Sodium Humate-Derived Gut Microbiota Ameliorates Intestinal Dysfunction Induced by Salmonella Typhimurium in Mice
ABSTRACT Salmonella is a foodborne pathogen that is one of the main causes of gastroenteric disease in humans and animals. As a natural organic substance, sodium humate (HNa) possesses antibacterial, antidiarrheal, and anti-inflammatory properties. However, it is unclear whether the HNa and HNa-deri...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-06-01
|
| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.05348-22 |
| _version_ | 1797803472719970304 |
|---|---|
| author | Dong Wang Yingce Zheng Yuying Fan Yanjun He Kexin Liu Shouxiang Deng Yun Liu |
| author_facet | Dong Wang Yingce Zheng Yuying Fan Yanjun He Kexin Liu Shouxiang Deng Yun Liu |
| author_sort | Dong Wang |
| collection | DOAJ |
| description | ABSTRACT Salmonella is a foodborne pathogen that is one of the main causes of gastroenteric disease in humans and animals. As a natural organic substance, sodium humate (HNa) possesses antibacterial, antidiarrheal, and anti-inflammatory properties. However, it is unclear whether the HNa and HNa-derived microbiota exert alleviative effects on Salmonella enterica serovar Typhimurium-induced enteritis. We found that treatment with HNa disrupted the cell wall of S. Typhimurium and decreased the virulence gene expression. Next, we explored the effect of HNa presupplementation on S. Typhimurium-induced murine enteritis. The results revealed that HNa ameliorated intestinal pathological damage. In addition, we observed that presupplementation with HNa enhanced intestinal barrier function via modulating gut microbiota, downregulating toll-like receptor 4 (TLR4)/nuclear factor kappa-B (NF-κB) and NOD-like receptor protein 3 (NLRP3) signaling pathways, regulating intestinal mucosal immunity, and enhancing tight junction protein expression. To further validate the effect of HNa-derived microbiota on S. Typhimurium-induced enteritis, we performed fecal microbiota transplantation and found that HNa-derived microbiota also alleviated S. Typhimurium-induced intestinal damage. It is noteworthy that both HNa and HNa-derived microbiota improved the liver injury caused by S. Typhimurium infection. Collectively, this is the first study to confirm that HNa could alleviate S. Typhimurium-induced enteritis in a gut microbiota-dependent manner. This study provides a new perspective on HNa as a potential drug to prevent and treat salmonellosis. IMPORTANCE Salmonella Typhimurium is an important zoonotic pathogen, widely distributed in nature. S. Typhimurium is one of the leading causes of foodborne illnesses worldwide, and more than 350,000 people died from Salmonella infection each year, which poses a substantial risk to public health and causes a considerable economic loss. Here, we found that the S. Typhimurium infection caused severe intestinal and liver damage. In addition, we first found that sodium humate (HNa) and HNa-derived gut microbiota can alleviate S. Typhimurium infection-induced intestinal damage. These findings extend the knowledge about the public health risk and pathogenic mechanisms of S. Typhimurium. |
| first_indexed | 2024-03-13T05:21:27Z |
| format | Article |
| id | doaj.art-839d121a639e4fb9a134e76ad06cafca |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-13T05:21:27Z |
| publishDate | 2023-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-839d121a639e4fb9a134e76ad06cafca2023-06-15T13:18:31ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.05348-22Sodium Humate-Derived Gut Microbiota Ameliorates Intestinal Dysfunction Induced by Salmonella Typhimurium in MiceDong Wang0Yingce Zheng1Yuying Fan2Yanjun He3Kexin Liu4Shouxiang Deng5Yun Liu6Heilongjiang Key Laboratory of Experimental Animals and Comparative Medicine, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory of Experimental Animals and Comparative Medicine, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory of Experimental Animals and Comparative Medicine, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory of Experimental Animals and Comparative Medicine, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory of Experimental Animals and Comparative Medicine, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory of Experimental Animals and Comparative Medicine, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory of Experimental Animals and Comparative Medicine, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaABSTRACT Salmonella is a foodborne pathogen that is one of the main causes