PLoS One. 2013 Dec 30;8(12):e84137.

Genome-wide transcriptional response of silkworm (Bombyx mori) to infection by the microsporidian Nosema bombycis

Zhengang Ma, Chunfeng Li, Guoqing Pan, Zhihong Li, Bing Han, Jinshan Xu, Xiqian Lan, Jie Chen, Donglin Yang, Quanmei Chen, Qi Sang, Xiaocun Ji, Tian Li, Mengxian Long, Zeyang Zhou.

The State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing, China; College of Life Sciences, Chongqing Normal University, Chongqing, China; Key Laboratory for Sericulture Functional Genomics and Biotechnology of Agricultural Ministry, Southwest University, Chongqing, China

 

Abstract

Microsporidia have attracted much attention because they infect a variety of species ranging from protists to mammals, including immunocompromised patients with AIDS or cancer. Aside from the study on Nosema ceranae, few works have focused on elucidating the mechanism in host response to microsporidia infection. Nosema bombycis is a pathogen of silkworm pébrine that causes great economic losses to the silkworm industry. Detailed understanding of the host (Bombyx mori) response to infection by N. bombycis is helpful for prevention of this disease. A genome-wide survey of the gene expression profile at 2, 4, 6 and 8 days post-infection by N. bombycis was performed and results showed that 64, 244, 1,328, 1,887 genes were induced, respectively. Up to 124 genes, which are involved in basal metabolism pathways, were modulated. Notably, B. mori genes that play a role in juvenile hormone synthesis and metabolism pathways were induced, suggesting that the host may accumulate JH as a response to infection. Interestingly, N. bombycis can inhibit the silkworm serine protease cascade melanization pathway in hemolymph, which may be due to the secretion of serpins in the microsporidia. N. bombycis also induced up-regulation of several cellular immune factors, in which CTL11 has been suggested to be involved in both spore recognition and immune signal transduction. Microarray and real-time PCR analysis indicated the activation of silkworm Toll and JAK/STAT pathways. The notable up-regulation of antimicrobial peptides, including gloverins, lebocins and moricins, strongly indicated that antimicrobial peptide defense mechanisms were triggered to resist the invasive microsporidia. An analysis of N. bombycis-specific response factors suggested their important roles in anti-microsporidia defense. Overall, this study primarily provides insight into the potential molecular mechanisms for the host-parasite interaction between B. mori and N. bombycis and may provide a foundation for further work on host-parasite interaction between insects and microsporidia.

PMID: 24386341

 

SUPPLEMENTARY

Although many studies of the infection mechanism of microsporidian have been reported, few studies have focused on elucidating the mechanism of the host response to microsporidia infection. Thus, investigation on the interplay of genome-wide expression profile of hosts and parasites is critical for understanding the mechanisms of self-protection, resistance and defense against invasive microsporidia. The study by Zhengang Ma et al. focused on elucidating the mechanism of the host response to microsporidia infection. This study revealed that a strong and complex host response is induced by N. bombycis infection, and it can provide a comprehensive transcriptional profile of the interaction between microsporidia and its host.

Zhengang Ma et al. challenged silkworm with N. bombycis isolate CQ1 and obtained the microarray data at 2, 4, 6 and 8 dpi. 23 K silkworm genome oligonucleotide chip (CapitalBio) was employed to perform further analysis. The schematic overview of the process for silkworm recognition and response to the invasion of N. bombycis was completed (Figure 1). The invasion of N. bombycis altered the expression of genes involved in JH biosynthesis and metabolism pathway, which could affect the physiological and development process of ecdysis and the metamorphosis of infected silkworm larvae. In addition, eight types of basal metabolism were significantly modulated after the infection of N. bombycis. The enhancement of the basal transcription level meets the requirements for the host silkworm and microsporidia. To combat proliferous microsporidia, silkworm activated complex immune responses as follows: 1) β-GRP2/4 participated in recognition of invasive N. bombycis and triggered Toll signaling pathway. Meanwhile, membrane receptor BmDome was up-regulated and induced the response of JAK/STAT pathway. 2) The effectors of systemic immunity, particularly the AMPs (gloverins, lebocins and moricins) showed up-regulation during the infectious progress. 3) Silkworm serine protease cascade melanization pathway was also induced, but a loss in effective melanization limited the pathogen clearance ability of the silkworm. The secreted serpins of the invasive N. bombycis may be involved in inhibiting the activity of silkworm serine proteases and then disturbed the formation of dopamine melanin. 4) Cellular immune effectors, such as lysozymes, immune-related proteins and immunoglobulins were also up-regulated to manage the microsporidia.

ZHOU FIG1

Figure 1. Schematic overview of the process for silkworm recognition and response to the invasion of N. bombycis.

In summation, the findings showed that N. bombycis infection increased the rate of basal metabolism and disturbed the synthesis and metabolism of silkworm JH. Moreover, Toll, JAK/STAT and melanization pathway were all induced during the N. bombycis infection, which is helpful to construct a global comprehension of molecular immunoresponse. Some important genes involved in pathogen recognition, immunoregulation, and immuoeffectors were obtained, and the melanization pathway could be perturbed by the pathogen secreted proteins, providing interesting clues for further research on host-parasite interaction. The identification of N. bombycis-specific response factors could provide structural models for anti-microsporidia drug design or candidate genes for generating transgenic silkworms with high resistance to N.bombycis. Additionally, 90% agricultural pests belong to Lepidoptera, silkworm as the model of Lepidoptera; thus, allowing us to explore the potential drug target proteins in silkworm immunoresponse to intracellular parasites as the vulnerability of pests, which can also be utilized in pest control.

 

Contact:

Zeyang Zhou Ph.D.

Professor

State Key Laboratory of Silkworm Genome Biology

Key Laboratory for Sericulture Functional Genomics and Biotechnology of Agricultural Ministry

SouthwestUniversity

Chongqing, China

E-mail: zyzhou@swu.edu.cn

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