Characteristics of Lactococcus petauri GB97 lysate isolated from porcine feces and its in vitro and in vivo effects on inflammation, intestinal barrier function, and gut microbiota composition in mice
ABSTRACT Weaning in piglet management is important to improve pork production. Controlling gut inflammation and colitis is important in managing growth performance in piglets after weaning. Previously, we found that treatment with a lysate of Lactococcus petauri GB97 (LPL97) from porcine feces allev...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2024-01-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01334-23 |
| _version_ | 1827383626456629248 |
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| author | Ki-Nam Yoon Soo-Jeong Lee Gi Beom Keum Ki-Young Song Jong-Heum Park Beom-Seok Song Seung Yeob Yu Jae Hyoung Cho Eun Sol Kim Hyunok Doo Jinok Kwak Sheena Kim Jong-Bang Eun Ju Huck Lee Hyeun Bum Kim Ju-Hoon Lee Jae-Kyung Kim |
| author_facet | Ki-Nam Yoon Soo-Jeong Lee Gi Beom Keum Ki-Young Song Jong-Heum Park Beom-Seok Song Seung Yeob Yu Jae Hyoung Cho Eun Sol Kim Hyunok Doo Jinok Kwak Sheena Kim Jong-Bang Eun Ju Huck Lee Hyeun Bum Kim Ju-Hoon Lee Jae-Kyung Kim |
| author_sort | Ki-Nam Yoon |
| collection | DOAJ |
| description | ABSTRACT Weaning in piglet management is important to improve pork production. Controlling gut inflammation and colitis is important in managing growth performance in piglets after weaning. Previously, we found that treatment with a lysate of Lactococcus petauri GB97 (LPL97) from porcine feces alleviated lipopolysaccharide-induced inflammatory response in RAW 264.7 cells. Here, we aimed to evaluate the exact role of LPL97 in modulating inflammation, epithelial barrier function, and gut microbiota composition, both in vitro and in vivo, in an experimental dextran sulfate sodium (DSS)-induced colitis mouse model. Compared to control colitis mice, LPL97 inhibited shortening of the colon, percentage body weight reduction, and mucosal damage. Moreover, LPL97 treatment downregulated the serum levels of pro-inflammatory factors and their mRNA expression in colon tissue but increased the levels of anti-inflammatory cytokine. LPL97 also reduced intestinal permeability by increasing the expression levels of tight junction (TJ) proteins in colon tissues. Additionally, 16S rRNA gene analysis demonstrated the effect of LPL97 treatment on DSS-induced inflammation via microbiome changes in the mouse intestine. At the genus level, the relative abundance of Mucispirillum, Intestinimonas, Staphylococcus, and Pseudomonas, which was significantly higher in the DSS-treated group than in the control group, decreased significantly in the LPL97 group compared to that in the DSS group. This study provides evidence that LPL97 can prevent intestinal inflammation and strengthen the integrity of the intestinal barrier by altering the gut microbiota, suggesting its promising potential for prophylaxis and treatment of colitis in pig farming. IMPORTANCE Weaning is a crucial step in piglet management to improve pork production. During the weaning phase, disruption of epithelial barrier function and intestinal inflammation can lead to decreased absorption of nutrients and diarrhea. Therefore, maintaining a healthy intestine, epithelial barrier function, and gut microbiota composition in this crucial phase is strategic for optimal weaning in pigs. We isolated a lysate of Lactococcus petauri GB97 (LPL97) from healthy porcine feces and evaluated its anti-inflammatory activities, barrier integrity, and gut microbial changes in LPS-induced murine macrophages and DSS-induced colitis mice. We found that LPL97 regulated the immune response by downregulating the TLR4/NF-κB/MAPK signaling pathway both in vitro and in vivo. Furthermore, LPL97 alleviated the disruption of intestinal epithelial integrity and gut microbiota dysbiosis in colitis mice. This study indicates that LPL97 has the potential to be developed as an alternative feed additive to antibiotics for the swine industry. |
| first_indexed | 2024-03-08T14:43:55Z |
| format | Article |
| id | doaj.art-5e2d247a856647778e46f6a378e722ac |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-08T14:43:55Z |
| publishDate | 2024-01-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-5e2d247a856647778e46f6a378e722ac2024-01-11T14:04:38ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-01-0112110.1128/spectrum.01334-23Characteristics of Lactococcus petauri GB97 lysate isolated from porcine feces and its in vitro and in vivo effects on inflammation, intestinal barrier function, and gut microbiota composition in miceKi-Nam Yoon0Soo-Jeong Lee1Gi Beom Keum2Ki-Young Song3Jong-Heum Park4Beom-Seok Song5Seung Yeob Yu6Jae Hyoung Cho7Eun Sol Kim8Hyunok Doo9Jinok Kwak10Sheena Kim11Jong-Bang Eun12Ju Huck Lee13Hyeun Bum Kim14Ju-Hoon Lee15Jae-Kyung Kim16Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute , Jeongeup-si, South KoreaDepartment of Food and Animal Biotechnology, Seoul National University , Seoul, South KoreaDepartment of Animal Resources Science, Dankook University , Cheonan, South KoreaAdvanced Radiation Technology Institute, Korea Atomic Energy Research Institute , Jeongeup-si, South KoreaAdvanced Radiation Technology Institute, Korea Atomic Energy Research Institute , Jeongeup-si, South KoreaAdvanced Radiation Technology Institute, Korea Atomic Energy Research Institute , Jeongeup-si, South KoreaKorean Collection for Type Cultures, Korea Research Institute of Bioscience and Biotechnology , Jeongeup-si, South KoreaDepartment of Animal Resources Science, Dankook University , Cheonan, South KoreaDepartment of Animal Resources Science, Dankook University , Cheonan, South KoreaDepartment of Animal Resources Science, Dankook