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Chapter 14 : Microsporidia in Insects

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Abstract:

This chapter highlights the biological and life cycle features of entomogenous microsporidia and provides some basic information on their taxonomic distribution. The development of all insect-parasitic microsporidia is restricted to the cytoplasm of the host cell. The development of all insect-parasitic microsporidia is restricted to the cytoplasm of the host cell. Specialized relationships between microsporidia and the host at the cellular level have been termed xenomas. Weiser distinguished two main types of xenomas in insects, syncytial and neoplastic. The chapter presents the major and minor pathways of transmission for insect microsporidia. Alternatively, the criteria used to establish the genera of microsporidia from aquatic insects may not truly reflect phylogenetic diversity but adaptations to specific habitats and host systems. A section lists a few genera for which insects are not the type hosts. This is because many species have been reported to occur in insects (such as , ) or because there are possible links to insect microsporidia (such as ). Finally, the chapter provides diagnostic information which is primarily restricted to the features of sporulation and the spore, with the addition of distinguishing life cycle characteristics when available. The type host and species are given followed by comments on distribution and other matters deemed of importance.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14

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Image of FIGURES 1–5
FIGURES 1–5

Gross pathology of insects with microsporidian infections. Culex salinarius larva exhibiting fat body infection with . Magnification, ×4.6. larva exhibiting fat body infection with . Magnification, ×6.6. Gastric ceca of a larva infected with . White cysts are cells filled with spores. Magnification, ×13.2. Dissected exhibiting healthy, yellowish-appearing fat body. Magnification, ×1.3. Dissected infected with , demonstrating infected fat body tissue appearing as white cysts. Magnification, ×1.2. Reprinted from with permission from the authors and publisher ( Fig. 4 and 5 ).

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 6–8
FIGURES 6–8

Gross pathology of healthy and microsporidia-infected Reprinted with permission from J. V. Maddox. Healthy dissected fat body tissue. Magnification, ×2. Dissected fat body tissue infected with Magnification, ×2. larvae; (left) healthy; (right) infected with (note pufly, dark appearance of posterior abdomen). Magnification, ×1.6.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 9 AND 10
FIGURES 9 AND 10

Navel orangeworm () larvae infected with . Reprinted with permission from W. Kellen, Horticultural Crops Research Laboratory, USDA, ARS, Fresno, Calif. Large, healthy control larvae on left, and stunted, infected larvae on right. Four weeks after infection. Pupae infected with . Large, healthy control pupae at left, and stunted, deformed, infected pupae on right.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 11 AND 12
FIGURES 11 AND 12

Gastric ceca of , demonstrating immune reaction to infection. Reprinted with permission from M.A. Johnson. Whole gastric cecum, exhibiting melanization of primary binucleate spores (arrows). Magnification, ×40. High magnification of infected area showing melanized spores. Magnification, ×250. S, spores.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 13–16
FIGURES 13–16

Electron micrographs of demonstrating developmental cycle within midgut epithelium cells of Early plasmodium at onset of nuclear division and microvilli (arrow). Magnification, ×5,600. Multinucleate plasmodium. Magnification, ×6,400. Multinucleate sporogonial plasmodium in early stages of multiple division by vacuolation. Magnification, ×4,250. Mature spores within polysporophorous vesicle. Magnification, ×5,900. Reprinted from with permission from the authors and publisher. HCN, host cell nucleus; N, nucleus; PSV, polysporophorous vesicle; S, spores.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 17-20
FIGURES 17-20

Microsporidia-infected host cells. Oenocyte in adult infected with . Magnification, ×4,400. Xenoma of . Magnification, ×250. Higher magnification of xenoma demonstrating multiple host cell nuclei. Magnification, ×350. Higher magnification of xenoma wall of . Magnification, ×6,500. Reprinted from ( Fig. 17 ) and ( Fig. 18 to 20 ) with permission of the authors and publishers. BM, basement membrane; CF, collagen fibrils; EmSP, empty spore; HCN , host cell nucleus; L, lipid; SV, sporophorous vesicle;W, wall.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURE 21
FIGURE 21

