The Mechanism of <i>Elizabethkingia miricola</i> Infection of the Black Spotted Frog as Revealed by Multi-Omics Analysis
<i>Elizabethkingia miricola</i> (<i>E. miricola</i>) is a significant pathogen that causes the crooked head disease in black spotted frogs. This disease has plagued numerous frog farms in China and has resulted in substantial losses to the frog farming industry. Nonetheless,...
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| Format: | Article |
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MDPI AG
2024-02-01
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| Series: | Fishes |
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| Online Access: | https://www.mdpi.com/2410-3888/9/3/91 |
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| author | Qingcong Wei Dan Wang Kaijin Wei Bin Xu Jin Xu |
| author_facet | Qingcong Wei Dan Wang Kaijin Wei Bin Xu Jin Xu |
| author_sort | Qingcong Wei |
| collection | DOAJ |
| description | <i>Elizabethkingia miricola</i> (<i>E. miricola</i>) is a significant pathogen that causes the crooked head disease in black spotted frogs. This disease has plagued numerous frog farms in China and has resulted in substantial losses to the frog farming industry. Nonetheless, the exact mechanism that causes the disease in frogs remains unknown. In this study, transcriptomic and microbiomic analyses were conducted to analyze frog samples infected with <i>E. miricola</i> to reveal the infection mechanism of the pathogen. Liver transcriptomic analysis indicated that the livers of infected frogs had 1469 differentially expressed genes when compared with an uninfected group. These DEGs are mainly involved in immunity and metabolism, including neutrophil extracellular trap formation, the NOD-like receptor signaling pathway, leukocyte transendothelial migration, chemokine signaling pathway, Fc gamma R-mediated phagocytosis, and “metabolism”-related pathways such as the pentose phosphate pathway, carbon metabolism, glycerophospholipid metabolism, and glycerolipid metabolism. Similarly, 4737 DEGs were found in the kidney of infected frogs. These DEGs are mainly involved in immunity, including neutrophil extracellular trap formation, the NOD-like receptor signaling pathway, B cell receptor signaling pathway, C-type lectin receptor signaling pathway, complement and coagulation cascade, and Toll-like receptor signaling pathway. Ten immune-associated DEGs were screened in liver and kidney DEGs, respectively. And it was hypothesized that <i>E. miricola</i> infection could influence the host immune response. Microbiome analysis results showed that some opportunistic pathogens such as <i>Citrobacter</i>, <i>Shigella</i>, and <i>Providencia</i> were significantly elevated (<i>p</i> < 0.05) in infected frogs. Additionally, functional prediction confirmed that most of the microbiota in infected frogs were linked to metabolism-related KEGG pathways. In this study, the screened genes linked to immunity showed an association with the gut microbiome. The majority of these genes were found to be linked with the abundance of opportunistic pathogens. The results showed that <i>E. miricola</i> infection led to the downregulation of immune and metabolic-related genes, which led to the inhibition of immune function and metabolic disorder, and then increased the abundance of opportunistic pathogens in the gut microbiota. The findings of this study offer a preliminary foundation for comprehending the pathogenic processes of <i>E. miricola</i> infection in black spotted frogs. |
| first_indexed | 2024-04-24T18:16:35Z |
| format | Article |
| id | doaj.art-238e96dec292445f8b334a519e771d07 |
| institution | Directory Open Access Journal |
| issn | 2410-3888 |
| language | English |
| last_indexed | 2024-04-24T18:16:35Z |
| publishDate | 2024-02-01 |
