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Differences in gene length among microsporidia and their fungal relatives. (a) Comparison of the length (in amino acids) of O. bayeri proteins to orthologs from Enc. cuniculi, Ent. bieneusi, S. cerevisiae, U. maydis, B. dendrobatidis and R. oryzae. In general, O. bayeri proteins are longer than microsporidian orthologues, but shorter than fungal orthologues. Vertical arrows indicate the average reduction or increase in protein size compared to O. bayeri. (b) Specific examples of length variation between orthologs from O. bayeri, Enc. cuniculi, Ent. bieneusi and S. cerevisiae.
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The highly compacted 2.9-Mb genome of Encephalitozoon cuniculi placed the microsporidia in the spotlight, encoding a mere 2,000 proteins and a highly reduced suite of biochemical pathways. This extreme level of reduction is not universal across the microsporidia, with genomes known to vary up to sixfold in size, suggesting that some genomes may har...
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... Neben vielen Studien zum Thema Wirt-Parasit-Interaktion rückt H. tvaerminnensis wegen seines Mikrosporidien-untypischen Genoms auch immer mehr ins Zen trum von genetischen Studien [5]. Bereits früh war klar, dass H. tvaerminnensis viel mehr nicht codierende DNA zwischen seinen Genen aufweist, als dies von anderen Mikrosporidien bekannt war [6]. Eine erste Hypothese postulierte deshalb eine Kombination aus geringerer Genomreduktion und sekundärer Genomexpansion als Erklärung für das größere Genom [3]. ...
Genomics is a powerful toolkit for unravelling how evolutionary processes drive organisms’ small- and large-scale genetic variation. Several outstanding questions remain concerning the evolution of genome size and architecture, especially in intracellular parasites. Microsporidia became a model for this field of study as they exhibit genome size variation of more than an order of magnitude. Here, we discuss evolution in the large-genome microsporidium Hamiltosporidium tvaerminnensis, a parasite of a water flea.
... A previous genome study of EHP was first reported in L. vannamei from Thailand (Dominic et al. 2017), revealing a genome size of 3.26 Mb with a GC content of 25.45%, and 64 contigs encoding 2540 genes, similar to our sequencing results. Since then, there have been few related reports, so we also questioned whether the genome of Chinese EHP had evolved and become compact, as genome contraction and compression are typical features of microsporidian genomes (Corradi et al. 2009). ...
Enterocytozoon hepatopenaei (EHP) is an obligate intracellular parasite of shrimp, that may cause growth retardation or even death of shrimp. However, the characteristics of the EHP genome and its evolutionary relationships with other microsporidian genomes are not well understood. In this research, the whole genome of a strain of EHP isolated from Litopenaeus vannamei was sequenced, and detailed functional annotation was performed by using different public databases and genome component analysis. The genome size was 3.03 Mb, with 15 contigs and 2283 protein-coding genes. There were 46 tRNAs and 14 rRNAs (including 6 5S rRNAs, 4 18S rRNAs, and 4 28S rRNAs) in the genome. In addition, details of EHP evolution were revealed by comparative genomic analysis, including analyses of gene family clustering, phylogenetic relationships, gene family expansion and contraction, and synteny. The results will deepen our understanding of the EHP genome and its evolutionary features.
... Large-sized microsporidia genomes are generally difficult to assemble due to a high number of repetitive elements (Parisot et al., 2014). H. tvaerminnensis has been the target of previous assembly trials using shotgun and Illumina sequencing (Corradi et al., 2009;Haag et al., 2020). Here, we were able to produce a very contiguous genome assembly of this microsporidium with a large genome size using long-read PacBio sequencing. ...
Analyzing variation in a species’ genomic diversity can provide insights into its historical demography, biogeography and population structure, and thus, its ecology and evolution. Although such studies are rarely undertaken for parasites, they can be highly revealing because of the parasite’s coevolutionary relationships with hosts. Modes of reproduction and transmission are thought to be strong determinants of genomic diversity for parasites and vary widely among microsporidia (fungal‐related intracellular parasites), which are known to have high intraspecific genetic diversity and interspecific variation in genome architecture. Here we explore genomic variation in the microsporidium Hamiltosporidium, a parasite of the freshwater crustacean Daphnia magna, looking especially at which factors contribute to nucleotide variation. Genomic samples from 18 Eurasian populations and a new, long‐read based reference genome were used to determine the roles that reproduction mode, transmission mode and geography play in determining population structure and demographic history. We demonstrate two main H. tvaerminnensis lineages and a pattern of isolation‐by‐distance, but note an absence of congruence between these two parasite lineages and the two Eurasian host lineages. We suggest a comparatively recent parasite spread through Northern Eurasian host populations after a change from vertical to mixed‐mode transmission and the loss of sexual reproduction. While gaining knowledge about the ecology and evolution of this focal parasite, we also identify common features that shape variation in genomic diversity for many parasites, e.g., distinct modes of reproduction and the intertwining of host–parasite demographies.
