Extremely Reduced Levels of Heterozygosity in the Vertebrate Pathogen Encephalitozoon cuniculi

Abstract

The genomes of microsporidia in the genus Encephalitozoon have been extensively studied for their minimalistic features, but they have seldom been used to investigate basic characteristics of the biology of these organisms, such as their ploidy or their mode of reproduction. In the present study, we aimed to tackle this issue by mapping Illumina sequence reads against the genomes of four strains of E. cuniculi. This approach, combined with more conventional molecular biology techniques, resulted in the identification of heterozygosity in all strains investigated, a typical signature of a diploid nuclear state. In sharp contrast with similar studies recently performed on a distant microsporidian lineage (Nematocida spp.), the level of heterozygosity that we identified across the E. cuniculi genomes was found to be extremely low. This reductive intraindividual genetic variation could result from the long-term propagation of these strains under laboratory conditions, but we propose that it could also reflect an intrinsic capacity of these vertebrate pathogens to self-reproduce.

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

“…Overall, these analyses demonstrate that genetic homogeneity is high and common in isolates of Encephalitoon cuniculi and related species, and confirms that nuclei in this lineage, referred to as monokaryons (Didier et al, 1991), are genetically very homogeneous, and possibly diploid like all mononucleate microsporidian species with sequenced genomes (Cuomo et al, 2012;Selman et al, 2013;Desjardins et al, 2015;Watson et al, 2015). An alternative explanation for the existence of a conserved 50/50 SNP would assume a balanced mixture of equally frequent homozygous genotypes in several independent mixed infections (and strains), a situation that sounds improbable.…”

“…In total, these procedures retrieved a total of 23 putative heterozygous SNPs in ECIII-L, a number almost identical to those previously reported from laboratory isolates (see Figure 1, Table 2; Selman et al, 2013). As for other isolates, the location of all SNP is unique to ECIII-L and does not appear to affect particular pathways, and the level and nature of intragenomic diversity of EcIII-L is virtually identical to that of lab strains.…”

“…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. diplokaryons-that is,the stage that triggers meiosis and formation of unikaryons in this genus (Pelin et al, 2015).…”

“…Homologs of genes involved in conserved biochemical pathways are few in microsporidia compared with other eukaryotes; a feature that highlights their dependence on host cells for metabolic supplies . Finally, most genome studies of species with mononucleated spores have revealed evidence of diploidy in microsporidia (Katinka et al, 2001;Cuomo et al, 2012;Selman et al, 2013;Desjardins et al, 2015;Watson et al, 2015), although recent analyses of diplokaryotic species have suggested that polyploidy can also occur in this group (Pelin et al, 2015).…”

Frequent Occurrence of Mixed Enterocytozoon bieneusi Infections in Humans

“…Many of the isolates that we genotyped contain more than two genotypes; duplication events by themselves, however, cannot explain the observed microsatellite diversity. The ploidy of E. bieneusi has not been determined, but evidence of diploidy in the taxonomically related microsporidian Encephalitozoon cuniculi has been reported (26). As for chromosomal rearrangements, diploidy cannot explain our results, leaving mixed populations as a plausible explanation of microsatellite heterogeneity.…”