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The net outcome of symbiosis depends on the costs and benefits to each partner. Those can be context dependent, driving the potential for an interaction to change between parasitism and mutualism. Understanding the baseline fitness impact in an interaction can help us understand those shifts; for an organism that is generally parasitic, it should be easier for it to become a mutualist if its baseline virulence is relatively low. Recently, a microsporidian was found to become beneficial to its Daphnia hosts in certain ecological contexts, but little was known about the symbiont (including its species identity). Here, we identify it as the microsporidium Ordospora pajunii . Despite the parasitic nature of microsporidia, we found O. pajunii to be, at most, mildly virulent; this helps explain why it can shift toward mutualism in certain ecological contexts and helps establish O. pajunii is a valuable model for investigating shifts along the mutualism-parasitism continuum.

Background Microsporidia are obligate intracellular parasites that can infect nearly all invertebrates and vertebrates, posing a threat to public health and causing large economic losses to animal industries such as those of honeybees, silkworms and shrimp. However, the global epidemiology of these pathogens is far from illuminated. Methods Publications on microsporidian infections were obtained from PubMed, Science Direct and Web of Science and filtered according to the Newcastle-Ottawa Quality Assessment Scale. Infection data about pathogens, hosts, geography and sampling dates were manually retrieved from the publications and screened for high quality. Prevalence rates and risk factors for different pathogens and hosts were analyzed by conducting a meta-analysis. The geographic distribution and seasonal prevalence of microsporidian infections were drawn and summarized according to sampling locations and date, respectively. Results Altogether, 287 out of 4129 publications up to 31 January 2020 were obtained and met the requirements, from which 385 epidemiological data records were retrieved and effective. The overall prevalence rates in humans, pigs, dogs, cats, cattle, sheep, nonhuman primates and fowl were 10.2% [2429/30,354; 95% confidence interval (CI) 9.2–11.2%], 39.3% (2709/5105; 95% CI 28.5–50.1%), 8.8% (228/2890; 95% CI 5.1–10.1%), 8.1% (112/1226; 95% CI 5.5–10.8%), 16.6% (2216/12,175; 95% CI 13.5–19.8%), 24.9% (1142/5967; 95% CI 18.6–31.1%), 18.5% (1388/7009; 95% CI 13.1–23.8%) and 7.8% (725/9243; 95% CI 6.4–9.2%), respectively. The higher prevalence in pigs suggests that routine detection of microsporidia in animals should be given more attention, considering their potential roles in zoonotic disease. The highest rate was detected in water, 58.5% (869/1351; 95% CI 41.6–75.5%), indicating that water is an important source of infections. Univariate regression analysis showed that CD4+ T cell counts and the living environment are significant risk factors for humans and nonhuman primates, respectively. Geographically, microsporidia have been widely found in 92 countries, among which Northern Europe and South Africa have the highest prevalence. In terms of seasonality, the most prevalent taxa, Enterocytozoon bieneusi and Encephalitozoon , display different prevalence trends, but no significant difference between seasons was observed. In addition to having a high prevalence, microsporidia are extremely divergent because 728 genotypes have been identified in 7 species. Although less investigated, microsporidia coinfections are more common with human immunodeficiency virus and Cryptosporidium than with other pathogens. Conclusions This study provides the largest-scale meta-analysis to date on microsporidia prevalence in mammals, birds and water worldwide. The results suggest that microsporidia are highly divergent, widespread and prevalent in some animals and water and should be further investigated to better understand their epidemic features. Graphical Abstract