... 615Comparatively high genomic variation in Hamiltosporidium 617Large-sized microsporidia genomes are generally difficult to assemble due to a high number of 618 repetitive elements(Parisot et al., 2014). H. tvaerminnensis has been target of previous assembly 619 trials using shotgun and Illumina sequencing(Corradi et al., 2009;Haag et al., 2020). Here, we were 620 able to produce a very contiguous genome assembly of this microsporidium with a large genome 621 size using long-read PacBio sequencing. ...
Analyzing variation in a species' genomic diversity can provide insights into its historical demography, biogeography and population structure, and thus, its ecology and evolution. Although such studies are rarely undertaken for parasites, they can be highly revealing because of the parasite's coevolutionary relationships with hosts. Modes of reproduction and transmission are thought to be strong determinants of genomic diversity for parasites and vary widely among microsporidia (fungal-related intracellular parasites), which are known to have high intraspecific genetic diversity and interspecific variation in genome architecture. Here we explore genomic variation in the microsporidium Hamiltosporidium, a parasite of the freshwater crustacean Daphnia magna, looking especially at which factors contribute to nucleotide variation. Genomic samples from 18 Eurasian populations and a new, long-read based reference genome were used to determine the roles that reproduction mode, transmission mode and geography play in determining population structure and demographic history. We demonstrate two main H. tvaerminnensis lineages and a pattern of isolation-by-distance, but note an absence of congruence between these two parasite lineages and the two Eurasian host lineages. We suggest a comparatively recent parasite spread through Northern Eurasian host populations after a change from vertical to mixed-mode transmission and the loss of sexual reproduction. While gaining knowledge about the ecology and evolution of this focal parasite, we also identify common features that shape variation in genomic diversity for many parasites, e.g., distinct modes of reproduction and the intertwining of host-parasite demographies.
... The protein sequences of other 19 microsporidian parasites (Encephalitozoon romaleae, Encephalitozoon hellem, Encephalitozoon intestinalis, Encephalitozoon cuniculi, Ordospora colligata, Nosema apis, Nosema bombycis, Enterocytozoon bieneusi, Enterospora canceri, Enterocytozoon hepatopenae, Vittaforma corneae, Trachipleistophora hominis, Vavraia culicis, Pseudoloma neurophilia, Edhazardia aedis, Anncaliia algerae, and Nematocida parisii) with assembled genomes were retrieved from NCBI and MicrosporidianDB 1 , 2 (Katinka et al., 2001;Corradi et al., 2007Corradi et al., , 2009Corradi et al., , 2010Cuomo et al., 2012;Heinz et al., 2012;Pombert et al., 2012Pombert et al., , 2013Pombert et al., , 2015Campbell et al., 2013;Chen Y. et al., 2013;Pan et al., 2013;Haag et al., 2014;Desjardins et al., 2015;Ndikumana et al., 2017;Reinke et al., 2017;Wiredu Boakye et al., 2017). These protein sequences were all used to query the BUSCO gene set microsporidian_odb 10 (Simao et al., 2015;Seppey et al., 2019). ...
Microsporidia comprise a phylum of single cell, intracellular parasites and represent the earliest diverging branch in the fungal kingdom. The microsporidian parasite Nosema ceranae primarily infects honey bee gut epithelial cells, leading to impaired memory, suppressed host immune responses and colony collapse under certain circumstances. As the genome of N. ceranae is challenging to assembly due to very high genetic diversity and repetitive region, the genome was re-sequenced using long reads. We present a robust 8.8 Mbp genome assembly of 2,280 protein coding genes, including a high number of genes involved in transporting nutrients and energy, as well as drug resistance when compared with sister species Nosema apis. We also describe the loss of the critical protein Dicer in approximately half of the microsporidian species, giving new insights into the availability of RNA interference pathway in this group. Our results provided new insights into the pathogenesis of N. ceranae and a blueprint for treatment strategies that target this parasite without harming honey bees. The unique infectious apparatus polar filament and transportation pathway members can help to identify treatments to control this parasite.
