The Microsporidian Polar Tube and Spore Wall

Weiss, Louis M.; Delbac, Frédéric; Hayman, J. Russell; Pan, Guoqing; Dang, Xiaoqun; Zhou, Zeyang

doi:10.1002/9781118395264.ch10

Cited by 26 publications

(18 citation statements)

References 212 publications

(470 reference statements)

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“…Based upon in silico predictions it appears that microsporidians cannot make pyrimidines de novo so there is a transport gap that needs to be filled [ 11 , 13 , 14 ]. UDP-N-acetylglucosamine is the direct monomeric precursor for chitin synthesis, an integral component of the microsporidian spore wall [ 34 ], but it is also biosynthesised by the mammalian host cell in which it plays roles as a co-enzyme, signalling molecule, and precursor for glycosylation [ 35 , 36 ]. The pyrimidine UDP is liberated from UDP-N-acetylglucosamine during chitin polymerisation by chitin synthase and during glycosylation, so as well as providing chitin precursors this novel transporter could potentially provide the starting substrate to make pyrimidines needed for T. hominis DNA and RNA biosynthesis (Fig.…”

Section: Resultsmentioning

confidence: 99%

Transcriptomic profiling of host-parasite interactions in the microsporidian Trachipleistophora hominis

Watson

Williams

et al. 2015

BMC Genomics

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BackgroundTrachipleistophora hominis was isolated from an HIV/AIDS patient and is a member of a highly successful group of obligate intracellular parasites.MethodsHere we have investigated the evolution of the parasite and the interplay between host and parasite gene expression using transcriptomics of T. hominis-infected rabbit kidney cells.ResultsT. hominis has about 30 % more genes than small-genome microsporidians. Highly expressed genes include those involved in growth, replication, defence against oxidative stress, and a large fraction of uncharacterised genes. Chaperones are also highly expressed and may buffer the deleterious effects of the large number of non-synonymous mutations observed in essential T. hominis genes. Host expression suggests a general cellular shutdown upon infection, but ATP, amino sugar and nucleotide sugar production appear enhanced, potentially providing the parasite with substrates it cannot make itself. Expression divergence of duplicated genes, including transporters used to acquire host metabolites, demonstrates ongoing functional diversification during microsporidian evolution. We identified overlapping transcription at more than 100 loci in the sparse T. hominis genome, demonstrating that this feature is not caused by genome compaction. The detection of additional transposons of insect origin strongly suggests that the natural host for T. hominis is an insect.ConclusionsOur results reveal that the evolution of contemporary microsporidian genomes is highly dynamic and innovative. Moreover, highly expressed T. hominis genes of unknown function include a cohort that are shared among all microsporidians, indicating that some strongly conserved features of the biology of these enormously successful parasites remain uncharacterised.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1989-z) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Transcriptomic profiling of host-parasite interactions in the microsporidian Trachipleistophora hominis

Watson

Williams

et al. 2015

BMC Genomics

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“…However, given that the distance from the lumen to the basolateral side of the intestine is variable within an animal, with some distances being as short as 2 μm (see Figs 2A and 5A ), polar tube lengths are not the only limiting factor for infecting non-intestinal tissues from the intestinal lumen. It is possible that spores must convey enough force on the polar tube upon germination in order to pierce through multiple membranes to reach non-intestinal tissues [ 31 ], or that specific proteins are required on the polar tube for interaction with tissue-specific host factors on a cell for polar tube entry and invasion [ 34 , 35 ].…”

Section: Discussionmentioning

confidence: 99%

Discovery of a Natural Microsporidian Pathogen with a Broad Tissue Tropism in Caenorhabditis elegans

et al. 2016

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Microbial pathogens often establish infection within particular niches of their host for replication. Determining how infection occurs preferentially in specific host tissues is a key aspect of understanding host-microbe interactions. Here, we describe the discovery of a natural microsporidian parasite of the nematode Caenorhabditis elegans that displays a unique tissue tropism compared to previously described parasites of this host. We characterize the life cycle of this new species, Nematocida displodere, including pathogen entry, intracellular replication, and exit. N. displodere can invade multiple host tissues, including the epidermis, muscle, neurons, and intestine of C. elegans. Despite robust invasion of the intestine very little replication occurs there, with the majority of replication occurring in the muscle and epidermis. This feature distinguishes N. displodere from two closely related microsporidian pathogens, N. parisii and N. sp. 1, which exclusively invade and replicate in the intestine. Comparison of the N. displodere genome with N. parisii and N. sp. 1 reveals that N. displodere is the earliest diverging species of the Nematocida genus. Over 10% of the proteins encoded by the N. displodere genome belong to a single species-specific family of RING-domain containing proteins of unknown function that may be mediating interactions with the host. Altogether, this system provides a powerful whole-animal model to investigate factors responsible for pathogen growth in different tissue niches.

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“…Germination conditions, to activate PT firing, are different among microsporidia species 46,47,74 . For A. algerae, the germination buffer was slightly modified from the previously reported condition 46 .…”

Section: Germination Conditions For Microsporidia Sporesmentioning

confidence: 99%

3-Dimensional Organization and Dynamics of the Microsporidian Polar Tube Invasion Machinery

Jaroenlak

Cammer

Davydov

et al. 2020

Preprint

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Microsporidia, a divergent group of single-celled eukaryotic parasites, harness a specialized harpoon-like invasion apparatus called the polar tube (PT) to gain entry into host cells. The PT is tightly coiled within the transmissible extracellular spore, and is about 20 times the length of the spore. Once triggered, the PT is rapidly ejected and is thought to penetrate the host cell, acting as a conduit for the transfer of infectious cargo into the host. The organization of this specialized infection apparatus in the spore, how it is deployed, and how the nucleus and other large cargo are transported through the narrow PT are not well understood. Here we use serial block-face scanning electron microscopy to reveal the 3-dimensional architecture of the PT and its relative spatial orientation to other organelles within the spore. Using high-speed optical microscopy, we also capture and quantify the entire PT germination process in vitro. Our results show that the emerging PT experiences very high accelerating forces to reach velocities exceeding 300 μm⋅s -1 , and that firing kinetics differ markedly between species. Live-cell imaging reveals that the nucleus, which is approximately 7 times larger than the diameter of the PT, undergoes extreme deformation to fit through the narrow tube, and moves at speeds comparable to PT extension. Our study sheds new light on the 3-dimensional organization, dynamics, and mechanism of PT extrusion, and shows how infectious cargo moves through the tube to initiate infection.

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The Microsporidian Polar Tube and Spore Wall

Cited by 26 publications

References 212 publications

Transcriptomic profiling of host-parasite interactions in the microsporidian Trachipleistophora hominis

Transcriptomic profiling of host-parasite interactions in the microsporidian Trachipleistophora hominis

Discovery of a Natural Microsporidian Pathogen with a Broad Tissue Tropism in Caenorhabditis elegans

3-Dimensional Organization and Dynamics of the Microsporidian Polar Tube Invasion Machinery

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