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Comprehensive characterization of the impairing effects of Nosema bombycis on the host digestive integrity and
Lu Cao1,2, Siying Yin1,2, Dexu Liu1,2
1The State Key Laboratory of Resource Insects, Southwest University, Chongqing, China.
Abstract:
Nosema bombycis (N. bombycis) infection causes growth retardation and indigestion of silkworms (Bombyx mori). The digestive tract is the primary infection route; thereby, in this study, we comprehensively investigated the disturbances of the digestive tract upon N. bombycis infection. Electron microscopy demonstrated the structure and integrity impairments of the peritrophic membrane and midgut after infection. A quantitative proteomic approach identified approximately 2,893 dysregulated proteins in the midgut after infection. Next, 16S rRNA and ITS analysis of the digestive juice and stool samples revealed that the gut microbiome profiles were significantly disturbed, such as bacterial genus Acinetobacter, Staphylococcus, as well as eukaryotic Penicillium, Chaetasbolisia, and so on. In addition, various digestive enzyme expressions were also disturbed upon N. bombycis infection. More interestingly, we found that chitin deacetylase BmCDA8, one of the top dysregulated host proteins, functioned as the key protective enzyme against N. bombycis since knocking down BmCDA8 leads to increased barrier permeability and higher N. bombycis loads. We also identified 24 N. bombycis proteins that would potentially interact with BmCDA8. Taken together, our investigation will help to fully elucidate the impairing effects of N. bombycis on host and to identify novel pathogen control targets.IMPORTANCEThe digestive tract is the major infection route of many pathogens. A comprehensive view of the impairing effects of N. bombycis on B. mori's digestive tract integrity, microbiome, and enzyme compositions is greatly needed. Therefore, we applied electron microscopy, quantitative proteomics, and microbiome analysis to clearly demonstrate that N. bombycis infections did impair host intestinal integrity, changed the gut microbiome composition, and dysregulated digestive enzymes. Interestingly, we found that the chitin deacetylase of B. mori exerts an essential protective role, and N. bombycis effector proteins may interact directly with it to facilitate the impairing effects. Our findings provide a comprehensive view and decode the phenomena of silkworm indigestion and growth retardation after N. bombycis infection and will provide potential targets for disease prevention and control.
Insights
Nosema bombycis infection severely impacts silkworm digestion and growth by damaging the gut lining and altering the microbiome. Silkworm chitin deacetylase BmCDA8 is crucial for defense, with pathogen proteins potentially targeting it.
Area of Science:
- Insect Pathology
- Microbiology
- Proteomics
Background:
- Nosema bombycis (N. bombycis) infection causes significant growth retardation and indigestion in silkworms (Bombyx mori).
- The digestive tract serves as the primary route for N. bombycis infection, necessitating a detailed investigation into its effects on this system.
Purpose of the Study:
- To comprehensively investigate the disturbances within the silkworm digestive tract caused by N. bombycis infection.
- To identify key host-pathogen interactions and potential targets for disease control.
Main Methods:
- Electron microscopy to assess structural integrity of the peritrophic membrane and midgut.
- Quantitative proteomics to identify dysregulated proteins in the midgut.
- 16S rRNA and ITS sequencing for gut microbiome profiling.
- Gene knockdown experiments to evaluate the role of BmCDA8.
Main Results:
- N. bombycis infection caused structural damage to the peritrophic membrane and midgut, with approximately 2,893 dysregulated proteins identified.
- Significant alterations in gut microbiome composition (bacterial and eukaryotic) were observed.
- Silkworm chitin deacetylase BmCDA8 was identified as a key protective enzyme; its knockdown increased pathogen load and barrier permeability.
- 24 N. bombycis proteins were predicted to interact with BmCDA8.
Conclusions:
- N. bombycis infection severely impairs silkworm intestinal integrity, alters gut microbiome, and dysregulates digestive enzymes.
- BmCDA8 plays a critical protective role against N. bombycis infection.
- N. bombycis effector proteins may directly target BmCDA8 to facilitate infection, offering potential targets for novel disease control strategies.
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