Diagram of the major and minor pathways of transmission for insect parasitic microsporidia.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURE 22
FIGURE 22

Diagram of The life cycle of in a larval midgut epithelial cell of Developmental stages of as seen in Giemsa-stained smears. Reprinted from with permission from the authors and publisher. Haplokaryotic schizonts. Schizonts undergoing binary fission. Ribbonlike schizonts, some dividing by budding or multiple fission. Sporogonial plasmodia exhibiting evidence of division by plasmotomy. Late-stage sporogonial plasmodium undergoing multiple fission to form sporoblasts. Group of spores. All magnifications, ×1,400.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 33–36
FIGURES 33–36

Electron micrographs of in midgut epithelial cells of Schizont in parasitophorous vacuole (PV) derived from cisternae of host cell rough endoplasmic reticulum. Magnification, ×34,600. Higher magnification of a schizont plasmalemma-parasitophorous vacuole interface. Double arrows indicate inner membrane without ribosomes closely associated with the plasmalemma, and single arrows indicate parasitophorous vacuole studded with ribosomes. Magnification, ×89,000. Uninucleate spore. Magnification, ×42,300. Infected midgut epithelial cell of Magnification, ×2,500. Reprinted from with permission from the authors and publisher ( Fig. 33-35 ). MV, microvilli; PV, parasitophorous vacuole; PM, peritrophic membrane; P, plasmalemma.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURE 37
FIGURE 37

Diagram of the life cycle of in midgut epithelial cells.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 38–39
FIGURES 38–39

Electron micrographs of spores formed in Reprinted with permission from I. Fries. Germinated primary binucleate spore of characterized by a thin spore wall and a large vacuole. Magnification, ×17,700. Binucleate spore (environmental spore) of characterized by a thick spore wall and a long polar filament. Magnification, ×17,000.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURE 40
FIGURE 40

Diagram of the life cycle of in a midgut epithelial cell and fat body.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 41 AND 42
FIGURES 41 AND 42

Electron micrographs of spores. Reprinted from with permission from the authors and publisher. Binucleate spore (environmental spore) of characterized by a thick spore wall and a long polar filament. Magnification, ×8,700. Meiospore of . Magnification, ×19,600. .

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURE 43
FIGURE 43

Diagram of the life cycle of in and .

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 44-46
FIGURES 44-46

Longitudinal section of spores of Binucleate spore from a female mosquito, Magnification, ×7,500. Meiospore from a fourth instar larva of Magnification, ×11,200. Haploid spore from a copepod, Magnification, ×10,600. AD, anchoring disk; EN, endospore; EX, exospore; P, polaroplast; PF, polar filament; PV, posterior vacuole; N, nucleus.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 47-64
FIGURES 47-64

Life cycle stages of as seen in Giemsa-stained smears. Stages in larval ( Fig. 47-50 ) and adult ( Fig. 51 and 52 ) following oral ingestion of copepod spore. Uninucleate schizont. Dividing schizont. Gamete. Gametes undergoing plasmogamy. Sporoblast. Binucleate spores. Stages in larval following transovarial transmission. Diplokaryotic sporont. Sporont undergoing meiosis. Binucleate sporont. Quadrinucleate sporont. Eight sporoblasts within sporophorous vesicle. Live meiospores (phase-contrast). Stages in following ingestion of meiospores. Early sporont. Binucleate sporont. Sporogonial plasmodia. Sporoblasts. Live spores (phase-contrast).All magnifications, ×950.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 65–70
FIGURES 65–70