Background Microsporidia MB , a Plasmodium -transmission-impairing symbiont in Anopheles arabiensis , has malaria control potential. This study assessed its prevalence and phylogeny in An. gambiae s.l. and An. funestus in Busia, Kenya and investigated the influence of environmental factors on its occurrence. Additionally, the prevalence of key insecticide resistance mutations in these mosquito populations was determined. Methods Mosquito larvae and adults were collected from three sub-counties in Busia County, Kenya and identified based on morphological characteristics. PCR was used to determine Anopheles species distribution and Microsporidia MB prevalence following DNA extraction from the samples. Insecticide resistance target-site mutations were identified using TaqMan genotyping in a subset of the mosquito samples. Multivariable logistic regression models were used to assess associations of Microsporidia MB infection and ecological factors. Microsporidia MB -positive samples were whole-genome sequenced and phylogenetically analysed. Results Overall, An. gambiae s.l. (including An. gambiae s.s. and possibly An. coluzzii ) comprised 57.3% of samples analysed while An. funestus comprised 25.7% and An. arabiensis 17% and their distribution varied significantly across the three sub-counties (Chi-square, χ² = 577.44, df = 4, p  < 0.001). Microsporidia MB prevalence was low to moderate (0 to 6.4%) and highest in An. gambiae s.l. Anopheles gambiae s.l. showed significantly higher odds of infection compared to An. arabiensis (aOR = 5.94, 95% CI: 1.96–26.77, p  = 0.006). Larvae reared to adults had significantly lower odds of infection than indoor-collected adults (aOR = 0.48, 95% CI: 0.26–0.86, p  = 0.014). Insecticide resistance genotyping revealed high frequencies of kdr- East (94.7%) and kdr- West (60%) mutations in the Anopheles subset analysed, while Ace-1 and GSTe2 mutations were absent. Phylogenetic analysis placed Microsporidia MB isolated from Busia, within Clade IV, closely related to the originally sequenced Ahero reference, but still distinct from other microsporidian clades (I and III). Conclusion The present study highlights the occurrence of Microsporidia MB in multiple Anopheles vectors associated with malaria suggesting its broader potential as a vector control tool. The high prevalence of kdr mutations indicate a significant challenge to insecticide-based vector control in the region. Further investigation into the phenotypic expression of insecticide resistance in these populations is important. Results of the phylogenetic analysis suggest a common ancestry for Microsporidia MB isolates from Busia with the Ahero reference one, highlighting shared traits with potential for malaria control.

Large taxa-rich genome-scale data sets are often necessary for resolving ancient phylogenetic relationships. But accurate phylogenetic inference requires that they are analyzed with realistic models that account for the heterogeneity in substitution patterns amongst the sites, genes and lineages. Two kinds of adjustments are frequently used: models that account for heterogeneity in amino acid frequencies at sites in proteins, and partitioned models that accommodate the heterogeneity in rates (branch lengths) among different proteins in different lineages (protein-wise heterotachy). Although partitioned and site-heterogeneous models are both widely used in isolation, their relative importance to the inference of correct phylogenies has not been carefully evaluated. We conducted several empirical analyses and a large set of simulations to compare the relative performances of partitioned models, site-heterogeneous models, and combined partitioned site heterogeneous models. In general, site-homogeneous models (partitioned or not) performed worse than site heterogeneous, except in simulations with extreme protein-wise heterotachy. Furthermore, simulations using empirically-derived realistic parameter settings showed amarked long-branch attraction (LBA) problem for analyses employing protein-wise partitioning even when the generating model included partitioning. This LBA problem results from a small sample bias compounded over many single protein alignments. In some cases, this problem was ameliorated by clustering similarly-evolving proteins together into larger partitions using the PartitionFinder method. Similar results were obtained under simulations with larger numbers of taxa or heterogeneity in simulating topologies over genes. For an empirical Microsporidia test data set, all but one tested site-heterogeneous models (with or without partitioning) obtain the correct Microsporidia+Fungi grouping, whereas site-homogenous models (with or without partitioning) did not. The single exception was the fully partitioned site-heterogeneous analysis that succumbed to the compounded small sample LBA bias. In general unless protein-wise heterotachy effects are extreme, it is more important to model site-heterogeneity than protein-wise heterotachy in phylogenomic analyses. Complete protein-wise partitioning should be avoided as it can lead to a serious LBA bias. In cases of extreme protein-wise heterotachy, approaches that cluster similarly-evolving proteins together and coupled with site-heterogeneous models work well for phylogenetic estimation.

