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Chapter 3 : Developmental Morphology and Life Cycles of the Microsporidia

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Developmental Morphology and Life Cycles of the Microsporidia, Page 1 of 2

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Abstract:

This chapter reviews the morphological features and development of the microsporidia. The general life cycle pattern of the microsporidia can be divided into three phases: the infective or environmental phase, the proliferative phase, and the sporogony or spore forming phase. The chapter discusses the host-parasite interface during parasite development. Microsporidia with host-produced interfacial envelopes are those that are separated from the hyaloplasm by host-produced membranes during proliferation through spore formation. Microsporidia having indirect contact between host- and parasite-produced interfacial envelopes are separated from the hyaloplasm by membranes and/or secretions produced by both the host and the parasite. The proliferative phase has been referred to as schizogonic and merogonic by some authors, however, different authors have assigned different types of nuclear activity to the terms merogony and schizogony with respect to the microsporidia. Recognizing the diversity of polaroplast morphology and organization in various species of microsporidia, Larsson described five types of polaroplast structural arrangements. In addition to environmental spores, some microsporidia produce autoinfective spores which become activated and germinate within the same host in which they were just produced. A few microsporidia of the genus have two host cycles with morphologically different spores in each and different development in the males and females of the same host species.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3

Key Concept Ranking

Endoplasmic Reticulum
0.6651186
Plasma Membrane
0.6082107
Golgi Apparatus
0.5898897
Nuclear Membrane
0.55834776
0.6651186
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Image of FIGURE 1
FIGURE 1

Diagram of a typical developmental cycle of the microsporidia. The three regions represent the three phases of the microsporidian life cycle. Phase I is the infective/environmental phase, the extracellular phase of the cycle. It contains the mature spores in the environment. Under appropriate conditions, the spore is activated (e.g., if the spore is ingested by an appropriate host, it is activated by the gut environment) and triggered to evert its polar filament (which becomes a hollow tubule). If the polar tubule pierces a susceptible host cell and injects the sporoplasm into it, phase II begins. Phase II is the proliferative phase, the first phase of intracellular development. During the proliferative part of the microsporidian life cycle, organisms are usually in direct contact with the host cell cytoplasm and increase in number. The transition to phase III, the sporogonic phase, represents the organism s commitment to spore formation. In many life cycles this stage is indicated morphologically by parasite secretions through the plasmalemma producing the thickened membrane. The number of cell divisions that follow varies depending on the genus in question, and the result is spore production.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 2
FIGURE 2

Diagram of the internal structure of a microsporidian spore. The spore coat has an outer electron-dense region called the exospore (Ex) and an inner thicker electron-lucent region, the endospore (En). A unit membrane (P) separates the spore coat from the spore contents. The extrusion apparatus, anchoring disk (A), polar tubule (Pt), lamellar polaroplast (Lp), and tubular polaroplast (Tp), dominates the spore contents and is diagnostic for microsporidian identification. The posterior vacuole (Pv) is a membrane-bound vesicle which sometimes contains a “membrane whirl,” a “glomerularlike” structure, flocculent material, or some combination of these structures. The spore cytoplasm is dense and contains ribosomes (R) in a tightly coiled helical array. The nucleation may consist of a single nucleus or a pair of abutted nuclei, a diplokaryon (D). The size of the spore depends on the particular species and can vary from less than 1 to more than 10 μm. The number of polar tubule coils also varies from a few to 30 or more, again depending on the species observed. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 3
FIGURE 3

Electron micrograph of spore from the angler fish, , depicting the structure of a typical uninucleate spore. The anterior end is filled with the anchoring disk (A), polar tube (Pt), and the various lamellar (Lp) and tubular (Tp) polaroplast membranes of the extrusion apparatus. Ribosomes (R), polar tube cross sections (Pt), and a single nucleus (N) occupy the mid-portion of the spore. The posterior end (asterisk) contains a vacuole that is not evident in this oblique section. (Inset) The posterior vacuole (Pv), often contains a dense body composed of tubular material which may appear “glomerular” (asterisk). The posterior vacuole is often abutted to the coils of the polar tube (Pt). (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 4
FIGURE 4

spores in an intestinal epithelial cell from the honeybee. The spores appear highly refractile when observed in a fresh squash preparation by phase contrast microscopy. Spores are 4 by 2 μm. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 5
FIGURE 5

