Effects of Antibiotic Residues on Fish Gut Microbiome Dysbiosis and Mucosal Barrier-Related Pathogen Susceptibility in Zebrafish Experimental Model
The symbiotic community of microorganisms in the gut plays an important role in the health of the host. While many previous studies have been performed on the interactions between the gut microbiome and the host in mammals, studies in fish are still lacking. In this study, we investigated changes in...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2024-01-01
|
| Series: | Antibiotics |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2079-6382/13/1/82 |
| _version_ | 1797344784965173248 |
|---|---|
| author | Jun Hyeok Yang Jeong Woo Park Ho Sung Kim Seungki Lee Aaron M. Yerke Yogini S. Jaiswal Leonard L. Williams Sungmin Hwang Ki Hwan Moon |
| author_facet | Jun Hyeok Yang Jeong Woo Park Ho Sung Kim Seungki Lee Aaron M. Yerke Yogini S. Jaiswal Leonard L. Williams Sungmin Hwang Ki Hwan Moon |
| author_sort | Jun Hyeok Yang |
| collection | DOAJ |
| description | The symbiotic community of microorganisms in the gut plays an important role in the health of the host. While many previous studies have been performed on the interactions between the gut microbiome and the host in mammals, studies in fish are still lacking. In this study, we investigated changes in the intestinal microbiome and pathogen susceptibility of zebrafish (<i>Danio rerio</i>) following chronic antibiotics exposure. The chronic antibiotics exposure assay was performed on zebrafish for 30 days using oxytetracycline (Otc), sulfamethoxazole/trimethoprim (Smx/Tmp), or erythromycin (Ery), which are antibiotics widely used in the aquaculture industry. The microbiome analysis indicated that Fusobacteria, Proteobacteria, Firmicutes, and Bacteroidetes were the dominant phyla in the gut microbiome of the zebrafish used in this study. However, in Smx/Tmp-treated zebrafish, the compositions of Fusobacteria and Proteobacteria were changed significantly, and in Ery-treated zebrafish, the compositions of Proteobacteria and Firmicutes were altered significantly. Although alpha diversity analysis showed that there was no significant difference in the richness, beta diversity analysis revealed a community imbalance in the gut microbiome of all chronically antibiotics-exposed zebrafish. Intriguingly, in zebrafish with dysbiosis in the gut microbiome, the pathogen susceptibility to <i>Edwardsiella piscicida</i>, a representative Gram-negative fish pathogen, was reduced. Gut microbiome imbalance resulted in a higher count of goblet cells in intestinal tissue and an upregulation of genes related to the intestinal mucosal barrier. In addition, as innate immunity was enhanced by the increased mucosal barrier, immune and stress-related gene expression in the intestinal tissue was downregulated. In this study, we provide new insight into the effect of gut microbiome dysbiosis on pathogen susceptibility. |
| first_indexed | 2024-03-08T11:07:56Z |
| format | Article |
| id | doaj.art-e660f8e4a56c4cbdb7cae015615dd362 |
| institution | Directory Open Access Journal |
| issn | 2079-6382 |
| language | English |
| last_indexed | 2024-03-08T11:07:56Z |
| publishDate | 2024-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Antibiotics |
| spelling | doaj.art-e660f8e4a56c4cbdb7cae015615dd3622024-01-26T14:38:24ZengMDPI AGAntibiotics2079-63822024-01-011318210.3390/antibiotics13010082Effects of Antibiotic Residues on Fish Gut Microbiome Dysbiosis and Mucosal Barrier-Related Pathogen Susceptibility in Zebrafish Experimental ModelJun Hyeok Yang0Jeong Woo Park1Ho Sung Kim2Seungki Lee3Aaron M. Yerke4Yogini S. Jaiswal5Leonard L. Williams6Sungmin Hwang7Ki Hwan Moon8Laboratory of Marine Microbiology, Division of Convergence of Marine Science, Korea Maritime & Ocean University, Busan 49112, Republic of KoreaLaboratory of Marine Microbiology, Division of Convergence of Marine Science, Korea Maritime & Ocean University, Busan 49112, Republic of KoreaLaboratory of Marine Microbiology, Division of Convergence of Marine Science, Korea Maritime & Ocean University, Busan 49112, Republic of KoreaNational Institute of Biological Resources, Environmental Research Complex, Incheon 22689, Republic of KoreaDepartment of Bioinformatics and Genomics, University of North Carolina at Charlotte, Charlotte, NC 28223, USACenter for Excellence in Post Harvest Technologies, North Carolina Agricultural and Technical State University, The North Carolina Research Campus, 500 Laureate Way, Kannapolis, NC 28081, USACenter for Excellence in Post Harvest Technologies, North Carolina Agricultural and Technical State University, The North Carolina Research Campus, 500 Laureate Way, Kannapolis, NC 28081, USADivision of Practical Research, Honam National Institute Biological Resources, Mokpo-si 58762, Republic of KoreaLaboratory of Marine Microbiology, Division of Convergence of Marine Science, Korea Maritime & Ocean