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PLoS Pathogens Jul 2023Microsporidia are a large phylum of intracellular parasites that can infect most types of animals. Species in the Nematocida genus can infect nematodes including...
Microsporidia are a large phylum of intracellular parasites that can infect most types of animals. Species in the Nematocida genus can infect nematodes including Caenorhabditis elegans, which has become an important model to study mechanisms of microsporidia infection. To understand the genomic properties and evolution of nematode-infecting microsporidia, we sequenced the genomes of nine species of microsporidia, including two genera, Enteropsectra and Pancytospora, without any previously sequenced genomes. Core cellular processes, including metabolic pathways, are mostly conserved across genera of nematode-infecting microsporidia. Each species encodes unique proteins belonging to large gene families that are likely used to interact with host cells. Most strikingly, we observed one such family, NemLGF1, is present in both Nematocida and Pancytospora species, but not any other microsporidia. To understand how Nematocida phenotypic traits evolved, we measured the host range, tissue specificity, spore size, and polar tube length of several species in the genus. Our phylogenetic analysis shows that Nematocida is composed of two groups of species with distinct traits and that species with longer polar tubes infect multiple tissues. Together, our work details both genomic and trait evolution between related microsporidia species and provides a useful resource for further understanding microsporidia evolution and infection mechanisms.
Topics: Animals; Microsporidia; Phylogeny; Nematoda; Caenorhabditis elegans; Genomics
PubMed: 37471459
DOI: 10.1371/journal.ppat.1011510 -
Microbiology Spectrum Feb 2024Microsporidia are obligate intracellular eukaryotic parasites with an extremely broad host range. They have both economic and public health importance. Ploidy in...
Microsporidia are obligate intracellular eukaryotic parasites with an extremely broad host range. They have both economic and public health importance. Ploidy in microsporidia is variable, with a few species formally identified as diploid and one as polyploid. Given the increase in the number of studies sequencing microsporidian genomes, it is now possible to assess ploidy levels across all currently explored microsporidian diversity. We estimate ploidy for all microsporidian data sets available on the Sequence Read Archive using k-mer-based analyses, indicating that polyploidy is widespread in Microsporidia and that ploidy change is dynamic in the group. Using genome-wide heterozygosity estimates, we also show that polyploid microsporidian genomes are relatively homozygous, and we discuss the implications of these findings on the timing of polyploidization events and their origin.IMPORTANCEMicrosporidia are single-celled intracellular parasites, distantly related to fungi, that can infect a broad range of hosts, from humans all the way to protozoans. Exploiting the wealth of microsporidian genomic data available, we use k-mer-based analyses to assess ploidy status across the group. Understanding a genome's ploidy is crucial in order to assemble it effectively and may also be relevant for better understanding a parasite's behavior and life cycle. We show that tetraploidy is present in at least six species in Microsporidia and that these polyploidization events are likely to have occurred independently. We discuss why these findings may be paradoxical, given that Microsporidia, like other intracellular parasites, have extremely small, reduced genomes.
Topics: Humans; Microsporidia; Phylogeny; Evolution, Molecular; Genome, Fungal; Polyploidy
PubMed: 38214524
DOI: 10.1128/spectrum.03669-23 -
Experientia Supplementum (2012) 2022Around 57.1% of microsporidia occupy aquatic environments, excluding a further 25.7% that utilise both terrestrial and aquatic systems. The aquatic microsporidia...
