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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.

Background Microsporidia MB , a naturally occurring Anopheles symbiont was shown to strongly impair Plasmodium transmission without imposing deleterious fitness effects on larval development, fecundity, adult survival, and adult sex ratio, and for these reasons it is being proposed as a promising tool for malaria control. However, there is a limited knowledge about its ecology, transmission dynamics in the environments with varying abiotic conditions, and whether these could impact on the mode of host transmission. This study aimed to determine the presence and prevalence of Microsporidia MB in rice fields in Benin during both the dry and wet seasons. Methods Anopheles larvae and adults were collected from rice fields and houses around rice fields in two locations (Koussin-Lélé and Magoumi). The collections took place during both the dry and wet seasons. The larvae and adults were molecularly identified to species level using molecular techniques and they were also screened for the presence of Microsporidia MB using PCR following standard protocols. Moreover, breeding sites were also analysed. Results The species identification results revealed that Anopheles coluzzii was the main species in Koussin-Lélé, accounting for 100% of the 1718 samples, while Anopheles gambiae sensu stricto ( s.s .) was predominant in Magoumi accounting for 98.17% of the 986 samples. In Koussin-Lélé, Microsporidia MB prevalence of 14% (n = 276) was observed, whereas in Magoumi, only two samples (0.3%) were tested positive out of 667 screened in the dry season. During the wet season, the prevalence of Microsporidia MB symbiont was low with rates of 0.7% (5) in Koussin-Lélé and 0.6% (8) in Magoumi. However, the prevalence was relatively moderate in adult field collected mosquitoes with 3.09% (n = 1554) followed by larvae samples with 2.93% (n = 682) and adults emerged from field-collected larvae with 2.67% (n = 1235). Analysis of breeding sites revealed high concentrations of nitrate, nitrite and copper in Magoumi during the dry season, which was associated with a low prevalence of Microsporidia MB symbiont in this area. In the wet season, high concentrations of lead and nitrate were recorded in Koussin-Lélé with high concentration of copper in Magoumi, and both localities showed low prevalence of Microsporidia MB infection. Conclusion This study revealed a high prevalence of Microsporidia MB symbiont in Benin during the dry season. Further investigations might be necessary, and modelling of the prevalence and characteristics of breeding sites could help predict the presence of this symbiont in other locations and countries.

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.

Microsporidia are obligate intracellular parasites of most animal groups including humans, but despite their significant economic and medical importance there are major gaps in our understanding of how they exploit infected host cells. We have investigated the evolution, cellular locations and substrate specificities of a family of nucleotide transport (NTT) proteins from Trachipleistophora hominis, a microsporidian isolated from an HIV/AIDS patient. Transport proteins are critical to microsporidian success because they compensate for the dramatic loss of metabolic pathways that is a hallmark of the group. Our data demonstrate that the use of plasma membrane-located nucleotide transport proteins (NTT) is a key strategy adopted by microsporidians to exploit host cells. Acquisition of an ancestral transporter gene at the base of the microsporidian radiation was followed by lineage-specific events of gene duplication, which in the case of T. hominis has generated four paralogous NTT transporters. All four T. hominis NTT proteins are located predominantly to the plasma membrane of replicating intracellular cells where they can mediate transport at the host-parasite interface. In contrast to published data for Encephalitozoon cuniculi, we found no evidence for the location for any of the T. hominis NTT transporters to its minimal mitochondria (mitosomes), consistent with lineage-specific differences in transporter and mitosome evolution. All of the T. hominis NTTs transported radiolabelled purine nucleotides (ATP, ADP, GTP and GDP) when expressed in Escherichia coli, but did not transport radiolabelled pyrimidine nucleotides. Genome analysis suggests that imported purine nucleotides could be used by T. hominis to make all of the critical purine-based building-blocks for DNA and RNA biosynthesis during parasite intracellular replication, as well as providing essential energy for parasite cellular metabolism and protein synthesis.

