The genome of an intranuclear parasite, Paramicrosporidium saccamoebae, reveals alternative adaptations to obligate intracellular parasitism

Abstract

Intracellular parasitism often results in gene loss, genome reduction, and dependence upon the host for cellular functioning. Rozellomycota is a clade comprising many such parasites and is related to the diverse, highly reduced, animal parasites, Microsporidia. We sequenced the nuclear and mitochondrial genomes of Paramicrosporidium saccamoebae [Rozellomycota], an intranuclear parasite of amoebae. A canonical fungal mitochondrial genome was recovered from P. saccamoebae that encodes genes necessary for the complete oxidative phosphorylation pathway including Complex I, differentiating it from most endoparasites including its sequenced relatives in Rozellomycota and Microsporidia. Comparative analysis revealed that P. saccamoebae shares more gene content with distantly related Fungi than with its closest relatives, suggesting that genome evolution in Rozellomycota and Microsporidia has been affected by repeated and independent gene losses, possibly as a result of variation in parasitic strategies (e.g. host and subcellular localization) or due to multiple transitions to parasitism.

Clarifying the Relationships between Microsporidia and Cryptomycota

“…), but the addition of nuclear and mitochondrial genomes of Paramicrosporidium saccamoebae (Quandt et al. ) have provided several intriguing new perspectives on microsporidian evolution. It is increasingly apparent that, although all SB‐microsporidia exhibit microsporidian‐defining morphological characters, their genomic evolution appears far more mosaic (Quandt et al.…”

“…It is increasingly apparent that, although all SB‐microsporidia exhibit microsporidian‐defining morphological characters, their genomic evolution appears far more mosaic (Quandt et al. ); Table . Rozella and LB‐Microsporidia both have horizontally acquired Rickettsia ‐like NTT ATP/ADP transporters, but metchnikovellids, Mitosporidium and Paramicrosporidium do not (Table ).…”

“…Based on the 49 flagellar toolkit proteins assembled for a previous study (Torruella et al. ), we searched by BLAST in available early‐branching microsporidian predicted protein sets from genomic data, in Mitosporidium daphniae (Haag et al ), Paramicrosporidium (Quandt et al ), and Amphiamblys sp. (Mikhailov et al.…”

“…; Quandt et al. ), has a mitochondrion, albeit lacking Complex I of the oxidative phosphorylation pathway. Paramicrosporidium has a canonical fungal mitochondrial genome, and shares more gene content with distantly related fungi than with its closest relatives (Quandt et al.…”

“…Paramicrosporidium has a canonical fungal mitochondrial genome, and shares more gene content with distantly related fungi than with its closest relatives (Quandt et al. ). Mitosporidium and Nucleophaga have possibly nonhomologous finger‐like extensions in naked intranuclear trophic stages similar to those of Rozella (Corsaro et al.…”