Around 57.1% of microsporidia occupy aquatic environments, excluding a further 25.7% that utilise both terrestrial and aquatic systems. The aquatic microsporidia therefore compose the most diverse elements of the Microsporidia phylum, boasting unique structural features, variable transmission pathways, and significant ecological influence. From deep oceans to tropical rivers, these parasites are present in most aquatic environments and have been shown to infect hosts from across the Protozoa and Animalia. The consequences of infection range from mortality to intricate behavioural change, and their presence in aquatic communities often alters the overall functioning of the ecosystem.In this chapter, we explore aquatic microsporidian diversity from the perspective of aquatic animal health. Examples of microsporidian parasitism of importance to an aquacultural ('One Health') context and ecosystem context are focussed upon. These include infection of commercially important penaeid shrimp by Enterocytozoon hepatopenaei and interesting hyperparasitic microsporidians of wild host groups.Out of ~1500 suggested microsporidian species, 202 have been adequately taxonomically described using a combination of ultrastructural and genetic techniques from aquatic and semi-aquatic hosts. These species are our primary focus, and we suggest that the remaining diversity have additional genetic or morphological data collected to formalise their underlying systematics.
Topics: Animals; Aquaculture; Ecosystem; Microsporidia; Phylogeny; Rivers
PubMed: 35544006
DOI: 10.1007/978-3-030-93306-7_10 -
Acta Parasitologica Jun 2021To evaluate the prevalence of Cryptosporidium and Microsporidia, associated risk factors and species identification in patients with haematological malignancies (HM).
PURPOSE
To evaluate the prevalence of Cryptosporidium and Microsporidia, associated risk factors and species identification in patients with haematological malignancies (HM).
METHODS
A total of 148 consecutive patients with HM and 101 healthy subjects were evaluated for Cryptosporidium and Microsporidia using modified Kinyoun and modified Trichrome staining. Clinical, demographic and laboratory parameters were studied. The species of Cryptosporidium and Microsporidia were studied using PCR-RFLP.
RESULTS
Of 148 HM patients initially screened, 47 were excluded from the final analysis due to inadequate clinical records. Patients with HM [n = 101, 63 (62.4%) male] more often had Cryptosporidium than healthy subjects [n = 101, 65 (74.4%) male] [3/101 (3%) vs. 0/101 (0%), p = 0.02]. Two of 101 (2%) HM patients and none of the healthy subjects had Microsporidia (p = 0.155). Diarrhea was more prevalent in HM patients with Cryptosporidium than those without [3, 100% vs. 39/96, 40.62%; p = 0.04). Both patients infected with Microsporidia presented with persistent diarrhea and fever. Cryptosporidium hominis was identified in all the three HM patients. Enterocytozoon bieneusi was identified in one HM patient infected with Microsporidia, which was classified as genotype Ind2.
CONCLUSION
Cryptosporidium and Microsporidia may infect HM patients leading to overwhelming diarrhea. The commonest species of Cryptosporidium and Microsporidia found to infect HM patients are C. hominis and E. bieneusi.
Topics: Cryptosporidiosis; Cryptosporidium; Enterocytozoon; Feces; Genotype; Hematologic Neoplasms; Humans; Male; Microsporidia; Microsporidiosis; Prevalence
PubMed: 33188485
DOI: 10.1007/s11686-020-00307-x -
Experientia Supplementum (2012) 2022Microsporidia represent an evolutionary outlier in the tree of life and occupy the extreme edge of the eukaryotic domain with some of their biological features. Many of...
Microsporidia represent an evolutionary outlier in the tree of life and occupy the extreme edge of the eukaryotic domain with some of their biological features. Many of these unicellular fungi-like organisms have reduced their genomic content to potentially the lowest limit. With some of the most compacted eukaryotic genomes, microsporidia are excellent model organisms to study reductive evolution and its functional consequences. While the growing number of sequenced microsporidian genomes have elucidated genome composition and organization, a recent increase in complementary post-genomic studies has started to shed light on the impacts of genome reduction in these unique pathogens. This chapter will discuss the biological framework enabling genome minimization and will use one of the most ancient and essential macromolecular complexes, the ribosome, to illustrate the effects of extreme genome reduction on a structural, molecular, and cellular level. We outline how reductive evolution in microsporidia has shaped DNA organization, the composition and function of the ribosome, and the complexity of the ribosome biogenesis process. Studying compacted mechanisms, processes, or macromolecular machines in microsporidia illuminates their unique lifestyle and provides valuable insights for comparative eukaryotic structural biology.
