Morphology and Transcriptome Analysis of <named-content content-type="genus-species">Nosema bombycis</named-content> Sporoplasm and Insights into the Initial Infection of Microsporidia

ABSTRACT Microsporidia are obligate intracellular parasites that infect a wide variety of host organisms, including humans. The sporoplasm is the initial stage of microsporidian infection and proliferation, but its morphological and molecular characteristics are poorly understood. In this study, the...

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Autores principales:	Qiang He, Jian Luo, Jin-Zhi Xu, Chun-xia Wang, Xian-zhi Meng, Guo-Qing Pan, Tian Li, Ze-Yang Zhou
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	sporoplasm microsporidia Nosema bombycis morphology infection mechanism transcriptome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d6e0787cc5e74e90b1a02efa28405d79
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spelling	oai:doaj.org-article:d6e0787cc5e74e90b1a02efa28405d792021-11-15T15:27:53ZMorphology and Transcriptome Analysis of <named-content content-type="genus-species">Nosema bombycis</named-content> Sporoplasm and Insights into the Initial Infection of Microsporidia10.1128/mSphere.00958-192379-5042https://doaj.org/article/d6e0787cc5e74e90b1a02efa28405d792020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00958-19https://doaj.org/toc/2379-5042ABSTRACT Microsporidia are obligate intracellular parasites that infect a wide variety of host organisms, including humans. The sporoplasm is the initial stage of microsporidian infection and proliferation, but its morphological and molecular characteristics are poorly understood. In this study, the sporoplasm of Nosema bombycis was successfully isolated and characterized after the induction of spore germination in vitro. The sporoplasm was spherical, 3.64 ± 0.41 μm in diameter, had the typical two nuclei, and was nonrefractive. Scanning and transmission electron microscopy analyses revealed that the sporoplasm was surrounded by a single membrane, and the cytoplasm was usually filled with relatively homogeneous granules, possibly ribosomes, and contained a vesicular structure comprising a concentric ring and coiled tubules. Propidium iodide staining revealed that the sporoplasm membrane showed stronger membrane permeability than did the cell plasma membrane. Transmission electron microscopy (TEM) revealed that the sporoplasm can gain entry to the host cell by phagocytosis. Transcriptome analysis of mature spores and sporoplasms showed that 541 significantly differentially expressed genes were screened (adjusted P value [Padj] < 0.05), of which 302 genes were upregulated and 239 genes were downregulated in the sporoplasm. The majority of the genes involved in trehalose synthesis metabolism, glycolysis, and the pentose phosphate pathway were downregulated, whereas 10 transporter genes were upregulated, suggesting that the sporoplasm may inhibit its own carbon metabolic activity and obtain the substances required for proliferation through transporter proteins. This study represents the first comprehensive and in-depth investigation of the sporoplasm at the morphological and molecular levels and provides novel insights into the biology of microsporidia and their infection mechanism. IMPORTANCE Once awoken from dormancy, the cellular matter of microsporidia is delivered directly into the host cell cytoplasm through the polar tube. This means that the microsporidia are difficult to study biologically in their active state without a contaminating signal from the host cell. Sporoplasm is a cell type of microsporidia in vitro, but relatively little attention has been paid to the sporoplasm in the past 150 years due to a lack of an effective separation method. Nosema bombycis, the first reported microsporidium, is a type of obligate intracellular parasite that infects silkworms and can be induced to germinate in alkaline solution in vitro. We successfully separated the N. bombycis sporoplasm in vitro, and the morphological and structural characteristics were investigated. These results provide important insight into the biology and pathogenesis of microsporidia and potentially provide a possible strategy for genetic manipulation of microsporidia targeting the sporoplasm.Qiang HeJian LuoJin-Zhi XuChun-xia WangXian-zhi MengGuo-Qing PanTian LiZe-Yang ZhouAmerican Society for MicrobiologyarticlesporoplasmmicrosporidiaNosema bombycismorphologyinfection mechanismtranscriptomeMicrobiologyQR1-502ENmSphere, Vol 5, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	sporoplasm microsporidia Nosema bombycis morphology infection mechanism transcriptome Microbiology QR1-502
spellingShingle	sporoplasm microsporidia Nosema bombycis morphology infection mechanism transcriptome Microbiology QR1-502 Qiang He Jian Luo Jin-Zhi Xu Chun-xia Wang Xian-zhi Meng Guo-Qing Pan Tian Li Ze-Yang Zhou Morphology and Transcriptome Analysis of <named-content content-type="genus-species">Nosema bombycis</named-content> Sporoplasm and Insights into the Initial Infection of Microsporidia
