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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.

SUBMITTER: Quandt CA

PROVIDER: S-EPMC5701793 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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

Quandt C Alisha CA Beaudet Denis D Corsaro Daniele D Walochnik Julia J Michel Rolf R Corradi Nicolas N James Timothy Y TY

eLife 20171124

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 encode ...[more]

PMID: 29171834

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Project description: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.

Dataset Information

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

Publications

The genome of an intranuclear parasite, <i>Paramicrosporidium saccamoebae</i>, reveals alternative adaptations to obligate intracellular parasitism.

Similar Datasets

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