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Comparative Study
. 2013 Mar 16;14:186.
doi: 10.1186/1471-2164-14-186.

Comparative Genomics of Parasitic Silkworm Microsporidia Reveal an Association Between Genome Expansion and Host Adaptation

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Free PMC article
Comparative Study

Comparative Genomics of Parasitic Silkworm Microsporidia Reveal an Association Between Genome Expansion and Host Adaptation

Guoqing Pan et al. BMC Genomics. .
Free PMC article

Abstract

Background: Microsporidian 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).

Results: Our 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.

Conclusions: Genome 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. The genome data and annotation information of N. bombycis and N.antheraeae were submitted to GenBank (Accession numbers ACJZ01000001 -ACJZ01003558).

Figures

Figure 1
Figure 1
Venn diagram showing the number of homologous genes and lineage-specific genes amongst three Nosema species, N. bombycis, N. antheraeae, and N. ceranae. The arabic numbers followed by characters represent the number of homologous genes in each Nosema species (‘a’ denotes N. antheraeae, ‘b’ denotes N. bombycis , and ‘c’ denotes N. ceranae). For instance, 2455b:1746a:1459c means that 2455 genes of N. bombycis, 1746 genes of N. antheraeae, and 1459 genes of N. ceranae are homologous to each other.
Figure 2
Figure 2
A maximum-likelihood phylogenetic tree of host-derived Piggybac transposase sequences. Arrows show the putative recent horizontal gene transfer (HGT) events of host-derived transposable elements. Several transposons are closely related to those from insects. Black boxes indicate elements from the two silkworm-infecting Nosema species, while white boxes indicate elements from the domesticated silkworm B. mori. Numbers in parentheses indicate the total copy numbers for each transposable element.
Figure 3
Figure 3
Horizontal gene transfers of protein-coding genes in N. bombycis. (A) Venn diagram showing the numbers of HGT genes between two different dataset that were identified using two different methods, the Darkhorse method and the phylogenetic method. The total number of the union of HGT genes between two dataset is 55. (B) The diagram showing the origination of those 55 HGT genes. All of them originated from prokaryotes.
Figure 4
Figure 4
Gene duplications and the dS distribution of paralogs and orthologs among three Nosema species. Abbreviation: Na, N. antheraeae; Nb, N. bombycis; Nc, N. ceranae. (A) A circos map showing the comparative genomics among three different Nosema species based on all available scaffolds. Each line represents the homologous syntenic regions between any two species or between any given two chromosome positions of single species. Many lines across different scaffolds of N. bombysis indicates higher rate of segmental syntenic duplications. (B) The dS distribution of segmental paralogs of Nb and the orthologs between Nb and Na showing a higher dS values in orthologs in general. Notably, a higher peak (arrow) seen in Nb suggests the possibility of a burst of paralogs recently over the Nb evolution after the separation of Na and Nb. (C) An example of syntenic comparisons among three Nosema species showing a cluster of tandem paralogs. The corresponding genetic position and names of identified element are provided in Additional file 8. The number of all identified tandem paralogs for each Nosema genome is summarized on the right side. (D) The dS distribution of tandem paralogs of Nb and orthologs between Na and Nb showing that majorities of tandem paralogs arose after the separation of Na and Nb because the dS values of those tandem paralogs are smaller than that of orthologs.
Figure 5
Figure 5
An example from the syntenic analysis showing that N. bombycis often consist of two homologous regions, instead of one such as N. antheraeae. When summarized the number of syntenic regions in both N. antheraeae and N. bombycis, the number of paralogous syntenic region of N. bombycis is often twice more than that of orthologous syntenic region between N. antheraeae and N. bombycis, indicating that large segmental duplication events have occurred over the evolution of N. bombycis.
Figure 6
Figure 6
A hypothetical model showing how the SPN protein of N. bombycis suppresses the serine protease cascade of the melanization pathway of the host B. mori. After the suppression of the serine protease cascade, the defensive response, the subsequent formation of melanization will be inhibited in the hosts. Abbreviation: PPO, prophenoloxidase; β-GRP, β-glucan recognition protein.

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