a Helicosporidium sp. was isolated from larvae of Cysts were counted using a hemacytometer and measured with the black ¯y Simulium jonesi Stone and Snoddy, collected in a split image micrometer. They were placed either at 4 8Cor Florida. This identi®cation was based on the presence of a cyst 270 8C for short and long-term storage, respectively. stage composed of three ovoid cells and an elongate ®lamentous Insect bioassays. The viability of the puri®ed cysts was as- cell. Preliminary assays demonstrated that this Helicosporidium sessed by per os challenge of early instar H. zea and tobacco sp. was capable of infecting Helicoverpa zea larvae challenged hornworm Manduca sexta larvae and by hemocoelic injection into late instar waxmoth Galleria mellonella larvae with 105 cysts/insect. Test insects were provided with their respective Corresponding Author: D. Boucias. Telephone number: 352-392- diet and incubated at 26 8C. 1901 ext.147; FAX number 352-392-0190; E-mail: [email protected]¯. Bioassays were conducted with several species of Diptera to edu determine their susceptibility to per os challenge with puri®ed 460 BOUCIAS ET AL.ÐDEVELOPMENT OF HELICOSPORIDIUM 461 cysts of the Helicosporidium sp. Mosquito assays were con- were resuspended and aliquots quantitated with a hemacytom- ducted with groups of 100 one- to two-day-old (1st instar) col- eter. ony larvae exposed at 27 8C in 3.5 oz plastic cups in 100 ml A ®nal series of assays addressed the ability of Helicospor- of water with 2% alfalfa and potbelly pig chow mixture (2:1) idium sp. to develop in conventional lab media including Cza- for 24 h. Mosquitoes and exposure media were then transferred pek Dox broth (CD), CD 1 2% yeast extract (CDY), Candida to enamel pans with 500 ml of water and fed according to liquid broth, Vogel-Bonner minimal broth, TC100, TC100 1 standard protocols. Mosquitoes (Aedes taeniorhynchus, Anoph- 10% FCS, and Sabouraud dextrose (SD) broth. These media eles albimanus, An. quadrimaculatus, and Culex quinquefascia- were tested for their ability to support the development of Hel- tus) were exposed to the Helicosporidium sp. at doses ranging icosporidium sp. The cells produced in TC100 1 FCS were from 3.5 3 102 to 5.0 3 105 cysts/ml. Because An. quadrima- inoculated into broth cultures (5 3 103 cells/ml21) and incubated culatus was highly susceptible, a 30% serial dilution of 5.0 3 without and with shaking (New Bruswick gyro-rotory shaker, 104 cysts/ml (6 doses, three replicates) was conducted to deter- 250 rpm) at both 25 8C and 35 8C. At intervals, aliquots were mine the 50% infective concentration (IC50). Mosquitoes were removed and cell replication assessed by hemacytometer examined for infection as larvae 5 to 6 d post-exposure and as counts. adults 1 to 2 d after emergence. In addition, 100 three-day-old Transmission electron microscopy. Gradient-puri®ed cysts (3rd instar) Musca domestica larvae were continuously exposed produced in H. zea were prepared for ultrastructural examina- to 7.8 3 108 cysts (total) mixed with their diet. Fly larvae were tion by primary ®xation in 2.5% glutaraldehyde plus 1% acro- examined for infection 6 to 7 d post-exposure for the presence lein at 60 8C for 2 h, post-®xing in 2% osmium tetroxide at RT, of cysts and as adults 1 to 2 d after emergence. dehydrating in an ethanol series, and embedding in Spurr's res- In vitro dehiscence of Helicosporidia cysts. The Helicos- in. Thin sections, stained in uranyl acetate and lead citrate, were poridium sp. used in these experiments was harvested from in- observed and photographed at 75 kV. fected H. zea larvae. Initial experiments addressed the ability Scanning electron microscopy (SEM).
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