The ancestors of fungi are believed to be simple aquatic forms with flagellated spores, similar to members of the extant phylum Chytridiomycota (chytrids). Current classifications assume that chytrids form an early-diverging clade within the kingdom Fungi and imply a single loss of the spore flagellum, leading to the diversification of terrestrial fungi. Here we develop phylogenetic hypotheses for Fungi using data from six gene regions and nearly 200 species.Our results indicate that there may have been at least four independent losses of the flagellum in the kingdom Fungi. These losses of swimming spores coincided with the evolution of new mechanisms of spore dispersal, such as aerial dispersal in mycelial groups and polar tube eversion in the microsporidia (unicellular forms that lack mitochondria). The enigmatic microsporidia seem to be derived from an endoparasitic chytrid ancestor similar to Rozella allomycis, on the earliest diverging branch of the fungal phylogenetic tree.

Abstract A vast literature explores a model system that consists of a prey crustacean, the water flea Daphnia spp., and an obligately pathogenic yeast that has been referred to as Metschnikowia bicuspidata and thought to represent the material used by Metschnikoff in his study of innate immunity. Typification of species bearing that name and indeed the whole genus has been problematic as regards yeasts that only grow or form aciculate ascospores in hospite. The neotype of M. bicuspidata, unlike the Daphnia parasite, is easily cultured on a variety of laboratory media, although it too can cause serious infections in a variety of mostly aquatic animals. It has become evident that the Daphnia parasite studied by Metschnikoff or current workers is not closely related to M. bicuspidata as currently understood. Analysis of whole genome DNA extracted from the yeast repeatedly found in infected Daphnia specimens shows that it belongs to the recently circumscribed genus Australozyma. The yeast is described here as Australozyma monospora sp. nov. The species, although haplontic and heterothallic, forms single-spored asci without mating. It also appears that all species in the genus are restricted to asexual reproduction, which may explain their rare status. The holotype is MICH 346683. The name is registered in Mycobank under the number MB 859667. An obligate parasite of Daphnia spp. is described as Australozyma monospora sp. nov.

Pathogens use a variety of secreted and surface proteins to interact with and manipulate their hosts, but a systematic approach for identifying such proteins has been lacking. To identify these ‘host-exposed’ proteins, we used spatially restricted enzymatic tagging followed by mass spectrometry analysis of Caenorhabditis elegans infected with two species of Nematocida microsporidia. We identified 82 microsporidia proteins inside of intestinal cells, including several pathogen proteins in the nucleus. These microsporidia proteins are enriched in targeting signals, are rapidly evolving and belong to large Nematocida -specific gene families. We also find that large, species-specific families are common throughout microsporidia species. Our data suggest that the use of a large number of rapidly evolving species-specific proteins represents a common strategy for microsporidia to interact with their hosts. The unbiased method described here for identifying potential pathogen effectors represents a powerful approach to study a broad range of pathogens. Unbiased identification of proteins from pathogens that are exposed to a host can provide insight into host–pathogen interaction. Here, the authors use an enzymatic tagging method and mass spectrometry to identify rapidly evolving Nematocida microsporidia proteins when infecting C. elegans .

