The Ordospora colligata Genome: Evolution of Extreme Reduction in Microsporidia and Host-To-Parasite Horizontal Gene Transfer

Abstract

Microsporidia are a group of obligate intracellular parasites that are best known for their unique infection mechanism and their unparalleled levels of genomic reduction and compaction. We sequenced the genome of Ordospora colligata, a gut parasite of the microcrustacean Daphnia sp. and the closest known relative to the microsporidia characterized by the most extreme genomic reduction, the model genus Encephalitozoon. We found that the O. colligata genome is as compact as those of Encephalitozoon spp., featuring few introns and a similar complement of about 2,000 genes, altogether showing that the extreme reduction took place before the origin of Encephalitozoon spp. and their adaptation to vertebrate hosts. We also found that the O. colligata genome has acquired by horizontal transfer from its animal host a septin that is structurally analogous to septin 7, a protein that plays a major role in the endocytosis-based invasion mechanism of the fungal pathogen Candida albicans. Microsporidian invasion is most often characterized by injection through a projectile tube, but microsporidia are also known to invade cells by inducing endocytosis. Given the function of septins in other systems, we hypothesize that the acquired septin could help O. colligata induce its uptake by mimicking host receptors.Importance The smallest known eukaryotic genomes are found in members of the Encephalitozoon genus of microsporidian parasites. Their extreme compaction, however, is not characteristic of the group, whose genomes can differ by an order of magnitude. The processes and evolutionary forces that led the Encephalitozoon genomes to shed so much of their ancestral baggage are unclear. We sequenced the genome of Ordospora colligata, a parasite of the water flea Daphnia sp. and the closest known relative of Encephalitozoon species, and show that this extreme reduction predated the split between the two lineages. We also found that O. colligata has acquired a septin gene by host-to-parasite horizontal transfer and predicted that the encoded protein folds like a septin 7, which plays a major role in endocytosis. We hypothesize that this acquisition could help O. colligata parasitize its hosts by facilitating endocytic infection, a mechanism that occurs in microsporidia but that is not yet well understood.

Error-prone protein synthesis in parasites with the smallest eukaryotic genome

“…To compare microsporidian synthetases with their homologs from other eukaryotes, we analyzed available genome sequences from 19 microsporidian species (SI Appendix, Table S1). Each of these genomes was shown to harbor a full set of 20 different aminoacyl-tRNA synthetases corresponding to the 20 proteinogenic amino acids, but to lack the genes coding for mitochondrial aminoacyl-tRNA synthetases due to degeneration of mitochondria in microsporidian cells (9,16,(22)(23)(24)(25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36). Moreover, microsporidian genomes lack duplicated synthetase genes or genes coding for synthetase fragments that are present in other eukaryotes (9,16,(23)(24)(25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38).…”

Not So Simple After All: Bacteria, Their Population Genetics, and Recombination

“…Together with other putative cases of transfer from hosts to infecting species (Pombert et al 2015), and a suggestion that more than 100 human genes may have originated in other species (Crisp et al 2015), it seems that horizontal transfer is not just for bacteria. However, a cautionary note is important, as we can produce a signal that looks like horizontal transfer by multiple means, including, but not limited to, restricted sampling of phylogenetic diversity combined with the loss of the gene from some taxa.…”

No genome is an island: toward a 21st century agenda for evolution

“…There is also evidence for reverse horizontal transfers from host genomes to the Microsporidia endosymbionts . These include DNA encoding purine and folate metabolism functions as well as septin, a protein involved in endocytosis transferred from the genome of the water flea Daphnia magna to its gut parasite, Ordospora colligate . The horizontally acquired septin appears to play a role in establishing new infections by endocytosis of Ordospora spores.…”

“…53 These include DNA encoding purine and folate metabolism functions as well as septin, a protein involved in endocytosis transferred from the genome of the water flea Daphnia magna to its gut parasite, Ordospora colligate. 54 The horizontally acquired septin appears to play a role in establishing new infections by endocytosis of Ordospora spores. In addition to metabolic and cell functions, there has also been extensive horizontal transfer of mobile DNA elements (DNA transposons) from hosts to Microsporidia parasites, which can then transfer them further to other animal hosts.…”