Sex and the Microsporidia

Lee, Soo Chan; Heitman, Joseph; Ironside, Joseph E.

doi:10.1002/9781118395264.ch8

Cited by 14 publications

(11 citation statements)

References 89 publications

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“…TE proliferation is also linked with the existence of sexual reproduction (Arkhipova and Meselson ; Lee et al. ; Wright and Finnegan ), a notion that is supported by the presence of diploidy and MRGs in P. neurophilia .…”

Section: Resultsmentioning

confidence: 97%

Genome Analysis of Pseudoloma neurophilia: A Microsporidian Parasite of Zebrafish (Danio rerio)

Ndikumana

Pelin

Williot

et al. 2016

J Eukaryotic Microbiology

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Microsporidia are highly successful parasites that infect virtually all known animal lineages, including the model Danio rerio (zebrafish). The widespread use of this aquatic model for biomedical research has resulted in an unexpected increase in infections from the microsporidium Pseudoloma neurophilia, which can lead to significant physical, behavioral and immunological modifications resulting in non-protocol variation during experimental procedures. Here, we seek to obtain insights into the biology of P. neurophilia by investigating its genome content, which was obtained from only 29 nanograms of DNA using the Miseq technology and paired-end Illumina sequencing. We found that the genome of P. neurophilia is phylogenetically and genetically related to other fish-microsporidians, but features unique to this intracellular parasite are also found. The small 5.25-Mb genome assembly includes 1,139 unique open reading frames and an unusually high number of transposable elements for such a small genome. Investigations of intragenomic diversity also provided strong indications that the mononucleate nucleus of this species is diploid. Overall, our study provides insights into the dynamics of microsporidian genomes, and represents a solid sequence reference to be used in future studies of host-parasite interactions using the zebrafish Danio rerio and P. neurophilia as a model.

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Section: Resultsmentioning

confidence: 97%

Genome Analysis of Pseudoloma neurophilia: A Microsporidian Parasite of Zebrafish (Danio rerio)

Ndikumana

Pelin

Williot

et al. 2016

J Eukaryotic Microbiology

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“…Indications of this process also come from evidence of recombination in the populations of several species in the group (29,36,51,74). Recent investigations (N. Corradi, unpublished findings) have discovered strains of E. cuniculi harboring pseudogenized versions of Spo11, a protein central to meiosis, and homologs of the corresponding gene are also absent in available genome data from E. bieneusi (55). This suggests that some microsporidians are completely clonal.…”

Section: Sex and The Microsporidiamentioning

confidence: 99%

Microsporidia: Eukaryotic Intracellular Parasites Shaped by Gene Loss and Horizontal Gene Transfers

Corradi

2015

Annu. Rev. Microbiol.

120

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Microsporidia are eukaryotic parasites of many animals that appear to have adapted to an obligate intracellular lifestyle by modifying the morphology and content of their cells. Living inside other cells, they have lost many, or all, metabolic functions, resulting in genomes that are always gene poor and often very small. The minute content of microsporidian genomes led many to assume that these parasites are biochemically static and uninteresting. However, recent studies have demonstrated that these organisms can be surprisingly complex and dynamic. In this review I detail the most significant recent advances in microsporidian genomics and discuss how these have affected our understanding of many biological aspects of these peculiar eukaryotic intracellular pathogens.

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“…Selfing is one mechanism that produces homozygous genomes, but this process requires a meiotic machinery (that is, sex) that may be broken in EcIII-L. Indeed, all E. cuniculi strains harbors complete sequences of most meiosisspecific genes (Lee et al, 2008(Lee et al, , 2014, but EcIII-L harbors a frameshift mutation that cannot fully restore meiosis in a model fungus. A priori, this suggests that ECIII-L (and to certain extent, also other species that potentially lack portions of Spo11, such as the Mitosporidium daphnia, Rozella allomycis and Nosema bombycis, Figure 5) may not be capable of sexual reproduction and that genome homogenization in this strain (and possibly all strains) must be driven by asexual mechanisms.…”

Section: What Drives Genome Homogenization In Encephalitozoon?mentioning

confidence: 99%

“…Perhaps, these must first fuse and form tetraploid diplokaryons (Bernander et al, 2001;Lee et al, 2014) to trigger meiosis and create genetic diversity? This hypothesis is supported by evidence of diploidy in mononucleate species (Katinka et al, 2001;Cuomo et al, 2012;Selman et al, 2013;Desjardins et al, 2015;Watson et al, 2015) and tetraploidy in Nosema spp.…”

Section: What Drives Genome Homogenization In Encephalitozoon?mentioning

confidence: 99%

“…In particular, their inspection could reveal if low genetic diversity is the norm in this species. Assuming that a conventional microsporidian sexual cycle exist in E. cuniculi (Lee et al, 2014), the presence of a highly heterozygous (assuming diploidy) or genetically diverse population of spores in natural strains could indicate that E. cuniculi strains occasionally outcross in the field . Genome sequence data from new natural strains are also a requisite to identify the extent and nature of genetic diversity that exist in field samples of these vertebrate parasites.…”

Section: Introductionmentioning

confidence: 99%

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The genome of an Encephalitozoon cuniculi type III strain reveals insights into the genetic diversity and mode of reproduction of a ubiquitous vertebrate pathogen

Pelin

Moteshareie

et al. 2016

Heredity

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Encephalitozoon cuniculi is a model microsporidian species with a mononucleate nucleus and a genome that has been extensively studied. To date, analyses of genome diversity have revealed the existence of four genotypes in E. cuniculi (EcI, II, III and IV). Genome sequences are available for EcI, II and III, and are all very divergent, possibly diploid and genetically homogeneous. The mechanisms that cause low genetic diversity in E. cuniculi (for example, selfing, inbreeding or a combination of both), as well as the degree of genetic variation in their natural populations, have been hard to assess because genome data have been so far gathered from laboratory-propagated strains. In this study, we aim to tackle this issue by analyzing the complete genome sequence of a natural strain of E. cuniculi isolated in 2013 from a steppe lemming. The strain belongs to the EcIII genotype and has been designated EcIII-L. The EcIII-L genome sequence harbors genomic features intermediate to known genomes of II and III lab strains, and we provide primers that differentiate the three E. cuniculi genotypes using a single PCR. Surprisingly, the EcIII-L genome is also highly homogeneous, harbors signatures of heterozygosity and also one strain-specific single-nucleotide polymorphism (SNP) that introduces a stop codon in a key meiosis gene, Spo11. Functional analyses using a heterologous system demonstrate that this SNP leads to a deficient meiosis in a model fungus. This indicates that EcIII-L meiotic machinery may be presently broken. Overall, our findings reveal previously unsuspected genome diversity in E. cuniculi, some of which appears to affect genes of primary importance for the biology of this pathogen.

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Sex and the Microsporidia

Cited by 14 publications

References 89 publications

Genome Analysis of Pseudoloma neurophilia: A Microsporidian Parasite of Zebrafish (Danio rerio)

Genome Analysis of Pseudoloma neurophilia: A Microsporidian Parasite of Zebrafish (Danio rerio)

Microsporidia: Eukaryotic Intracellular Parasites Shaped by Gene Loss and Horizontal Gene Transfers

The genome of an Encephalitozoon cuniculi type III strain reveals insights into the genetic diversity and mode of reproduction of a ubiquitous vertebrate pathogen

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