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| spelling | doaj.art-238e96dec292445f8b334a519e771d072024-03-27T13:38:18ZengMDPI AGFishes2410-38882024-02-01939110.3390/fishes9030091The Mechanism of <i>Elizabethkingia miricola</i> Infection of the Black Spotted Frog as Revealed by Multi-Omics AnalysisQingcong Wei0Dan Wang1Kaijin Wei2Bin Xu3Jin Xu4College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, ChinaYangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan 430223, ChinaYangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan 430223, ChinaYangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan 430223, ChinaYangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan 430223, China<i>Elizabethkingia miricola</i> (<i>E. miricola</i>) is a significant pathogen that causes the crooked head disease in black spotted frogs. This disease has plagued numerous frog farms in China and has resulted in substantial losses to the frog farming industry. Nonetheless, the exact mechanism that causes the disease in frogs remains unknown. In this study, transcriptomic and microbiomic analyses were conducted to analyze frog samples infected with <i>E. miricola</i> to reveal the infection mechanism of the pathogen. Liver transcriptomic analysis indicated that the livers of infected frogs had 1469 differentially expressed genes when compared with an uninfected group. These DEGs are mainly involved in immunity and metabolism, including neutrophil extracellular trap formation, the NOD-like receptor signaling pathway, leukocyte transendothelial migration, chemokine signaling pathway, Fc gamma R-mediated phagocytosis, and “metabolism”-related pathways such as the pentose phosphate pathway, carbon metabolism, glycerophospholipid metabolism, and glycerolipid metabolism. Similarly, 4737 DEGs were found in the kidney of infected frogs. These DEGs are mainly involved in immunity, including neutrophil extracellular trap formation, the NOD-like receptor signaling pathway, B cell receptor signaling pathway, C-type lectin receptor signaling pathway, complement and coagulation cascade, and Toll-like receptor signaling pathway. Ten immune-associated DEGs were screened in liver and kidney DEGs, respectively. And it was hypothesized that <i>E. miricola</i> infection could influence the host immune response. Microbiome analysis results showed that some opportunistic pathogens such as <i>Citrobacter</i>, <i>Shigella</i>, and <i>Providencia</i> were significantly elevated (<i>p</i> < 0.05) in infected frogs. Additionally, functional prediction confirmed that most of the microbiota in infected frogs were linked to metabolism-related KEGG pathways. In this study, the screened genes linked to immunity showed an association with the gut microbiome. The majority of these genes were found to be linked with the abundance of opportunistic pathogens. The results showed that <i>E. miricola</i> infection led to the downregulation of immune and metabolic-related genes, which led to the inhibition of immune function and metabolic disorder, and then increased the abundance of opportunistic pathogens in the gut microbiota. The findings of this study offer a preliminary foundation for comprehending the pathogenic processes of <i>E. miricola</i> infection in black spotted frogs.https://www.mdpi.com/2410-3888/9/3/91black spotted frog<i>Elizabethkingia miricola</i>transcriptomegut microbiome |
| spellingShingle | Qingcong Wei Dan Wang Kaijin Wei Bin Xu Jin Xu The Mechanism of <i>Elizabethkingia miricola</i> Infection of the Black Spotted Frog as Revealed by Multi-Omics Analysis Fishes black spotted frog <i>Elizabethkingia miricola</i> transcriptome gut microbiome |
| title | The Mechanism of <i>Elizabethkingia miricola</i> Infection of the Black Spotted Frog as Revealed by Multi-Omics Analysis |
| title_full | The Mechanism of <i>Elizabethkingia miricola</i> Infection of the Black Spotted Frog as Revealed by Multi-Omics Analysis |
| title_fullStr | The Mechanism of <i>Elizabethkingia miricola</i> Infection of the Black Spotted Frog as Revealed by Multi-Omics Analysis |
| title_full_unstemmed | The Mechanism of <i>Elizabethkingia miricola</i> Infection of the Black Spotted Frog as Revealed by Multi-Omics Analysis |
| title_short | The Mechanism of <i>Elizabethkingia miricola</i> Infection of the Black Spotted Frog as Revealed by Multi-Omics Analysis |
| title_sort | mechanism of i elizabethkingia miricola i infection of the black spotted frog as revealed by multi omics analysis |
| topic | black spotted frog <i>Elizabethkingia miricola</i> transcriptome gut microbiome |
| url | https://www.mdpi.com/2410-3888/9/3/91 |
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