Topics: Evolution, Molecular; Genome, Fungal; Genomics; Microsporidia; Ribosomes
PubMed: 35543997
DOI: 10.1007/978-3-030-93306-7_1 -
Experientia Supplementum (2012) 2022The microsporidia are a phylum of intracellular parasites that represent the eukaryotic cell in a state of extreme reduction, with genomes and metabolic capabilities...
The microsporidia are a phylum of intracellular parasites that represent the eukaryotic cell in a state of extreme reduction, with genomes and metabolic capabilities embodying eukaryotic cells in arguably their most streamlined state. Over the past 20 years, microsporidian genomics has become a rapidly expanding field starting with sequencing of the genome of Encephalitozoon cuniculi, one of the first ever sequenced eukaryotes, to the current situation where we have access to the data from over 30 genomes across 20+ genera. Reaching back further in evolutionary history, to the point where microsporidia diverged from other eukaryotic lineages, we now also have genomic data for some of the closest known relatives of the microsporidia such as Rozella allomycis, Metchnikovella spp. and Amphiamblys sp. Data for these organisms allow us to better understand the genomic processes that shaped the emergence of the microsporidia as a group. These intensive genomic efforts have revealed some of the processes that have shaped microsporidian cells and genomes including patterns of genome expansions and contractions through gene gain and loss, whole genome duplication, differential patterns of invasion and purging of transposable elements. All these processes have been shown to occur across short and longer time scales to give rise to a phylum of parasites with dynamic genomes with a diversity of sizes and organisations.
Topics: Base Sequence; Evolution, Molecular; Genome, Fungal; Genomics; Microsporidia
PubMed: 35543998
DOI: 10.1007/978-3-030-93306-7_2 -
Trends in Parasitology Aug 2022Microsporidian diversity is vast. There is a renewed drive to understand how microsporidian pathological, genomic, and ecological traits relate to their phylogeny. We... (Review)
Review
Microsporidian diversity is vast. There is a renewed drive to understand how microsporidian pathological, genomic, and ecological traits relate to their phylogeny. We comprehensively sample and phylogenetically analyse 125 microsporidian genera for which sequence data are available. Comparing these results with existing phylogenomic analyses, we suggest an updated taxonomic framework to replace the inconsistent clade numbering system, using informal taxonomic names: Glugeida (previously clades 5/3), Nosematida (4a), Enterocytozoonida (4b), Amblyosporida (3/5), Neopereziida (1), and Ovavesiculida (2). Cellular, parasitological, and ecological traits for 281 well-defined species are compared with identify clade-specific patterns across long-branch Microsporidia. We suggest that future taxonomic circumscriptions of Microsporidia should involve additional markers (SSU/ITS/LSU), and that a comprehensive suite of phenotypic and ecological traits help to predict broad microsporidian functional and lineage diversity.
Topics: Microsporidia; Phylogeny
PubMed: 35667993
DOI: 10.1016/j.pt.2022.05.007 -
Experientia Supplementum (2012) 2022Microsporidia are poorly understood, ubiquitous eukaryotic parasites that are completely dependent on their hosts for replication. With the discovery of microsporidia... (Review)
Review
Microsporidia are poorly understood, ubiquitous eukaryotic parasites that are completely dependent on their hosts for replication. With the discovery of microsporidia species naturally infecting the genetically tractable transparent nematode C. elegans, this host has been used to explore multiple areas of microsporidia biology. Here we review results about microsporidia infections in C. elegans, which began with the discovery of the intestinal-infecting species Nematocida parisii. Recent findings include new species identification in the Nematocida genus, with more intestinal-infecting species, and also a species with broader tissue tropism, the epidermal and muscle-infecting species Nematocida displodere. This species has a longer polar tube infection apparatus, which may enable its wider tissue range. After invasion, multiple Nematocida species appear to fuse host cells, which likely promotes their dissemination within host organs. Localized proteomics identified Nematocida proteins that have direct contact with the C. elegans intestinal cytosol and nucleus, and many of these host-exposed proteins belong to expanded, species-specific gene families. On the host side, forward genetic screens have identified regulators of the Intracellular Pathogen Response (IPR), which is a transcriptional response induced by both microsporidia and the Orsay virus, which is also a natural, obligate intracellular pathogen of the C. elegans intestine. The IPR constitutes a novel immune/stress response that promotes resistance against microsporidia, virus, and heat shock. Overall, the Nematocida/C. elegans system has provided insights about strategies for microsporidia pathogenesis, as well as innate defense pathways against these parasites.