(Sprague, 1974) , formerly . Spores in the muscularis of the jejunum are shown. The spore coats are well illustrated by Grocott-methenamine-silver stain AFIP# 71-5887. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 6
FIGURE 6

spores in the muscularis. The anterior end of the spores contains a PAS-positive granule (arrows). AFIP # 71-5883. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 7
FIGURE 7

() in biopsy tissue from human intestine. A light micrograph of densely staining spores concentrated in the cytoplasm of enterocytes at the tip of a distorted villus is shown (semithin plastic section, toluidine blue stain). (Reprinted with perrnission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 8
FIGURE 8

Diagram of the life cycles of several horizontally transmitted genera of microsporidia, illustrating developmental diversity. In the infective phase, the proper environmental conditions are required to activate mature spores, resulting in polar tubule extrusion. The polar tubule of each spore is shown piercing the host cell plasmalemma, represented by the solid black line. Below it is the intracellular cytoplasmic area. The sporoplasms travel through the everted polar tubules and are deposited inside the host cells, initiating the proliferative phase of development. The sporoplasm on the left is uninucleate, and the cells produced from it represent the developmental patterns of several microsporidia with isolated nuclei. The sporoplasm on the right is diplokaryotic, and it similarly produces the various diplokaryotic developmental patterns. Cells containing either type of nucleation produce one of three basic developmental forms. Some cycles have cells that divide by binary fission immediately after karyokinesis (e.g., ).A second type forms elongated moniliform multinucleate cells that divide by multiple fission (e.g., some spp.).The third type forms rounded plasmodial multinucleate cells that divide by plasmotomy (e.g., ). Cells may repeat their division cycles one to several times in the proliferative phase. The intracellular stages in this phase are in direct contact with the host cell cytoplasm or closely abutted to the host ER. There are two types of exceptions: (1) the proliferative cells of and are surrounded by a host formed parasitophorous vacuole throughout their development (possibly Tetramicra); and (2) the proliferative plasmodium of the genus is surrounded by a thick layer o f parasite secretions in the proliferative phase that separates and becomes the sporophorous vesicle in the sporogonic phase. Below the dashed line are the stages o f the sporogonic phase. A few cycles maintain direct contact with the host cell cytoplasm in the sporogonic phase: , , , , and . The remaining genera form a sporophorous vesicle as illustrated by the circles around developing sporogonial stages. Note that in the cycle and the part of the cycle, the diplokarya separate and continue their development as cells with isolated nuclei.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 9
FIGURE 9

. Mature spores were incubated in a germination medium and fixed for EM. (A) Activated spore just about to evert its polar filament; (B) activated spore with polar tube in the process of everting as it passes through the apical portion of the spore coat; (C) empty spore shell with the polar tube still attached.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 10
FIGURE 10

. A parasitophorous vacuole containing proliferative cells with large, round isolated nuclei (Nu) is shown.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 11
FIGURE 11

. A proliferative cell containing nuclei (Nu) in diplokaryotic arrangement is shown. The parasite cells are in direct contact with the host cell cytoplasm.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 12
FIGURE 12

Early proliferative cell of with diplokaryotic nuclear pair (Nu) undergoing karyokinesis. Nuclear membrane invaginations containing spindle plaques on each nuclear envelope (arrows) of the diplokaryotic pair and chromosomes (asterisk) within each respective nucleoplasm are present. Note the presence of vesiculotubular material (T) in the host cytoplasm and thickened plasmalemma. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 13
FIGURE 13

Proliferative cell o f containing two diplokaryotic nuclear pairs, both with nuclei in late anaphase. Note chromosomes (asterisk) in close association with spindle plaque (arrows). Plasmalemmal invagination (broad arrowheads) indicates that cytokinesis has begun before the nuclei enter interphase, thus linking the two processes. The parasite cells are in direct contact with the muscle cell cytoplasm with no intervening parasitophorous vacuole as evidenced by the proximity of the myofilaments (F). (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 14
FIGURE 14

. Nuclear “isthmus” (arrow) between separating diplokaryotic nuclei of a sporont and invagination of cytoplasm. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 15
FIGURE 15

Proliferative plasmodial stage of . The cytoplasm is relatively simple, containing only ribosomes and small amounts of membrane. Adjacent to electron-lucent inclusions (asterisk) are multiple elongated nuclei (N), none of which are abutting in diplokaryon form. Note the close approximation of the host nucleus and mitochondria to the parasite plasmalemma. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 16
FIGURE 16