University , Cheonan, South KoreaDepartment of Animal Resources Science, Dankook University , Cheonan, South KoreaDepartment of Animal Resources Science, Dankook University , Cheonan, South KoreaDepartment of Food Science and Technology, Graduate School of Chonnam National University , Gwangju, South KoreaKorean Collection for Type Cultures, Korea Research Institute of Bioscience and Biotechnology , Jeongeup-si, South KoreaDepartment of Animal Resources Science, Dankook University , Cheonan, South KoreaDepartment of Food and Animal Biotechnology, Seoul National University , Seoul, South KoreaAdvanced Radiation Technology Institute, Korea Atomic Energy Research Institute , Jeongeup-si, South KoreaABSTRACT Weaning in piglet management is important to improve pork production. Controlling gut inflammation and colitis is important in managing growth performance in piglets after weaning. Previously, we found that treatment with a lysate of Lactococcus petauri GB97 (LPL97) from porcine feces alleviated lipopolysaccharide-induced inflammatory response in RAW 264.7 cells. Here, we aimed to evaluate the exact role of LPL97 in modulating inflammation, epithelial barrier function, and gut microbiota composition, both in vitro and in vivo, in an experimental dextran sulfate sodium (DSS)-induced colitis mouse model. Compared to control colitis mice, LPL97 inhibited shortening of the colon, percentage body weight reduction, and mucosal damage. Moreover, LPL97 treatment downregulated the serum levels of pro-inflammatory factors and their mRNA expression in colon tissue but increased the levels of anti-inflammatory cytokine. LPL97 also reduced intestinal permeability by increasing the expression levels of tight junction (TJ) proteins in colon tissues. Additionally, 16S rRNA gene analysis demonstrated the effect of LPL97 treatment on DSS-induced inflammation via microbiome changes in the mouse intestine. At the genus level, the relative abundance of Mucispirillum, Intestinimonas, Staphylococcus, and Pseudomonas, which was significantly higher in the DSS-treated group than in the control group, decreased significantly in the LPL97 group compared to that in the DSS group. This study provides evidence that LPL97 can prevent intestinal inflammation and strengthen the integrity of the intestinal barrier by altering the gut microbiota, suggesting its promising potential for prophylaxis and treatment of colitis in pig farming. IMPORTANCE Weaning is a crucial step in piglet management to improve pork production. During the weaning phase, disruption of epithelial barrier function and intestinal inflammation can lead to decreased absorption of nutrients and diarrhea. Therefore, maintaining a healthy intestine, epithelial barrier function, and gut microbiota composition in this crucial phase is strategic for optimal weaning in pigs. We isolated a lysate of Lactococcus petauri GB97 (LPL97) from healthy porcine feces and evaluated its anti-inflammatory activities, barrier integrity, and gut microbial changes in LPS-induced murine macrophages and DSS-induced colitis mice. We found that LPL97 regulated the immune response by downregulating the TLR4/NF-κB/MAPK signaling pathway both in vitro and in vivo. Furthermore, LPL97 alleviated the disruption of intestinal epithelial integrity and gut microbiota dysbiosis in colitis mice. This study indicates that LPL97 has the potential to be developed as an alternative feed additive to antibiotics for the swine industry.https://journals.asm.org/doi/10.1128/spectrum.01334-23Lactococus petauriparaprobioticslysateinflammation cytokinegut microbiotaintestinal barrier function |
| spellingShingle | Ki-Nam Yoon Soo-Jeong Lee Gi Beom Keum Ki-Young Song Jong-Heum Park Beom-Seok Song Seung Yeob Yu Jae Hyoung Cho Eun Sol Kim Hyunok Doo Jinok Kwak Sheena Kim Jong-Bang Eun Ju Huck Lee Hyeun Bum Kim Ju-Hoon Lee Jae-Kyung Kim Characteristics of Lactococcus petauri GB97 lysate isolated from porcine feces and its in vitro and in vivo effects on inflammation, intestinal barrier function, and gut microbiota composition in mice Microbiology Spectrum Lactococus petauri paraprobiotics lysate inflammation cytokine gut microbiota intestinal barrier function |
| title | Characteristics of Lactococcus petauri GB97 lysate isolated from porcine feces and its in vitro and in vivo effects on inflammation, intestinal barrier function, and gut microbiota composition in mice |
| title_full | Characteristics of Lactococcus petauri GB97 lysate isolated from porcine feces and its in vitro and in vivo effects on inflammation, intestinal barrier function, and gut microbiota composition in mice |
| title_fullStr | Characteristics of Lactococcus petauri GB97 lysate isolated from porcine feces and its in vitro and in vivo effects on inflammation, intestinal barrier function, and gut microbiota composition in mice |
| title_full_unstemmed | Characteristics of Lactococcus petauri GB97 lysate isolated from porcine feces and its in vitro and in vivo effects on inflammation, intestinal barrier function, and gut microbiota composition in mice |
| title_short | Characteristics of Lactococcus petauri GB97 lysate isolated from porcine feces and its in vitro and in vivo effects on inflammation, intestinal barrier function, and gut microbiota composition in mice |
| title_sort | characteristics of lactococcus petauri gb97 lysate isolated from porcine feces and its in vitro and in vivo effects on inflammation intestinal barrier function and gut microbiota composition in mice |
| topic | Lactococus petauri paraprobiotics lysate inflammation cytokine gut microbiota intestinal barrier function |
| url | https://journals.asm.org/doi/10.1128/spectrum.01334-23 |
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