University, Busan 49112, Republic of KoreaThe symbiotic community of microorganisms in the gut plays an important role in the health of the host. While many previous studies have been performed on the interactions between the gut microbiome and the host in mammals, studies in fish are still lacking. In this study, we investigated changes in the intestinal microbiome and pathogen susceptibility of zebrafish (<i>Danio rerio</i>) following chronic antibiotics exposure. The chronic antibiotics exposure assay was performed on zebrafish for 30 days using oxytetracycline (Otc), sulfamethoxazole/trimethoprim (Smx/Tmp), or erythromycin (Ery), which are antibiotics widely used in the aquaculture industry. The microbiome analysis indicated that Fusobacteria, Proteobacteria, Firmicutes, and Bacteroidetes were the dominant phyla in the gut microbiome of the zebrafish used in this study. However, in Smx/Tmp-treated zebrafish, the compositions of Fusobacteria and Proteobacteria were changed significantly, and in Ery-treated zebrafish, the compositions of Proteobacteria and Firmicutes were altered significantly. Although alpha diversity analysis showed that there was no significant difference in the richness, beta diversity analysis revealed a community imbalance in the gut microbiome of all chronically antibiotics-exposed zebrafish. Intriguingly, in zebrafish with dysbiosis in the gut microbiome, the pathogen susceptibility to <i>Edwardsiella piscicida</i>, a representative Gram-negative fish pathogen, was reduced. Gut microbiome imbalance resulted in a higher count of goblet cells in intestinal tissue and an upregulation of genes related to the intestinal mucosal barrier. In addition, as innate immunity was enhanced by the increased mucosal barrier, immune and stress-related gene expression in the intestinal tissue was downregulated. In this study, we provide new insight into the effect of gut microbiome dysbiosis on pathogen susceptibility.https://www.mdpi.com/2079-6382/13/1/82antibioticsgut microbiomeintestinal mucosal barrierpathogen susceptibilityzebrafish |
| spellingShingle | Jun Hyeok Yang Jeong Woo Park Ho Sung Kim Seungki Lee Aaron M. Yerke Yogini S. Jaiswal Leonard L. Williams Sungmin Hwang Ki Hwan Moon Effects of Antibiotic Residues on Fish Gut Microbiome Dysbiosis and Mucosal Barrier-Related Pathogen Susceptibility in Zebrafish Experimental Model Antibiotics antibiotics gut microbiome intestinal mucosal barrier pathogen susceptibility zebrafish |
| title | Effects of Antibiotic Residues on Fish Gut Microbiome Dysbiosis and Mucosal Barrier-Related Pathogen Susceptibility in Zebrafish Experimental Model |
| title_full | Effects of Antibiotic Residues on Fish Gut Microbiome Dysbiosis and Mucosal Barrier-Related Pathogen Susceptibility in Zebrafish Experimental Model |
| title_fullStr | Effects of Antibiotic Residues on Fish Gut Microbiome Dysbiosis and Mucosal Barrier-Related Pathogen Susceptibility in Zebrafish Experimental Model |
| title_full_unstemmed | Effects of Antibiotic Residues on Fish Gut Microbiome Dysbiosis and Mucosal Barrier-Related Pathogen Susceptibility in Zebrafish Experimental Model |
| title_short | Effects of Antibiotic Residues on Fish Gut Microbiome Dysbiosis and Mucosal Barrier-Related Pathogen Susceptibility in Zebrafish Experimental Model |
| title_sort | effects of antibiotic residues on fish gut microbiome dysbiosis and mucosal barrier related pathogen susceptibility in zebrafish experimental model |
| topic | antibiotics gut microbiome intestinal mucosal barrier pathogen susceptibility zebrafish |
| url | https://www.mdpi.com/2079-6382/13/1/82 |
| work_keys_str_mv | AT junhyeokyang effectsofantibioticresiduesonfishgutmicrobiomedysbiosisandmucosalbarrierrelatedpathogensusceptibilityinzebrafishexperimentalmodel AT jeongwoopark effectsofantibioticresiduesonfishgutmicrobiomedysbiosisandmucosalbarrierrelatedpathogensusceptibilityinzebrafishexperimentalmodel AT hosungkim effectsofantibioticresiduesonfishgutmicrobiomedysbiosisandmucosalbarrierrelatedpathogensusceptibilityinzebrafishexperimentalmodel AT seungkilee effectsofantibioticresiduesonfishgutmicrobiomedysbiosisandmucosalbarrierrelatedpathogensusceptibilityinzebrafishexperimentalmodel AT aaronmyerke effectsofantibioticresiduesonfishgutmicrobiomedysbiosisandmucosalbarrierrelatedpathogensusceptibilityinzebrafishexperimentalmodel AT yoginisjaiswal effectsofantibioticresiduesonfishgutmicrobiomedysbiosisandmucosalbarrierrelatedpathogensusceptibilityinzebrafishexperimentalmodel AT leonardlwilliams effectsofantibioticresiduesonfishgutmicrobiomedysbiosisandmucosalbarrierrelatedpathogensusceptibilityinzebrafishexperimentalmodel AT sungminhwang effectsofantibioticresiduesonfishgutmicrobiomedysbiosisandmucosalbarrierrelatedpathogensusceptibilityinzebrafishexperimentalmodel AT kihwanmoon effectsofantibioticresiduesonfishgutmicrobiomedysbiosisandmucosalbarrierrelatedpathogensusceptibilityinzebrafishexperimentalmodel |