Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation

Abstract

BackgroundMicrosporidian Nosema bombycis has received much attention because the pébrine disease of domesticated silkworms results in great economic losses in the silkworm industry. So far, no effective treatment could be found for pébrine. Compared to other known Nosema parasites, N. bombycis can unusually parasitize a broad range of hosts. To gain some insights into the underlying genetic mechanism of pathological ability and host range expansion in this parasite, a comparative genomic approach is conducted. The genome of two Nosema parasites, N. bombycis and N. antheraeae (an obligatory parasite to undomesticated silkworms Antheraea pernyi), were sequenced and compared with their distantly related species, N. ceranae (an obligatory parasite to honey bees).ResultsOur comparative genomics analysis show that the N. bombycis genome has greatly expanded due to the following three molecular mechanisms: 1) the proliferation of host-derived transposable elements, 2) the acquisition of many horizontally transferred genes from bacteria, and 3) the production of abundnant gene duplications. To our knowledge, duplicated genes derived not only from small-scale events (e.g., tandem duplications) but also from large-scale events (e.g., segmental duplications) have never been seen so abundant in any reported microsporidia genomes. Our relative dating analysis further indicated that these duplication events have arisen recently over very short evolutionary time. Furthermore, several duplicated genes involving in the cytotoxic metabolic pathway were found to undergo positive selection, suggestive of the role of duplicated genes on the adaptive evolution of pathogenic ability.ConclusionsGenome expansion is rarely considered as the evolutionary outcome acting on those highly reduced and compact parasitic microsporidian genomes. This study, for the first time, demonstrates that the parasitic genomes can expand, instead of shrink, through several common molecular mechanisms such as gene duplication, horizontal gene transfer, and transposable element expansion. We also showed that the duplicated genes can serve as raw materials for evolutionary innovations possibly contributing to the increase of pathologenic ability. Based on our research, we propose that duplicated genes of N. bombycis should be treated as primary targets for treatment designs against pébrine.

Interaction and Assembly of Two Novel Proteins in the Spore Wall of the Microsporidian Species Nosema bombycis and Their Roles in Adherence to and Infection of Host Cells

“…Recently, phylogenetic analyses based on conserved proteins (3)(4)(5), ribosomal DNA (rDNA) sequences (6,7), and complete sequencing of the Encephalitozoon cuniculi genome (8) have suggested that microsporidia, which undergo a highly reductive evolution, are closely related to fungi (9). However, the N. bombycis genome has greatly expanded due to transposable elements and gene duplications (10).…”

Exploiting the architecture and the features of the microsporidian genomes to investigate diversity and impact of these parasites on ecosystems

“…In any case, the differences in TE content between N. bombycis and the other Nosema species are substantial and correlated with genome size variations, a trend also observed between Nematocida species (Cuomo et al, 2012). The unusually large expansion in N. bombycis has been attributed to the propagation of TEs, to the acquisition of genes by horizontal transfer and to largescale and small-scale gene duplication events (Pan et al, 2013). All of these species feature LTR retrotransposons but differ in non-LTR retrotransposon, DNA transposon and helitron contents (Figure 3b; Peyretaillade et al, 2012;Chen et al, 2013;Pan et al, 2013)).…”

“…Genome sequencing has also revealed a variable proportion of duplicate genes from different species (Nassonova et al, 2005;Akiyoshi et al, 2009;Pan et al, 2013). Nevertheless, in some cases, such gene duplication may in fact be related to polyploidy of the microsporidian genome as suggested for N. ceranae and A. algerae Roudel et al, 2013) In microsporidian genomes, transcriptional and translational regulation signals are highly conserved.…”

“…Only a few TEs were initially reported in N. apis (Chen et al, 2013) whereas the genomes of N. ceranae, N. antheraeae and N. bombycis were shown to display around 1%, 6% and 20% of TEs, respectively (Pan et al, 2013). However, BLASTP (Altschul et al, 1997) and TransposonPSI (http://transposonpsi.sourceforge.net/) analyses allowed us to determine that many TEs were wrongly annotated as host genes in the four species (unpublished data), such that the real TE content is higher in these genomes and, respectively, closer to 2%, 7%, 10% and 25% in N. apis, N. ceranae, N. antheraeae and N. bombycis.…”

“…The unusually large expansion in N. bombycis has been attributed to the propagation of TEs, to the acquisition of genes by horizontal transfer and to largescale and small-scale gene duplication events (Pan et al, 2013). All of these species feature LTR retrotransposons but differ in non-LTR retrotransposon, DNA transposon and helitron contents (Figure 3b; Peyretaillade et al, 2012;Chen et al, 2013;Pan et al, 2013)). For example, N apis lacks Merlin and Mariner DNA transposon families whereas N. ceranae lacks piggyBac DNA transposons.…”