Topics: Animals; Biology; Caenorhabditis elegans; Caenorhabditis elegans Proteins; Host-Pathogen Interactions; Microsporidia
PubMed: 35544001
DOI: 10.1007/978-3-030-93306-7_5 -
Genome Biology and Evolution May 2021There is an expectation that analyses of molecular sequences might be able to distinguish between alternative hypotheses for ancient relationships, but the phylogenetic... (Review)
Review
There is an expectation that analyses of molecular sequences might be able to distinguish between alternative hypotheses for ancient relationships, but the phylogenetic methods used and types of data analyzed are of critical importance in any attempt to recover historical signal. Here, we discuss some common issues that can influence the topology of trees obtained when using overly simple models to analyze molecular data that often display complicated patterns of sequence heterogeneity. To illustrate our discussion, we have used three examples of inferred relationships which have changed radically as models and methods of analysis have improved. In two of these examples, the sister-group relationship between thermophilic Thermus and mesophilic Deinococcus, and the position of long-branch Microsporidia among eukaryotes, we show that recovering what is now generally considered to be the correct tree is critically dependent on the fit between model and data. In the third example, the position of eukaryotes in the tree of life, the hypothesis that is currently supported by the best available methods is fundamentally different from the classical view of relationships between major cellular domains. Since heterogeneity appears to be pervasive and varied among all molecular sequence data, and even the best available models can still struggle to deal with some problems, the issues we discuss are generally relevant to phylogenetic analyses. It remains essential to maintain a critical attitude to all trees as hypotheses of relationship that may change with more data and better methods.
Topics: Biological Evolution; Deinococcus; Microsporidia; Models, Genetic; Phylogeny; Thermus
PubMed: 33772552
DOI: 10.1093/gbe/evab067 -
Parasites & Vectors Apr 2022Microsporidia are a group of intracellular parasitic eukaryotes, serious pathogens that cause widespread infection in humans, vertebrates, and invertebrates. Because...
BACKGROUND
Microsporidia are a group of intracellular parasitic eukaryotes, serious pathogens that cause widespread infection in humans, vertebrates, and invertebrates. Because microsporidia have a thick spore wall structure, the in vitro transformation, cell culture, and genetic operation technology of microsporidia are far behind that of other parasites.
METHODS
In this study, according to an analysis of the life-cycle of microsporidia, Nosema bombycis, and different electro-transformation conditions, the transduction efficiency of introducing foreign genes into N. bombycis was systematically determined.
RESULTS
We analyzed the direct electro-transformation of foreign genes into germinating N. bombycis using reporters under the regulation of different characteristic promoters. Furthermore, we systematically determined the efficiency of electro-transformation into N. bombycis under different electro-transformation conditions and different developmental stages through an analysis of the whole life-cycle of N. bombycis. These results revealed that foreign genes could be effectively introduced through a perforation voltage of 100 V pulsed for 15 ms during the period of N. bombycis sporeplasm proliferation.
CONCLUSIONS
We present an effective method for electro-transformation of a plasmid encoding a fluorescent protein into N. bombycis, which provides new insight for establishing genetic modifications and potential applications in these intracellular parasites.
Topics: Animals; Bombyx; Electroporation; Humans; Nosema; Spores, Fungal
PubMed: 35449112
DOI: 10.1186/s13071-022-05236-4