Bacterial Catalase in the Microsporidian Nosema locustae : Implications for Microsporidian Metabolism and Genome Evolution

Abstract

Microsporidia constitute a group of extremely specialized intracellular parasites that infect virtually all animals. They are highly derived, reduced fungi that lack several features typical of other eukaryotes, including canonical mitochondria, flagella, and peroxisomes. Consistent with the absence of peroxisomes in microsporidia, the recently completed genome of the microsporidian Encephalitozoon cuniculi lacks a gene for catalase, the major enzymatic marker for the organelle. We show, however, that the genome of the microsporidian Nosema locustae, in contrast to that of E. cuniculi, encodes a group II large-subunit catalase. Surprisingly, phylogenetic analyses indicate that the N. locustae catalase is not specifically related to fungal homologs, as one would expect, but is instead closely related to proteobacterial sequences. This finding indicates that the N. locustae catalase is derived by lateral gene transfer from a bacterium. The catalase gene is adjacent to a large region of the genome that appears to be far less compact than is typical of microsporidian genomes, a characteristic which may make this region more amenable to the insertion of foreign genes. The N. locustae catalase gene is expressed in spores, and the protein is detectable by Western blotting. This type of catalase is a particularly robust enzyme that has been shown to function in dormant cells, indicating that the N. locustae catalase may play some functional role in the spore. There is no evidence that the N. locustae catalase functions in a cryptic peroxisome.

Simplicity and Complexity of Microsporidian Genomes

“…In the extremely compacted genomes of microsporidia, however, it is possible that what is a minor force in "normal" genomes takes on a more substantial role, resulting in the greater degree of stability apparent between these two distantly related species. The absences of repetitive and mobile DNA in the genome further enhance this effect, although evidence for some repetitive DNA exists in A. locustae (14), and retroelements exist in V. corneae (39) and Spraguea lophii (22). If compaction has enhanced genome stability in microsporidia, then it has probably done so only at certain levels of organization.…”

“…However, these studies looked only at relatively short genomic fragments and did not provide clues to the influence of such elements in genome architecture. A. locustae (formerly Nosema locustae) (53, 54) is another microsporidian for which more-substantial genomic data have now been produced (13,14,51). A. locustae has been shown to be relatively distantly related to E. cuniculi (53,54); however, a random genome survey of 685 kbp showed that the two genomes have a good deal in common.…”

Comparative genomics of microsporidia

“…Alternatively, there may be large gene-poor regions of the genome that have not been sampled. The region around catalase (Fast et al 2003) could represent one such area since this 13,000 bp region only contains three genes (for a density of only 0.23 genes/Kbp -over four times lower than the average found in gene-rich areas). Lastly, it is also possible that most of the genome shares a high gene-density, but that more than one copy of some genes exist.…”

“…Catalase converts hydrogen peroxide to water and hydrogen gas, and is a marker enzyme for peroxisomes, although it is also found in many prokaryotes in eukaryotes outside of the organelle. A. locustae has been shown to encode a catalase of the non-peroxisomal, group II variety that is functional and expressed in spores (Fast et al 2003). The gene is likely not ancestral to microsporidia, since it is not of fungal ancestry, but is instead derived from a proteobacterium by lateral gene transfer.…”

Disease Ecology in the Face of Climate Change

“…The first cases of HGT in eukaryotes were associated with parasite evolution [21,22]. Whether through acquisition of antibiotic resistance, pathogenicity islands, or expanding to new metabolism [23] or host-specific environments [24], HGT is due in part to the fact that those genes that confer some evolutionary benefit are most likely to be found in other organisms already adapted to those circumstances [25]. [26] identified the source of the cholera outbreak in Haiti as a group of Nepalese peacekeeping troops.…”