of gastroenteric disease in humans and animals. As a natural organic substance, sodium humate (HNa) possesses antibacterial, antidiarrheal, and anti-inflammatory properties. However, it is unclear whether the HNa and HNa-derived microbiota exert alleviative effects on Salmonella enterica serovar Typhimurium-induced enteritis. We found that treatment with HNa disrupted the cell wall of S. Typhimurium and decreased the virulence gene expression. Next, we explored the effect of HNa presupplementation on S. Typhimurium-induced murine enteritis. The results revealed that HNa ameliorated intestinal pathological damage. In addition, we observed that presupplementation with HNa enhanced intestinal barrier function via modulating gut microbiota, downregulating toll-like receptor 4 (TLR4)/nuclear factor kappa-B (NF-κB) and NOD-like receptor protein 3 (NLRP3) signaling pathways, regulating intestinal mucosal immunity, and enhancing tight junction protein expression. To further validate the effect of HNa-derived microbiota on S. Typhimurium-induced enteritis, we performed fecal microbiota transplantation and found that HNa-derived microbiota also alleviated S. Typhimurium-induced intestinal damage. It is noteworthy that both HNa and HNa-derived microbiota improved the liver injury caused by S. Typhimurium infection. Collectively, this is the first study to confirm that HNa could alleviate S. Typhimurium-induced enteritis in a gut microbiota-dependent manner. This study provides a new perspective on HNa as a potential drug to prevent and treat salmonellosis. IMPORTANCE Salmonella Typhimurium is an important zoonotic pathogen, widely distributed in nature. S. Typhimurium is one of the leading causes of foodborne illnesses worldwide, and more than 350,000 people died from Salmonella infection each year, which poses a substantial risk to public health and causes a considerable economic loss. Here, we found that the S. Typhimurium infection caused severe intestinal and liver damage. In addition, we first found that sodium humate (HNa) and HNa-derived gut microbiota can alleviate S. Typhimurium infection-induced intestinal damage. These findings extend the knowledge about the public health risk and pathogenic mechanisms of S. Typhimurium.https://journals.asm.org/doi/10.1128/spectrum.05348-22Salmonella Typhimuriumsodium humategut microbiotafecal microbiota transplantationintestinal barrier function |
| spellingShingle | Dong Wang Yingce Zheng Yuying Fan Yanjun He Kexin Liu Shouxiang Deng Yun Liu Sodium Humate-Derived Gut Microbiota Ameliorates Intestinal Dysfunction Induced by Salmonella Typhimurium in Mice Microbiology Spectrum Salmonella Typhimurium sodium humate gut microbiota fecal microbiota transplantation intestinal barrier function |
| title | Sodium Humate-Derived Gut Microbiota Ameliorates Intestinal Dysfunction Induced by Salmonella Typhimurium in Mice |
| title_full | Sodium Humate-Derived Gut Microbiota Ameliorates Intestinal Dysfunction Induced by Salmonella Typhimurium in Mice |
| title_fullStr | Sodium Humate-Derived Gut Microbiota Ameliorates Intestinal Dysfunction Induced by Salmonella Typhimurium in Mice |
| title_full_unstemmed | Sodium Humate-Derived Gut Microbiota Ameliorates Intestinal Dysfunction Induced by Salmonella Typhimurium in Mice |
| title_short | Sodium Humate-Derived Gut Microbiota Ameliorates Intestinal Dysfunction Induced by Salmonella Typhimurium in Mice |
| title_sort | sodium humate derived gut microbiota ameliorates intestinal dysfunction induced by salmonella typhimurium in mice |
| topic | Salmonella Typhimurium sodium humate gut microbiota fecal microbiota transplantation intestinal barrier function |
| url | https://journals.asm.org/doi/10.1128/spectrum.05348-22 |
| work_keys_str_mv | AT dongwang sodiumhumatederivedgutmicrobiotaamelioratesintestinaldysfunctioninducedbysalmonellatyphimuriuminmice AT yingcezheng sodiumhumatederivedgutmicrobiotaamelioratesintestinaldysfunctioninducedbysalmonellatyphimuriuminmice AT yuyingfan sodiumhumatederivedgutmicrobiotaamelioratesintestinaldysfunctioninducedbysalmonellatyphimuriuminmice AT yanjunhe sodiumhumatederivedgutmicrobiotaamelioratesintestinaldysfunctioninducedbysalmonellatyphimuriuminmice AT kexinliu sodiumhumatederivedgutmicrobiotaamelioratesintestinaldysfunctioninducedbysalmonellatyphimuriuminmice AT shouxiangdeng sodiumhumatederivedgutmicrobiotaamelioratesintestinaldysfunctioninducedbysalmonellatyphimuriuminmice AT yunliu sodiumhumatederivedgutmicrobiotaamelioratesintestinaldysfunctioninducedbysalmonellatyphimuriuminmice |