Electron micrograph of a sp. developing in the skeletal muscle (M) of a patient with AIDS. The proliferative stages (PR) and sporoblasts (SB) are enclosed in thick walled sporophorous vacuoles (PV).The proliferative forms are multinucleated, with only isolated nuclei (N). An early sporont has a plasmalemma pulling away from the sporophorous vacuole (PV), and the plasmalemma has started to thicken (TKM). (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 17
FIGURE 17

Elongated tetranucleate cell of tightly abutted by host ER in the xenoma periphery. Nu, nucleus.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 18
FIGURE 18

Diagram of the life cycle of . A triggered spore injects its diplokaryotic sporoplasm into the host cell cytoplasm beginning the proliferative phase. The organisms multiply by binary fission or multiple fission of ribbonlike moniliform multinucleate cells. The transition to the sporogonic phase is morphologically indicated by parasite secretions through the plasmalemma, producing the thickened membrane. In the genus , each sporont produces two sporoblasts, which results in the production of two spores. This entire cycle takes place in direct contact with the host cell cytoplasm (type I interfacial relationship). N, nucleus.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 19
FIGURE 19

Diagram of the life cycle of . (A) An empty spore with its polar tubule extruded is injected into the cytoplasm of a host intestinal enterocyte cell and has a sporoplasm (B) at the end. (B to J) Intracellular developmental stages. (C) An early proliferative cell containing a single dividing nucleus. (D) Abutted proliferative plasmodial cells with no intervening host cytoplasmic organelles suggest recent cytokinetic division. (E) A proliferative plasmodial cell containing multiple elongated nuclei (N) and electron-lucent inclusions (asterisk). (F) Early sporogonial plasmodium showing electron-dense disks forming at the surface of the electron-lucent inclusions. (G) A late sporogonial plasmodium filled with electron-dense disks, some in stacks and some fused in arcs in advanced stages o f polar tubule formation. Nuclei are now round and dense and usually associated with electron-dense disk complexes and electron-lucent inclusions. Polar tubule attachment complexes (umbrella-shaped dense structures) appear at this stage. (H) During sporogonial division the plasmalemma thickens and invaginates, segregating individual nuclei with polar tubule complexes. (I) Several newly formed sporoblast cells which are irregularly shaped and possess a thickened plasmalemma and five to six coils o f polar tube. (J) Mature spores characterized by the presence of a small electron-lucent inclusion in the sporoplasm, a single nucleus, a polar tubule forming about six coils in a double row, an anterior attachment complex extending down around the polaroplast, and a thick electron-lucent spore coat. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 20
FIGURE 20

Diagram of the life cycle of . A triggered spore injects its unikaryotic sporoplasm into the host cell cytoplasm, beginning the proliferative phase. This genus develops in a host-formed parasitophorous vacuole surrounding all the developing stages. The organisms multiply by binary fission or multiple fission of ribbonlike moniliform multinucleate cells. The transition to the sporogonic phase is morphologically indicated by parasite secretions through the plasmalemma, producing the thickened membrane of the sporont. In this genus the number of sporoblasts produced depends on the species in question. produces two sporoblasts, while may produce more. All sporoblasts undergo a metamorphosis into spores. This entire cycle takes place in a parasitophorous vacuole in the host cell cytoplasm (type II interfacial relationship). N, nucleus.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 21
FIGURE 21

. The double membrane of the host endoplasmic reticulum (HER) completely surrounds the multinucleated plasmodium (M) in the host cytoplasm (HC) with at least three nuclei (N). (Inset) The sporogonial plasmodium divides by plasmotomy, producing several uninucleate sporonts. A portion of the double-membraned parasitophorous vacuole contains single nucleated sporonts (SP). (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 22
FIGURE 22

. A thick amorphous coat surrounding a proliferative plasmodium is shown. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 23
FIGURE 23

Diagram of the -secreted SPOV. The proliferative phase includes formation of a plasmodium by multiple nuclear divisions of isolated nuclei (A). The proliferative plasmodium secretes a thick, electron-dense amorphous coat which is retained and becomes the SPOV when the parasite plasmalemma retracts away from it (B). The plasmalemma thickens as it retreats from the SPOV. The sporogonial plasmodium divides by plasmotomy, producing smaller multinucleate cells (C). This division process continues until all the cells are uninucleate. These cells are sporoblasts and all undergo a metamorphosis into spores. The entire cycle takes place in the SPOV in the host cell cytoplasm (type III interfacial relationship).

