Surface-Displayed Amuc_1100 From Akkermansia muciniphila on Lactococcus lactis ZHY1 Improves Hepatic Steatosis and Intestinal Health in High-Fat-Fed Zebrafish

Fatty liver and intestinal barrier damage were widespread in most farmed fish, which severely restrict the development of aquaculture. Therefore, there was an urgent need to develop green feed additives to maintain host liver and intestinal health. In this study, a probiotic pili-like protein, Amuc_...

Full description

Bibliographic Details
Main Authors: Feng-Li Zhang, Ya-Lin Yang, Zhen Zhang, Yuan-Yuan Yao, Rui Xia, Chen-Chen Gao, Dong-Dong Du, Juan Hu, Chao Ran, Zhen Liu, Zhi-Gang Zhou
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-10-01
Series:Frontiers in Nutrition
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnut.2021.726108/full
_version_ 1818824327683899392
author Feng-Li Zhang
Ya-Lin Yang
Zhen Zhang
Yuan-Yuan Yao
Rui Xia
Chen-Chen Gao
Dong-Dong Du
Juan Hu
Chao Ran
Zhen Liu
Zhi-Gang Zhou
author_facet Feng-Li Zhang
Ya-Lin Yang
Zhen Zhang
Yuan-Yuan Yao
Rui Xia
Chen-Chen Gao
Dong-Dong Du
Juan Hu
Chao Ran
Zhen Liu
Zhi-Gang Zhou
author_sort Feng-Li Zhang
collection DOAJ
description Fatty liver and intestinal barrier damage were widespread in most farmed fish, which severely restrict the development of aquaculture. Therefore, there was an urgent need to develop green feed additives to maintain host liver and intestinal health. In this study, a probiotic pili-like protein, Amuc_1100 (AM protein), was anchored to the surface of Lactococcus lactis ZHY1, and the effects of the recombinant bacteria AM-ZHY1 on liver fat accumulation and intestinal health were evaluated. Zebrafish were fed a basal diet, high-fat diet, and high-fat diet with AM-ZHY1 (108 cfu/g) or control bacteria ZHY1 for 4 weeks. Treatment with AM-ZHY1 significantly reduced hepatic steatosis in zebrafish. Quantitative PCR (qPCR) detection showed that the expression of the lipogenesis [peroxisome-proliferator-activated receptors (PPARγ), sterol regulatory element-binding proteins-1c (SREBP-1c), fatty acid synthase (FAS), and acetyl-CoA carboxylase 1 (ACC1)] and lipid transport genes (CD36 and FABP6) in the liver were significantly downregulated (p < 0.05), indicating that AM-ZHY1 could reduce liver fat accumulation by inhibiting lipid synthesis and absorption. Moreover, supplementing AM-ZHY1 to a high-fat diet could significantly reduce serum aspartate aminotransferase (AST) and alanine aminotransferase (ALT) levels, indicating that liver injury caused by high-fat diets was improved. The expression of tumor necrosis factor (TNF)-a and interleukin (IL)-6 in the liver decreased significantly (p < 0.05), while IL-1β and IL-10 did not change significantly in the AM-ZHY1 group. Compared to the high-fat diet-fed group, the AM-ZHY1 group, but not the ZHY1 group, significantly increased the expression of intestinal tight junction (TJ) proteins (TJP1a, claudina, claudin7, claudin7b, claudin11a, claudin12, and claudin15a; p < 0.05). Compared to the high-fat diet group, the Proteobacteria and Fusobacteria were significantly reduced and increased in the AM-ZHY1 group, respectively. In conclusion, the recombinant bacteria AM-ZHY1 has the capacity to maintain intestinal health by protecting intestinal integrity and improving intestinal flora structure and improving fatty liver disease by inhibiting lipid synthesis and absorption. This study will lay a foundation for the application of AM protein in improving abnormal fat deposition and restoring the intestinal barrier in fish.