Developmental stages of from larval fat body tissue of Diplokaryotic meront. Magnification, ×5,000. Binucleate sporont. Magnification, ×5,200. Binucleate sporont during prophase of meiosis. Magnification, ×6,000. Sporont at metaphase I. Magnification, ×5,400. Multinucleated sporont within sporophorous vesicle. Magnification, ×3,700. Sporoblast. Magnification, ×9,600. AD, anchoring disk; C, chromosomes; MG, metabolic granules; N, nucleus; P, polaroplast; PF, polar filament; PV, posterior vacuole; SC, synaptonemal complex; SP, spindle plaque; SV, sporophorous vesicle; RER , rough endoplasmic reticulum; SW, spore wall.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 71–74
FIGURES 71–74

Histological sections of infections in copepod and mosquito hosts. Sagittal section of a female copepod, showing infection within the median ovary (Ov) and paired lateral oviducts (Od). Magnification, ×150. Infected epithelial cell (arrow) of the gastric cecum from a fourth instar larva. Magnification, ×250. Infected oenocyte cell (arrow) from a fourth instar larva. Magnification, ×340. Infected oenocyte containing binucleate spores (arrow) from the ovaries of an adult female O, host oocyte. Magnification, ×920

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURE 75
FIGURE 75

Diagram of the life cycle of in .

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 76–93
FIGURES 76–93

Life cycle stages of as seen in Giemsa-stained smears. Reproduced from with permission from the publisher. Sporulation sequence of in after horizontal transmission producing the primary binucleate spore. Uninucleate sporoplasm in gastric cecum. Schizont dividing. Gametes. Paired gametes undergoing plasmogamy. Primary binucleate spore. Sporulation sequence of in after horizontal transmission producing binucleate (transovarial) spores. Diplokaryotic sporont undergoing binary fission. Binucleate sporoblast. Binucleate (transovarial) spore (phase-contrast). Sporulation sequence of producing the uninucleate pyriform spore from nuclear dissociation in the filial generation. Diplokaryotic meront. Sporont undergoing cytokinesis after nuclear dissociation. Sporogonial plasmodium. Sporogonial plasmodium dividing into uninucleate sporoblasts. Uninucleate thin-walled pyriform spores from filial host larva (phase-contrast). Sporulation sequence of that involves meiosis to produce the meiospores in the filial generation. Diplokaryotic meront. Zygote or early sporont derived from a diplokaryotic meront. Sporont. Tetranucleate sporogonial plasmodium. Meiospores (arrows, phase-contrast). All magnifications, ×l,700.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 94–97
FIGURES 94–97

Electron micrographs of in after horizontal transmission. Reprinted from with permission from the publisher. Gamete with papilla (arrow). Magnification, ×11,200. A pair of gametes at the beginning of plasmogamy. Magnification, ×6,400. Diplokaryotic meront. The arrow indicates a papilla at the apex of the cell. Magnification, ×7,600. Diplokaryotic sporoblast. Magnification, ×9,900.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 98–103
FIGURES 98–103

Electron micrographs of in after transovarial transmission. Reprinted from with permission from the publisher. FIGURE 98Diplokaryotic meront. Magnification, ×8,300. Dissociation of diplokaryon. Magnification, ×7,650. Dividing schizont. Magnification, ×5,300. Sporogonial plasmodium in process of sporogony. Magnification, ×3,700. Early sporoblasts. Magnification, ×5,800. Sporoblast isolated in a sporophorous vesicle. Magnification, ×7,650.

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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Image of FIGURES 104–107
FIGURES 104–107

Electron micrographs of the four different spore types of in Primary binucleate spore. N, nucleus; PV, posterior vacuole;T, tubules. Magnification, ×16,000. Binucleate (transovarial) spore. AD, anchoring disk; PF, polar filament; P, polaroplast. Magnification, ×l5,400. Haploid, uninucleate (environmental) spore. Magnification, ×7,700. Meiospore. Magnification, ×12,700. Reprinted from with permission from the authors and publisher ( Fig. 104 ) and from with permission from the publisher ( Fig. 105-107 ).

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14
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References

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Tables

Generic image for table
TABLE 1

Distribution by insect order of microsporidia with insects as type hosts

Citation: Becnel J, Andreadis T. 1999. Microsporidia in Insects, p 447-501. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch14

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