... Microsporidia are a large group of obligate intracellular parasites of insects and mammals [1][2][3][4][5][6][7][8]. The taxonomic status of this group of unicellular parasites remains controversial, although recent studies have suggested that microsporidia belong to the fungal kingdom. ...
Microsporidia are a large group of unicellular parasites that infect insects and mammals. The simpler life cycle of microsporidia in insects provides a model system for understanding their evolution and molecular interactions with their hosts. However, no complete genome is available for insect-parasitic microsporidian species. The complete genome of Antonospora locustae , a microsporidian parasite that obligately infects insects, is reported here. The genome size of A. locustae is 3 170 203 nucleotides, composed of 17 chromosomes onto which a total of 1857 annotated genes have been mapped and detailed. A unique feature of the A. locustae genome is the presence of an ultra-low GC region of approximately 25 kb on 16 of the 17 chromosomes, in which the average GC content is only 20 %. Transcription profiling indicated that the ultra-low GC region of the parasite could be associated with differential regulation of host defences in the fat body to promote the parasite’s survival and propagation. Phylogenetic gene analysis showed that A. locustae , and the microsporidian family in general, is likely at an evolutionarily transitional position between prokaryotes and eukaryotes, and that it evolved independently. Transcriptomic analysis showed that A. locustae can systematically inhibit the locust phenoloxidase PPO, TCA and glyoxylate cycles, and PPAR pathways to escape melanization, and can activate host energy transfer pathways to support its reproduction in the fat body, which is an insect energy-producing organ. Our study provides a platform and model for studies of the molecular mechanisms of microsporidium–host interactions in an energy-producing organ and for understanding the evolution of microsporidia.
... At the other extreme are the large, gene-sparse genomes of several phylogenetically distant species, such as Edhazardia aedis (≅ 50 Mb), Hamiltosporidium spp. (≅ 17-25 Mb), Nosema bombycis (≅ 15 Mb) and Anncaliia algerae (≅ 12-17 Mb) [6][7][8][9][10]. ...
The extreme genome reduction and physiological simplicity of some microsporidia has been attributed to their intracellular, obligate parasitic lifestyle. Although not all microsporidian genomes are small (size range from about 2 to 50 MB), it is suggested that the size of their genomes has been streamlined by natural selection. We explore the hypothesis that vertical transmission in microsporidia produces population bottlenecks, and thus reduces the effectiveness of natural selection. Here we compare the transposable element (TE) content of 47 microsporidian genomes, and show that genome size is positively correlated with the amount of TEs, and that species that experience vertical transmission have larger genomes with higher proportion of TEs. Our findings are consistent with earlier studies inferring that nonadaptive processes play an important role in microsporidian evolution.
... At the other extreme are the large, gene-sparse genomes of several phylogenetically distant species, such as Edhazardia aedis (≅ 50 Mb), Hamiltosporidium spp. (≅ 17-25 Mb), Nosema bombycis (≅ 15 Mb) and Anncaliia algerae (≅ 12-17 Mb) [6][7][8][9][10]. Despite showing an about 25-fold difference in size, the gene-sparse and gene-dense genomes only differ by a factor of 2-3 in the number of proteins they encode, and a large fraction of the noncoding regions in the gene-sparse genomes is populated by repetitive sequences, most of which have been identi ed as transposable elements [11]. ...
The extreme genome reduction and physiological simplicity of some microsporidia has been attributed to their intracellular, obligate parasitic lifestyle. Although not all microsporidian genomes are small (size range from about 2 to 50 MB), it is suggested that the size of their genomes has been streamlined by natural selection. We explore the hypothesis that vertical transmission in microsporidia produces population bottlenecks, and thus reduces the effectiveness of natural selection. Here we compare the transposable element (TE) content of 47 microsporidian genomes, and show that genome size is positively correlated with the amount of TEs, and that species that experience vertical transmission have larger genomes with higher proportion of TEs. Our findings are consistent with earlier studies inferring that nonadaptive processes play an important role in microsporidian evolution.
