Comparative genomics

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The E. cuniculi genome surely represents many of the main characteristics of microsporidian genomes in general, but we must nonetheless remember that this is only one species of a group with vast diversity, and its genome ranks among the smallest and therefore perhaps most extreme. In addition, a single genome can say little about certain patterns of change over time, so there are many questions that will only become apparent with comparative genomics of microsporidia. In addition to the E. cuniculi genome, there are small sequence surveys from Vittaforma corineae (Mittleider et al. 2002) and Spraguea lophii (Hinkle et al. 1997), as well as a larger survey (Slamovits et al. 2004a) and an ongoing complete genome project ( = intro) from Antonospora locustae (formerly Nosema locustae (Slamovits et al. 2004b)). These are very likely just the beginning: a four-fold coverage survey is about to commence for Enterocytozoon beineusi and other smaller projects are underway for other species, so the coming years should see the generation of at least samples of genomes from a reasonable diversity of micro-sporidia. What can we expect from these data? In general we would predict that the metabolic and overall proteomic diversity will be much greater than previously imagined. Taking the mitochondrion as an example, the small A. locustae survey already revealed another two proteins in addition to those already characterized in E. cuniculi (Williams and Keeling 2005). Similarly, S. lophii was found to encode a reverse transcriptase (Hinkle et al. 1997), while E. cuniculi has no evidence of transposons (Katinka et al. 2001), and two interesting enzymes, catalase and photolyase, have been found in A. locustae but not E. cuniculi (Fast et al. 2003; Slamovits and Keeling 2004), and the former appears to have been acquired by lateral gene transfer from a bacterium (Fast et al. 2003). With good samples of many genomes, individual but nevertheless important cases like these should abound, and each has the potential to reveal additional functional diversity and therefore better inform our generalizations.

As far as the genome as a whole is concerned, comparisons between E. cuniculi and A. locustae have already revealed one surprising characteristic. Over time, the conservation of gene order is lost, mostly due to many short-range events and a few longer-range events which eventually randomize the genome. A. locustae and E. cuniculi are very distantly related species of microsporidia (Slamovits et al. 2004b), so it is surprising that they share a fairly high level of gene order conservation. Comparing 94 pairs of genes it was found that 13% of pairs were present in both genomes, while almost 26% of pairs were within five genes of one another (Slamovits et al. 2004a). It is impossible to quantify our expectations for gene order conservation without knowing how long ago two species diverged, which we cannot know for microsporidia, but if we compare this level of conservation with other fungi, the contrast is obvious. The closely related yeasts Saccharomyces cerevisiae and Candida albicans share only 9% of gene pairs and S. cerevisiae and the fission yeast

Schizosaccharomyces pombe share no gene order conservation. For the microsporidian genomes to be evolving at the same rate as these ascomycetes they would have to have evolved around the time that Saccharomyces and Candida diverged, which does not fit with the distribution or host range of microsporidia (Slamovits et al. 2004a). More likely, their genomes are evolving more slowly. It has been suggested that this is because compaction has reduced the number of potentially harmless breakpoints in the genome (Hurst et al. 2002; Slamovits et al. 2004a), which are needed to reorganize without ill effect. Indeed, there is a negative correlation between conservation of gene pairs and the length of their intergenic regions (Hurst et al. 2002; Slamovits et al. 2004a).

The conservation in genome order is potentially a general feature of compacted genomes, but no other comparison of such genomes is available as of yet, so it remains to be seen if other highly reduced genomes behave similarly. In the meantime, however, the conserved arrangement of microsporidian chromosomes has proved to be of use in detecting highly divergent genes. Using the map of the E. cuniculi genome, the two polar tube proteins from A. locustae were identified when the sequence conservation between these proteins was too low to allow detection by conventional means. Localization and biochemical analysis confirmed the identity of the two divergent sequences (Polonais et al. 2005), demonstrating one practical importance of comparative genomics.

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