Patterns of Genome Evolution among the Microsporidian Parasites Encephalitozoon cuniculi, Antonospora locustae and Enterocytozoon bieneusi

Antonospora locustae and Enterocytozoon bieneusi. PLoS ONE 2(12): e1277. doi:10.1371/journal.pone.0001277 Patterns of Genome Evolution among the Microsporidian Parasites Encephalitozoon cuniculi , Antonospora locustae and Enterocytozoon bieneusi Nicolas Corradi 0 1 2 Donna E. Akiyoshi 0 1 2 Hilary G. Morrison 0 1 2 Xiaochuan Feng 0 1 2 Louis M. Weiss 0 1 2 Saul Tzipori 0 1 2 Patrick J. Keeling 0 1 2 0 Funding: The Enterocytozoon bieneusi genome sequence survey was supported by National Institutes of Health grants R21 AI52792 and R21 AI064118 and analysis was supported by a grant from the Canadian Institutes for Heath Research (MOP-84265). We acknowledge the Josephine Bay Paul Center for Comparative Molecular Biology and Evolution for the use of data included in the Antonospora locustae Genome Project funded by NSF award number 0135272. NC is supported by a fellowship from the Swiss National Science Foundation (PBLAA-114238). PJK is a fellow of the Canadian Institute for Advanced Research and the Michael Smith Foundation for Health Research. None of these institutions played a role in the design and conduct of the study, in the collection, analysis and interpretation of the data and in the preparation, review or approval of this manuscript 1 Academic Editor: Geraldine Butler, University College Dublin , Ireland 2 1 Department of Botany, Canadian Institute for Advanced Research, University of British Columbia , Vancouver, British Columbia , Canada , 2 Division of Infectious Diseases, Tufts Cummings School of Veterinary Medicine, North Grafton, Massachusetts, United States of America, 3 Marine Biological Laboratory, Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Woods Hole, Massachusetts, United States of America, 4 Department of Medicine, Albert Einstein College of Medicine , Bronx, New York , United States of America Background. Microsporidia are intracellular parasites that are highly-derived relatives of fungi. They have compacted genomes and, despite a high rate of sequence evolution, distantly related species can share high levels of gene order conservation. To date, only two species have been analysed in detail, and data from one of these largely consists of short genomic fragments. It is therefore difficult to determine how conservation has been maintained through microsporidian evolution, and impossible to identify whether certain regions are more prone to genomic stasis. Principal Findings. Here, we analyse three large fragments of the Enterocytozoon bieneusi genome (in total 429 kbp), a species of medical significance. A total of 296 ORFs were identified, annotated and their context compared with Encephalitozoon cuniculi and Antonospora locustae. Overall, a high degree of conservation was found between all three species, and interestingly the level of conservation was similar in all three pairwise comparisons, despite the fact that A. locustae is more distantly related to E. cuniculi and E. bieneusi than either are to each other. Conclusions/Significance. Any two genes that are found together in any pair of genomes are more likely to be conserved in the third genome as well, suggesting that a core of genes tends to be conserved across the entire group. The mechanisms of rearrangments identified among microsporidian genomes were consistent with a very slow evolution of their architecture, as opposed to the very rapid sequence evolution reported for these parasites. - INTRODUCTION Microsporidia are a diverse group of intracellular eukaryotic parasites including 1,300 described species [1], over a dozen of which are known to infect humans [2]. These organisms were once regarded as primitively simple eukaryotes, however it is now widely acknowledged that they are extremely specialized, highly derived relatives of fungi [36]. Microsporidia are known to harbour very small genomes, the most extreme being the 2.3 Mbp genome of Encephalitozoon intestinalis [7]. Microsporidian genomes have shrunk in two different ways. First, their obligate intracellular parasitic lifestyle has permitted the loss of many genes whose functions can be provided by the host cell, so that that the number of genes is severely reduced, in the case of the complete genome of E. cuniculi to about 2,000 genes [8,9]. Second, those genes that remain have been packed into a smaller space by a reduction in the overall size of genes (due to a paucity of introns and slightly smaller proteins) and by a significant reduction in intergenic spaces [8,10]. A survey of genomic sequences from Antonospora locustae, a microsporidian that is distantly related to E. cuniculi, suggested that this compaction has further effects on the evolution of microsporidian genomes. Specifically, this survey showed that the order of genes in the A. locustae and E. cuniculi genomes share a high degree of conservation, and that this conservation was correlated with short intergenic spaces [10]. Conservation of gene order usually degrade (...truncated)