... In a few species with well-characterized life cycles, abortive meiosis is observed (Canning et al. 1999), and population genetic studies suggest that some microsporidia are clonal (Haag, Traunecker, et al. 2013). Daphnia magna is the host of a diversity of microsporidia with divergent life-styles and genomic features (Ebert 2005;Corradi et al. 2009;Haag et al. 2014;Pombert et al. 2015) offering the unique opportunity to investigate the influence of microsporidian life history strategies on genome evolution while keeping the host factor constant. Here, to investigate the impact of transmission modes on the evolution of genomic architectures of microsporidia, we sequenced seven genomes from two clades of microsporidia that specifically parasitize D. magna with contrasting life histories: Hamiltosporidium and Ordospora. ...
Microsporidia have the leanest genomes among eukaryotes, and their physiological and genomic simplicity has been attributed to their intracellular, obligate parasitic lifestyle. However, not all microsporidia genomes are small or lean, with the largest dwarfing the smallest ones by at least an order of magnitude. To better understand the evolutionary mechanisms behind this genomic diversification, we explore here two clades of microsporidia with distinct life histories, Ordospora and Hamiltosporidium, parasitizing the same host species, Daphnia magna. Based on seven newly assembled genomes, we show that mixed-mode transmission (the combination of horizontal and vertical transmission), which occurs in Hamiltosporidium, is found to be associated with larger and AT-biased genomes, more genes and longer intergenic regions, as compared to the exclusively horizontally transmitted Ordospora. Furthermore, the Hamiltosporidium genome assemblies contain a variety of repetitive elements and long segmental duplications. We show that there is an excess of non-synonymous substitutions in the microsporidia with mixed-mode transmission, which cannot be solely attributed to the lack of recombination, suggesting that bursts of genome size in these microsporidia result primarily from genetic drift. Overall, these findings suggest that the switch from a horizontal-only to a mixed mode of transmission likely produces population bottlenecks in Hamiltosporidium species, therefore reducing the effectiveness of natural selection, and allowing their genomic features to be largely shaped by nonadaptive processes.
... This metapopulation has been the subject of biannual censuses for 33 years, providing data on population age, population extinction, and recolonization events (Pajunen & Pajunen, 2003), as well as on the presence and absence of different parasite species (since 2009). The microsporidian parasite Hamiltosporidium tvaerminnensis (previously Octosporea bayerii; Corradi, Haag, Pombert, Ebert, & Keeling, 2009;Haag et al., 2011) is the most prevalent parasite in the Finnish D. magna metapopulation, infecting about half of all populations. H. tvaerminnensis transmits horizontally from dead individuals, as well as vertically from mother to parthenogenetic and sexual host offspring; therefore, the parasite reaches prevalence as high as 100% within a population by the end of the season (Lass & Ebert, 2006). ...
Parasite‐mediated selection varying across time and space in metapopulations is expected to result in host local adaptation and the maintenance of genetic diversity in disease‐related traits. However, non‐adaptive processes like migration and extinction‐(re)colonization dynamics might interfere with adaptive evolution. Understanding how adaptive and non‐adaptive processes interact to shape genetic variability in life‐history and disease‐related traits can provide important insights into their evolution in subdivided populations. Here we investigate signatures of spatially fluctuating, parasite‐mediated selection in a natural metapopulation of Daphnia magna. Host genotypes from infected and uninfected populations were genotyped at microsatellite markers, and phenotyped for life‐history and disease traits in common garden experiments. Combining phenotypic and genotypic data a QST‐FST‐like analysis was conducted to test for signatures of parasite mediated selection. We observed high variation within and among populations for phenotypic traits, but neither an indication of host local adaptation nor a cost of resistance. Infected populations have a higher gene diversity (Hs) than uninfected populations and Hs is strongly positively correlated with fitness. These results suggest a strong parasite effect on reducing population level inbreeding. We discuss how stochastic processes related to frequent extinction‐(re)colonization dynamics as well as host and parasite migration impede the evolution of resistance in the infected populations. We suggest that the genetic and phenotypic patterns of variation are a product of dynamic changes in the host gene pool caused by the interaction of colonization bottlenecks, inbreeding, immigration, hybrid vigor, rare host genotype advantage and parasitism. Our study highlights the effect of the parasite in ameliorating the negative fitness consequences caused by the high drift load in this metapopulation.
