Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi

By M. Katinka, S. Duprat, E. Cornillot, G. Méténier, Fabienne Thomarat, G. Prensier, V. Barbe, E. Peyretaillade, P. Brottier, P. Wincker and 7 more. Nature, 2001

1,038 citations recorded by the source corpus.

Microsporidia are obligate intracellular parasites infesting many animal groups. Lacking mitochondria and peroxysomes, these unicellular eukaryotes were first considered a deeply branching protist lineage that diverged before the endosymbiotic event that led to mitochondria. The discovery of a gene for a mitochondrial-type chaperone combined with molecular phylogenetic data later implied that microsporidia are atypical fungi that lost mitochondria during evolution. Here we report the DNA sequences of the 11 chromosomes of the ∼2.9-megabase (Mb) genome of Encephalitozoon cuniculi (1,997 potential protein-coding genes). Genome compaction is reflected by reduced intergenic spacers and by the shortness of most putative proteins relative to their eukaryote orthologues. The strong host dependence is illustrated by the lack of genes for some biosynthetic pathways and for the tricarboxylic acid cycle. Phylogenetic analysis lends substantial credit to the fungal affiliation of microsporidia. Because the E. cuniculi genome contains genes related to some mitochondrial functions (for example, Fe–S cluster assembly), we hypothesize that microsporidia have retained a mitochondrion-derived organelle.

Subfields: Animal Science and Zoology, Ecology, Evolution, Behavior and Systematics, Parasitology

View Paper: https://www.semanticscholar.org/paper/031d9e43ca8865aca7fa7223925c942d2c1783d7

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Citations in the corpus

Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. (2003, background): “…parasites (primarily of animals) once thought to be basal, primitively amitochondrial eukaryotes, are now known to be highly degenerate and reduced fungi, possessing a relict of a mitochondrion of uncertain function (see Katinka et al., 2001; Williams et al., 2002 and references therein).”
Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. (2004, background): “…hypothesized to be nested within the Fungi, possibly related to Zygomycota (Keeling, 2003), and have undergone extreme nuclear genome reduction (Katinka et al., 2001) and degeneration of the mitochondrion to a remnant genome-lacking organelle called the ‘‘mitosome’’ (Williams et al., 2002).”
Congruent evidence from α-tubulin and β-tubulin gene phylogenies for a zygomycete origin of microsporidia (2003, neutral): “…as the complete sequence of the E. cuniculi genome contains a number of genes (e.g., TF IIB, V-ATPase-A, Ser-tRNA synthetase, and Glu-tRNA synthetase), previously uncharacterised from microsporidia, that also retain a very strong phylogenetic signal of their fungal origin (Katinka et al., 2001).”
Stress-induced transposition of Tn4652 in Pseudomonas putida (2006, background): “Since their discovery by Barbara McClintock in the 1940s (reviewed in Jones, 2005), the TEs have been found in almost all organisms examined to date (exceptional are some specialised intracellular parasites with highly degenerate genomes) (Katinka et al., 2001; Moran and Plague, 2004).”
Introns in gene evolution. (2003, background): “9 megabase and whose genome compaction is reflected by reduced intergenic spacers and by the shortness of most proteins (Katinka et al., 2001).”
Insect-Fungal Associations: Ecology and Evolution (2005, methodology): “, insertions in enolase and EF-1a sequences, presence of chitin and trehalose) unite microsporidia with animals and fungi, but not specifically with fungi (Van der Meer and Gochnauer 1971; Undeen et al. 1987; Kamaishi et al. 1996a; Katinka et al. 2001).”
The COG database: an updated version includes eukaryotes (2003, methodology): “Given the dramatic genome reduction seen in the microsporidium [38], it is not unexpected that the query retrieves only a small set of 13 COGs.”
On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. (2003, background): “But the microsporidia are in fact highly derived fungi (Keeling 2001), as revealed by genome sequencing (Katinka et al. 2001), and the seemingly deep position of their rRNA sequence is a phylogenetic artefact.”
Microsporidia: a journey through radical taxonomical revisions (2009, background): “Finally, the publication of the first microsporidian genome (Katinka et al., 2001) also provided a wealth of data in favor of a fungal relationship.”
Hydrogenosomes and Mitosomes: Conservation and Evolution of Functions (2009, background): “The discovery of this organelle was pre-empted by the team that an- notated the Encephalitozoon cuniculi genome (Katinka et al. 2001), they discovered several further genes normally encoding mitochondrial proteins.”