Secondary symbionts of insects include a range of bacteria and fungi that perform various functional roles on their hosts, such as fitness, tolerance to heat stress, susceptibility to insecticides and effects on reproduction. These endosymbionts could have the potential to shape microbial communites and high potential to develop strategies for mosquito-borne disease control. The relative frequency and molecular phylogeny of Wolbachia, Microsporidia and Cardinium were determined of phlebotomine sand flies and mosquitoes in two regions from Colombia. Illumina Miseq using the 16S rRNA gene as a biomarker was conducted to examine the microbiota. Different percentages of natural infection by Wolbachia, Cardinium, and Microsporidia in phlebotomines and mosquitoes were detected. Phylogenetic analysis of Wolbachia shows putative new strains of Lutzomyia gomezi (wLgom), Brumptomyia hamata (wBrham), and a putative new group associated with Culex nigripalpus (Cnig) from the Andean region, located in Supergroup A and Supergroup B, respectively. The sequences of Microsporidia were obtained of Pi. pia and Cx. nigripalpus, which are located on phylogeny in the IV clade (terrestrial origin). The Cardinium of Tr. triramula and Ps. shannoni were located in group C next to Culicoides sequences while Cardinium of Mi. cayennensis formed two putative new subgroups of Cardinium in group A. In total were obtained 550 bacterial amplicon sequence variants (ASVs) and 189 taxa to the genus level. The microbiota profiles of Sand flies and mosquitoes showed mainly at the phylum level to Proteobacteria (67.6%), Firmicutes (17.9%) and Actinobacteria (7.4%). High percentages of relative abundance for Wolbachia (30%-83%) in Lu. gomezi, Ev. dubitans, Mi. micropyga, Br. hamata, and Cx. nigripalpus were found. ASVs assigned as Microsporidia were found in greater abundance in Pi. pia (23%) and Cx. nigripalpus (11%). An important finding is the detection of Rickettsia in Pi. pia (58,8%) and Bartonella sp. in Cx. nigripalpus. We found that Wolbachia infection significantly decreased the alpha diversity and negatively impacts the number of taxa on sand flies and Culex nigripalpus. The Principal Coordinate Analysis (PCoA) is consistent, which showed statistically significant differences (PERMANOVA, F = 2.4744; R2 = 0.18363; p-value = 0.007) between the microbiota of sand flies and mosquitoes depending on its origin, host and possibly for the abundance of some endosymbionts (Wolbachia, Rickettsia).

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.

Infectious diseases pose one of the greatest threats to endangered species, and a risk of gastrointestinal parasite transmission from humans to wildlife has always been considered as a major concern of tourism. Increased anthropogenic impact on primate populations may result in general changes in communities of their parasites, and also in a direct exchange of parasites between humans and primates. To evaluate the impact of close contact with humans on the occurrence of potentially zoonotic protists in great apes, we conducted a long-term monitoring of microsporidia, Cryptosporidium and Giardia infections in western lowland gorillas at different stages of the habituation process, humans, and other wildlife in Dzanga-Sangha Protected Areas in the Central African Republic. We detected Encephalitozoon cuniculi genotypes I and II (7.5%), Enterocytozoon bieneusi genotype D and three novel genotypes (gorilla 1-3) (4.0%), Giardia intestinalis subgroup A II (2.0%) and Cryptosporidium bovis (0.5%) in gorillas, whereas in humans we found only G. intestinalis subgroup A II (2.1%). In other wild and domestic animals we recorded E. cuniculi genotypes I and II (2.1%), G. intestinalis assemblage E (0.5%) and C. muris TS03 (0.5%). Due to the non-specificity of E. cuniculi genotypes we conclude that detection of the exact source of E. cuniculi infection is problematic. As Giardia intestinalis was recorded primarily in gorilla groups with closer human contact, we suggest that human-gorilla transmission has occurred. We call attention to a potentially negative impact of habituation on selected pathogens which might occur as a result of the more frequent presence of humans in the vicinity of both gorillas under habituation and habituated gorillas, rather than as a consequence of the close contact with humans, which might be a more traditional assumption. We encourage to observe the sections concerning hygiene from the IUCN best practice guidelines for all sites where increased human-gorilla contact occurs.

The dynamics of reductive genome evolution for eukaryotes living inside other eukaryotic cells are poorly understood compared to well-studied model systems involving obligate intracellular bacteria. Here we present 8.5 Mb of sequence from the genome of the microsporidian Trachipleistophora hominis, isolated from an HIV/AIDS patient, which is an outgroup to the smaller compacted-genome species that primarily inform ideas of evolutionary mode for these enormously successful obligate intracellular parasites. Our data provide detailed information on the gene content, genome architecture and intergenic regions of a larger microsporidian genome, while comparative analyses allowed us to infer genomic features and metabolism of the common ancestor of the species investigated. Gene length reduction and massive loss of metabolic capacity in the common ancestor was accompanied by the evolution of novel microsporidian-specific protein families, whose conservation among microsporidians, against a background of reductive evolution, suggests they may have important functions in their parasitic lifestyle. The ancestor had already lost many metabolic pathways but retained glycolysis and the pentose phosphate pathway to provide cytosolic ATP and reduced coenzymes, and it had a minimal mitochondrion (mitosome) making Fe-S clusters but not ATP. It possessed bacterial-like nucleotide transport proteins as a key innovation for stealing host-generated ATP, the machinery for RNAi, key elements of the early secretory pathway, canonical eukaryotic as well as microsporidian-specific regulatory elements, a diversity of repetitive and transposable elements, and relatively low average gene density. Microsporidian genome evolution thus appears to have proceeded in at least two major steps: an ancestral remodelling of the proteome upon transition to intracellular parasitism that involved reduction but also selective expansion, followed by a secondary compaction of genome architecture in some, but not all, lineages.