first_indexed 2024-12-18T23:54:07Z
format Article
id doaj.art-197a311876504c30b0bef28ea33b2d24
institution Directory Open Access Journal
issn 2296-861X
language English
last_indexed 2024-12-18T23:54:07Z
publishDate 2021-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Nutrition
spelling doaj.art-197a311876504c30b0bef28ea33b2d242022-12-21T20:46:46ZengFrontiers Media S.A.Frontiers in Nutrition2296-861X2021-10-01810.3389/fnut.2021.726108726108Surface-Displayed Amuc_1100 From Akkermansia muciniphila on Lactococcus lactis ZHY1 Improves Hepatic Steatosis and Intestinal Health in High-Fat-Fed ZebrafishFeng-Li Zhang0Ya-Lin Yang1Zhen Zhang2Yuan-Yuan Yao3Rui Xia4Chen-Chen Gao5Dong-Dong Du6Juan Hu7Chao Ran8Zhen Liu9Zhi-Gang Zhou10Sino-Norway Fish Gastrointestinal Microbiota Joint Lab, Institute of Feed Research of Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory for Feed Biotechnology of the Ministry of Agriculture, Institute of Feed Research of Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory for Feed Biotechnology of the Ministry of Agriculture, Institute of Feed Research of Chinese Academy of Agricultural Sciences, Beijing, ChinaSino-Norway Fish Gastrointestinal Microbiota Joint Lab, Institute of Feed Research of Chinese Academy of Agricultural Sciences, Beijing, ChinaSino-Norway Fish Gastrointestinal Microbiota Joint Lab, Institute of Feed Research of Chinese Academy of Agricultural Sciences, Beijing, ChinaSino-Norway Fish Gastrointestinal Microbiota Joint Lab, Institute of Feed Research of Chinese Academy of Agricultural Sciences, Beijing, ChinaSino-Norway Fish Gastrointestinal Microbiota Joint Lab, Institute of Feed Research of Chinese Academy of Agricultural Sciences, Beijing, ChinaSino-Norway Fish Gastrointestinal Microbiota Joint Lab, Institute of Feed Research of Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory for Feed Biotechnology of the Ministry of Agriculture, Institute of Feed Research of Chinese Academy of Agricultural Sciences, Beijing, ChinaHunan Provincial Key Laboratory of Nutrition and Quality Control of Aquatic Animals, Department of Biological and Environmental Engineering, Changsha University, Changsha, ChinaSino-Norway Fish Gastrointestinal Microbiota Joint Lab, Institute of Feed Research of Chinese Academy of Agricultural Sciences, Beijing, ChinaFatty liver and intestinal barrier damage were widespread in most farmed fish, which severely restrict the development of aquaculture. Therefore, there was an urgent need to develop green feed additives to maintain host liver and intestinal health. In this study, a probiotic pili-like protein, Amuc_1100 (AM protein), was anchored to the surface of Lactococcus lactis ZHY1, and the effects of the recombinant bacteria AM-ZHY1 on liver fat accumulation and intestinal health were evaluated. Zebrafish were fed a basal diet, high-fat diet, and high-fat diet with AM-ZHY1 (108 cfu/g) or control bacteria ZHY1 for 4 weeks. Treatment with AM-ZHY1 significantly reduced hepatic steatosis in zebrafish. Quantitative PCR (qPCR) detection showed that the expression of the lipogenesis [peroxisome-proliferator-activated receptors (PPARγ), sterol regulatory element-binding proteins-1c (SREBP-1c), fatty acid synthase (FAS), and acetyl-CoA carboxylase 1 (ACC1)] and lipid transport genes (CD36 and FABP6) in the liver were significantly downregulated (p < 0.05), indicating that AM-ZHY1 could reduce liver fat accumulation by inhibiting lipid synthesis and absorption. Moreover, supplementing AM-ZHY1 to a high-fat diet could significantly reduce serum aspartate aminotransferase (AST) and alanine aminotransferase (ALT) levels, indicating that liver injury caused by high-fat diets was improved. The expression of tumor necrosis factor (TNF)-a and interleukin (IL)-6 in the liver decreased significantly (p < 0.05), while IL-1β and IL-10 did not change significantly in the AM-ZHY1 group. Compared to the high-fat diet-fed group, the AM-ZHY1 group, but not the ZHY1 group, significantly increased the expression of intestinal tight junction (TJ) proteins (TJP1a, claudina, claudin7, claudin7b, claudin11a, claudin12, and claudin15a; p < 0.05). Compared to the high-fat diet group, the Proteobacteria and Fusobacteria were significantly reduced and increased in the AM-ZHY1 group, respectively. In conclusion, the recombinant bacteria AM-ZHY1 has the capacity to maintain intestinal health by protecting intestinal integrity and improving intestinal flora structure and improving fatty liver disease by inhibiting lipid synthesis and absorption. This study will lay a foundation for the application of AM protein in improving abnormal fat deposition and restoring the intestinal barrier in fish.https://www.frontiersin.org/articles/10.3389/fnut.2021.726108/fullAmuc_1100Lactococcus lactisfatty liverintestinal healthmicrobiotainflammation
spellingShingle Feng-Li Zhang
Ya-Lin Yang
Zhen Zhang
Yuan-Yuan Yao
Rui Xia
Chen-Chen Gao
Dong-Dong Du
Juan Hu
Chao Ran
Zhen Liu
Zhi-Gang Zhou
Surface-Displayed Amuc_1100 From Akkermansia muciniphila on Lactococcus lactis ZHY1 Improves Hepatic Steatosis and Intestinal Health in High-Fat-Fed Zebrafish
Frontiers in Nutrition
Amuc_1100
Lactococcus lactis
fatty liver
intestinal health
microbiota
inflammation
title Surface-Displayed Amuc_1100 From Akkermansia muciniphila on Lactococcus lactis ZHY1 Improves Hepatic Steatosis and Intestinal Health in High-Fat-Fed Zebrafish
title_full Surface-Displayed Amuc_1100 From Akkermansia muciniphila on Lactococcus lactis ZHY1 Improves Hepatic Steatosis and Intestinal Health in High-Fat-Fed Zebrafish
title_fullStr Surface-Displayed Amuc_1100 From Akkermansia muciniphila on Lactococcus lactis ZHY1 Improves Hepatic Steatosis and Intestinal Health in High-Fat-Fed Zebrafish
title_full_unstemmed Surface-Displayed Amuc_1100 From Akkermansia muciniphila on Lactococcus lactis ZHY1 Improves Hepatic Steatosis and Intestinal Health in High-Fat-Fed Zebrafish
title_short Surface-Displayed Amuc_1100 From Akkermansia muciniphila on Lactococcus lactis ZHY1 Improves Hepatic Steatosis and Intestinal Health in High-Fat-Fed Zebrafish
title_sort surface displayed amuc 1100 from akkermansia muciniphila on lactococcus lactis zhy1 improves hepatic steatosis and intestinal health in high fat fed zebrafish
topic Amuc_1100
Lactococcus lactis
fatty liver
intestinal health
microbiota
inflammation
url https://www.frontiersin.org/articles/10.3389/fnut.2021.726108/full
work_keys_str_mv AT fenglizhang surfacedisplayedamuc1100fromakkermansiamuciniphilaonlactococcuslactiszhy1improveshepaticsteatosisandintestinalhealthinhighfatfedzebrafish
AT yalinyang surfacedisplayedamuc1100fromakkermansiamuciniphilaonlactococcuslactiszhy1improveshepaticsteatosisandintestinalhealthinhighfatfedzebrafish
AT zhenzhang surfacedisplayedamuc1100fromakkermansiamuciniphilaonlactococcuslactiszhy1improveshepaticsteatosisandintestinalhealthinhighfatfedzebrafish
AT yuanyuanyao surfacedisplayedamuc1100fromakkermansiamuciniphilaonlactococcuslactiszhy1improveshepaticsteatosisandintestinalhealthinhighfatfedzebrafish
AT ruixia surfacedisplayedamuc1100fromakkermansiamuciniphilaonlactococcuslactiszhy1improveshepaticsteatosisandintestinalhealthinhighfatfedzebrafish
AT chenchengao surfacedisplayedamuc1100fromakkermansiamuciniphilaonlactococcuslactiszhy1improveshepaticsteatosisandintestinalhealthinhighfatfedzebrafish
AT dongdongdu surfacedisplayedamuc1100fromakkermansiamuciniphilaonlactococcuslactiszhy1improveshepaticsteatosisandintestinalhealthinhighfatfedzebrafish
AT juanhu surfacedisplayedamuc1100fromakkermansiamuciniphilaonlactococcuslactiszhy1improveshepaticsteatosisandintestinalhealthinhighfatfedzebrafish
AT chaoran surfacedisplayedamuc1100fromakkermansiamuciniphilaonlactococcuslactiszhy1improveshepaticsteatosisandintestinalhealthinhighfatfedzebrafish
AT zhenliu surfacedisplayedamuc1100fromakkermansiamuciniphilaonlactococcuslactiszhy1improveshepaticsteatosisandintestinalhealthinhighfatfedzebrafish
AT zhigangzhou surfacedisplayedamuc1100fromakkermansiamuciniphilaonlactococcuslactiszhy1improveshepaticsteatosisandintestinalhealthinhighfatfedzebrafish