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Open Access Highly Accessed Research article

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

Guoqing Pan1, Jinshan Xu23, Tian Li1, Qingyou Xia1, Shao-Lun Liu3, Guojie Zhang4, Songgang Li4, Chunfeng Li1, Handeng Liu1, Liu Yang1, Tie Liu1, Xi Zhang2, Zhengli Wu1, Wei Fan4, Xiaoqun Dang1, Heng Xiang1, Meilin Tao1, Yanhong Li1, Junhua Hu1, Zhi Li12, Lipeng Lin1, Jie Luo1, Lina Geng1, LinLing Wang2, Mengxian Long1, Yongji Wan1, Ningjia He1, Ze Zhang1, Cheng Lu1, Patrick J Keeling3, Jun Wang4, Zhonghuai Xiang1 and Zeyang Zhou12*

Author Affiliations

1 State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing, 400715, China

2 College of Life Sciences, Chongqing Normal University, Chongqing, 400047, China

3 Department of Botany, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada

4 Beijing Genomics Institute at Shenzhen, Shenzhen, 518000, China

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BMC Genomics 2013, 14:186  doi:10.1186/1471-2164-14-186

Published: 16 March 2013

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.

Keywords:
Gene duplication; Horizontal gene transfer; Host-derived transposable element; Host adaptation; Microsporidian; Silkworms