description	ABSTRACT Microsporidia are obligate intracellular parasites that infect a wide variety of host organisms, including humans. The sporoplasm is the initial stage of microsporidian infection and proliferation, but its morphological and molecular characteristics are poorly understood. In this study, the sporoplasm of Nosema bombycis was successfully isolated and characterized after the induction of spore germination in vitro. The sporoplasm was spherical, 3.64 ± 0.41 μm in diameter, had the typical two nuclei, and was nonrefractive. Scanning and transmission electron microscopy analyses revealed that the sporoplasm was surrounded by a single membrane, and the cytoplasm was usually filled with relatively homogeneous granules, possibly ribosomes, and contained a vesicular structure comprising a concentric ring and coiled tubules. Propidium iodide staining revealed that the sporoplasm membrane showed stronger membrane permeability than did the cell plasma membrane. Transmission electron microscopy (TEM) revealed that the sporoplasm can gain entry to the host cell by phagocytosis. Transcriptome analysis of mature spores and sporoplasms showed that 541 significantly differentially expressed genes were screened (adjusted P value [Padj] < 0.05), of which 302 genes were upregulated and 239 genes were downregulated in the sporoplasm. The majority of the genes involved in trehalose synthesis metabolism, glycolysis, and the pentose phosphate pathway were downregulated, whereas 10 transporter genes were upregulated, suggesting that the sporoplasm may inhibit its own carbon metabolic activity and obtain the substances required for proliferation through transporter proteins. This study represents the first comprehensive and in-depth investigation of the sporoplasm at the morphological and molecular levels and provides novel insights into the biology of microsporidia and their infection mechanism. IMPORTANCE Once awoken from dormancy, the cellular matter of microsporidia is delivered directly into the host cell cytoplasm through the polar tube. This means that the microsporidia are difficult to study biologically in their active state without a contaminating signal from the host cell. Sporoplasm is a cell type of microsporidia in vitro, but relatively little attention has been paid to the sporoplasm in the past 150 years due to a lack of an effective separation method. Nosema bombycis, the first reported microsporidium, is a type of obligate intracellular parasite that infects silkworms and can be induced to germinate in alkaline solution in vitro. We successfully separated the N. bombycis sporoplasm in vitro, and the morphological and structural characteristics were investigated. These results provide important insight into the biology and pathogenesis of microsporidia and potentially provide a possible strategy for genetic manipulation of microsporidia targeting the sporoplasm.
format	article
author	Qiang He Jian Luo Jin-Zhi Xu Chun-xia Wang Xian-zhi Meng Guo-Qing Pan Tian Li Ze-Yang Zhou
author_facet	Qiang He Jian Luo Jin-Zhi Xu Chun-xia Wang Xian-zhi Meng Guo-Qing Pan Tian Li Ze-Yang Zhou
author_sort	Qiang He
title	Morphology and Transcriptome Analysis of <named-content content-type="genus-species">Nosema bombycis</named-content> Sporoplasm and Insights into the Initial Infection of Microsporidia
title_short	Morphology and Transcriptome Analysis of <named-content content-type="genus-species">Nosema bombycis</named-content> Sporoplasm and Insights into the Initial Infection of Microsporidia
title_full	Morphology and Transcriptome Analysis of <named-content content-type="genus-species">Nosema bombycis</named-content> Sporoplasm and Insights into the Initial Infection of Microsporidia
title_fullStr	Morphology and Transcriptome Analysis of <named-content content-type="genus-species">Nosema bombycis</named-content> Sporoplasm and Insights into the Initial Infection of Microsporidia
title_full_unstemmed	Morphology and Transcriptome Analysis of <named-content content-type="genus-species">Nosema bombycis</named-content> Sporoplasm and Insights into the Initial Infection of Microsporidia
title_sort	morphology and transcriptome analysis of <named-content content-type="genus-species">nosema bombycis</named-content> sporoplasm and insights into the initial infection of microsporidia
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/d6e0787cc5e74e90b1a02efa28405d79
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Morphology and Transcriptome Analysis of <named-content content-type="genus-species">Nosema bombycis</named-content> Sporoplasm and Insights into the Initial Infection of Microsporidia

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