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 24
FIGURE 24

. Plasmodia forming electron-dense coats from the material in the episporontal space, which appears to be connected to the parasite (arrows). (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 25
FIGURE 25

Diagram of the proposed life cycle of , showing the two patterns of development, disporoblastic (-like) and octosporoblastic (-like). During the sporogonic phase of octosporoblastic development, the parasite appears to develop as two plasmodia in a single sporophorous vesicle. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 26
FIGURE 26

. Early proliferative parasites in the periphery of a xenoma surrounded by host endoplasmic reticulum (ER) and host mitochondria (M) are shown. Note the diffuse parasite cytoplasm devoid of any mitochondria.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 27
FIGURE 27

sporoblasts in a SPOV. Note the thickened plasmalemma, the increased cytoplasmic density of sporoblasts, and the presence of tubules (T) in the SPOV (arrows).

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 28
FIGURE 28

. An electron micrograph of an anastomosing complex of PQM with tubules adjoining the meront (M) is shown. The position of the meront plasma membrane is indicated by three arrows. Abundant ER vesicles are aligned with the PQM surface. Single arrows indicate the membrane-surrounded tubules and the points at which the tubule-enveloped membrane is confluent with ER membrane around PQM. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 29
FIGURE 29

Commencement of sporogony and formation of sporonts in . The first sign of sporogony is the deposition of secretory material on the plasmalemmal surface (SC) of single nucleated cells now called sporonts. As deposition of this material continues (SC), the sporont cell surface takes o n a scalloped appearance and pulls away from the fibrillar lamina (arrows). It is at this stage that the presence of a parasitophorous vacuole membrane becomes evident (PV). (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 30
FIGURE 30

Diagram of the life cycle of . () . (A) An empty spore with its polar tubule extruded is injected into the cytoplasm of a host intestinal enterocyte cell. It has a sporoplasm (B) at the end. (B to G) Intracelluar developmental stages. (C) Proliferation cells may be uninucleated, binucleated, or tetranuleated. Multinucleate cells are elongated and divide by simple fission. The plasmalemma of these cells is a unit membrane which secretes droplets that become a fibrillar matrix in which the parasites are embedded. (D) Sporont cells with thick plasmalemmal membranes may be uninucleated, binucleated, or tetranucleated and continue to secrete the fibrillar matrix. The sporont cell surface appears to pull away from the fibrillar matrix, making the cells appear to be in individual chambers. A parasitophorous vacuole membrane becomes evident, and long tubular appendages form at the surface of the sporonts and are scattered between the parasite cells. (E) After the last cell division, sporoblast metamorphosis begins. These single nucleated, oval cells contain a vesicular Golgi-like mass associated with polar tubule formation. (F) Spores measure 2 by 1 μm and are characterized by a thick electron-lucent spore coat, a single nucleus, a polar tubule that forms about five coils in a single row and its anterior attachment complex, and a posterior vacuole. (G) A parasite cluster, illustrating the asynchronous nature of development, the separation of individual cells by the fibrillar matrix, and the presence of type I tubular appendages. Other cells in the lamina propria that may become infected are fibroblastic (Fb), endothelial (End), and macrophage (Mp) cells. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 31
FIGURE 31

Example of a type I tubule (T) in . The tubule is continuous with the sporoblast (S) plasmalemma (PM), and its distal end constricts (arrow) before terminating in a bulbous structure. Note the granular and filamentous material covering the bulb. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 32
FIGURE 32

. A cluster of type II tubules (T) projects from a sporoblast. At this magnification, the constrictions along the length of the tubules are apparent. PS indicates a SPOV. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 33
FIGURE 33

sporoblasts (SB), identified by the presence of a developing polar filament (PF), have type III tubules (T) projecting from their plasmalemma (arrows). The tubules contain regularly spaced electron-dense particles inside the tubule lumen. Note the tubule abutting the host mitochondrion (M). (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 34
FIGURE 34

. Shown is an electron micrograph of the -like pattern of development during sporogony in an SPOV which contains multinucleate plasmodium surrounded by type IV tubules in the episporontal space. Nu, nucleus. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 35
FIGURE 35

. Electron micrograph of a spore surface with projections. (Reprinted with permission of E. Weidner.)