Background Microsporidia MB disrupts Plasmodium development in Anopheles mosquitoes, making it a possible biocontrol tool for malaria. As a tool for vector/disease control, its ecological distribution and the factors that determine their occurrence must be defined. We investigated the frequency of Microsporidia MB in Anopheles mosquitoes across selected sites in northern and southern Ghana, as well as the physicochemical parameters of mosquito breeding water that are associated with the occurrence of the fungus, by fitting regression models. Methods A non-column extraction method was used to extract DNA from the abdomens of 4255 adult Anopheles mosquitoes that emerged from larvae and pupae collected between August and October of 2021 and 2022. Detection of Microsporidia MB was achieved using quantitative PCR (qPCR), while mosquito species were molecularly identified using short interspersed nuclear elements (SINE), restriction fragment length polymorphism (RFLP) methods, and the ANOSPP algorithm. Results Overall Microsporidia MB distribution was 2.2% (92/4255). Male mosquitoes exhibited a higher frequency of infections and had a predicted probability of infection that was 85% higher than that of females. Sites in Ghana's Savannah zone had the highest Microsporidia MB distribution (68.5%). Biochemical oxygen demand in mosquito breeding water was estimated to be positively associated with and significantly predicts Microsporidia MB in mosquitoes with an accuracy of 94%. Increasing ammonium ion concentrations reduced the chances of finding Microsporidia MB -positive mosquitoes. According to our data, all Anopheles mosquitoes, including minor species such as An. squamosus , An. pretoriensis and An. rufipes , had equal probability of Microsporidia MB infection. Conclusions These results provide preliminary information on micro-ecological factors that potentially support the sustainability of Microsporidia MB infection in mosquitoes during their aquatic life stages. It will be important, therefore, to explore the impact of strategies for larval source management on these factors to ensure that the symbiont's persistence during the host's aquatic stages may not be adversely affected should it be used as an integrated approach for mosquito/disease control. Graphical abstract

A new microsporidian species, Globosporidium paramecii gen. nov., sp. nov., from Paramecium primaurelia is described on the basis of morphology, fine structure, and SSU rRNA gene sequence. This is the first case of microsporidiosis in Paramecium reported so far. All observed stages of the life cycle are monokaryotic. The parasites develop in the cytoplasm, at least some part of the population in endoplasmic reticulum and its derivates. Meronts divide by binary fission. Sporogonial plasmodium divides by rosette-like budding. Early sporoblasts demonstrate a well-developed exospore forming blister-like structures. Spores with distinctive spherical shape are dimorphic in size (3.7 ± 0.2 and 1.9 ± 0.2 μm). Both types of spores are characterized by a thin endospore, a short isofilar polar tube making one incomplete coil, a bipartite polaroplast, and a large posterior vacuole. Experimental infection was successful for 5 of 10 tested strains of the Paramecium aurelia species complex. All susceptible strains belong to closely related P. primaurelia and P. pentaurelia species. Phylogenetic analysis placed the new species in the Clade 4 of Microsporidia and revealed its close relationship to Euplotespora binucleata (a microsporidium from the ciliate Euplotes woodruffi), to Helmichia lacustris and Mrazekia macrocyclopis, microsporidia from aquatic invertebrates.

Obligate intracellular pathogens depend on their host for growth yet must also evade detection by host defenses. Here we investigate host adaptation in two Microsporidia, the specialist Edhazardia aedis and the generalist Vavraia culicis , pathogens of disease vector mosquitoes. Genomic analysis and deep RNA-Seq across infection time courses reveal fundamental differences between these pathogens. E. aedis retains enhanced cell surface modification and signalling capacity, upregulating protein trafficking and secretion dynamically during infection. V. culicis is less dependent on its host for basic metabolites and retains a subset of spliceosomal components, with a transcriptome broadly focused on growth and replication. Transcriptional profiling of mosquito immune responses reveals that response to infection by E. aedis differs dramatically depending on the mode of infection, and that antimicrobial defensins may play a general role in mosquito defense against Microsporidia. This analysis illuminates fundamentally different evolutionary paths and host interplay of specialist and generalist pathogens. Microsporidia are intracellular parasitic fungi that infect diverse animal hosts including humans. Here, Desjardins et al. present genomic and transcriptomic data for two microsporidia that infect disease-transmitting mosquitoes, highlighting differences in potential host interplay mechanisms.