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 36
FIGURE 36

Electron micrograph of proliferative stage undergoing division (asterisk). The nuclei (N) are in the diplokaryon arrangement (paired and abutted) typical of this genus. Note the direct contact between the parasite and the host cytoplasm. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 37
FIGURE 37

. The periphery of the xenoma (X) containing proliferating parasites (P) distributed among host nuclei (HN) is shown. Collagen (C) and fibroblasts (F) encapsulate the xenoma.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 38
FIGURE 38

sporogony. Deposition of material results in a uniformly thick plasmalemma surrounding the sporont cells. These sporonts continue to secrete the fibrillar lamina. The sporont (ST) is a tetranucleate (n) elongated cell in the process of cytokinesis (arrowhead). This cluster of parasite cells also contains many mature electron-dense spores, proliferative cells (P), and a dense fibrillar lamina separating the individual parasite cells. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 39
FIGURE 39

plasmodium with multiple developing polar filaments and many nuclei. A sporogonial plasmodium containing at least 12 nuclei (N) in a single plane of the section is shown. The round, dense nuclei are each associated with electron-dense disk complexes and electron-lucent inclusions (asterisk). Electron-dense disks fuse into arcs, forming polar filament coils. Despite the advanced maturation and organelle separation associated with each nucleus, there is not yet any evidence of cytokinesis or plasmalemmal thickening. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 40
FIGURE 40

cell after the diplokaryon has completed its division in a cell possessing a thickened membrane. Cytokinesis has commenced, but a connection between the two diplokaryotic parts of the cell is still present. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 41
FIGURE 41

Electron micrograph of sporont undergoing cytokinesis. Note the thickened membrane (arrowhead) and single nucleus. It is the occurrence of cell division at this stage of development that makes this parasite disporous. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 42
FIGURE 42

sporoblast. The cell-limiting membrane is thick, a diplokaryon is present, and polar filament formation has commenced. The morphogenic process of this cell into a spore has begun. Nu, nucleus. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 43
FIGURE 43

sporoblasts histochemically treated to demonstrate the presence of the Golgi-associated enzyme TPPase, which produces an electron-dense reaction product (RP). (A) The TPPase activity in membranes and a dense body (forming polar filament). (B) As maturation of the sporoblast continues, vesicular and lamellar structures associated with the forming polar filament contain to increase the amount of RP. (C) RP is visible in the forming polar filament coil cross sections and the associated vesicular and lamellar structures. No other sporoblast structures contained TPPase activity. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 47
FIGURE 47

spore containing six cross sections of the isofilar polar filament.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 44
FIGURE 44

maturing sporoblasts in a sporophorous vesicle. Note the advanced stage of the developing polar filaments, the absence of the electron-lucent endospore, and the decreased amount of electron-dense material in the episporontal space. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 45
FIGURE 45

Longitudinal section through the anterior portion of a spore. Note the hinge-like structure (arrows) in the anchoring disk (A) attached to the manubroid portion of the polar filament (PF). The polaroplast is divided into three regions, the anterior tightly compressed lamellae (PL) followed by the less compressed region and then the vesicular region (VP). Ribosomes (R) are regularly arranged in tightly packed arrays.

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 46
FIGURE 46

. The polar cap (PC) is well illustrated in this oblique section through the anterior portion of a spore. The tubular nature of the third region of the polaroplast (TP) is well illustrated in this section of the spore. Note the thinning of the spore wall in the region of the polar cap. PL, pleated “compressed” lamellae; PF, polar filament. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 48
FIGURE 48

Electron micrographs of mature spores of . (A) A spore containing a polar filament with 44 to 45 coils arranged in five rows; (B) a spore containing a polar filament with 26 to 27 coils arranged in two or three rows. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 49
FIGURE 49

mature spore containing a fully developed electron-lucent endospore coat. The exospore surface has several vesiculotubular structures on it. Note the presence of nine polar filament cross sections arranged in two rows. This polar filament is anisofilar, and the last two or three cross sections are smaller in diameter than the others. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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Image of FIGURE 50
FIGURE 50

autoinfective spore with extruded polar tubule. Note its ability to pierce through the thick SPOV wall surrounding it. A portion of the tubule is visible in the adjacent cytoplasm where the sporoplasm has been injected. (Reprinted with permission from )

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
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References

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Tables

Generic image for table
TABLE 1

Interfacial relationships of the microsporidia

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3
Generic image for table
TABLE 2

Classification of tubular appendages

Types I to III have been described by ; type IV has been described by .

Citation: Cali A, Takvorian P. 1999. Developmental Morphology and Life Cycles of the Microsporidia, p 85-128. In Wittner M, Weiss L (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC. doi: 10.1128/9781555818227.ch3

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