PRR-Mediated Immune Response and Intestinal Flora Profile in Soybean Meal-Induced Enteritis of Pearl Gentian Groupers, Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus♂
Pattern recognition receptors (PRRs) can recognize microbial-specific pathogen-associated molecular patterns, initiate signal cascade transduction, activate the expressions of host immunity and proinflammatory genes, and, ultimately, trigger an immune response against identified pathogens. The prese...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-02-01
|
| Series: | Frontiers in Immunology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.814479/full |
| _version_ | 1818982149744754688 |
|---|---|
| author | Wei Zhang Wei Zhang Wei Zhang Beiping Tan Beiping Tan Beiping Tan Junming Deng Junming Deng Junming Deng Qihui Yang Qihui Yang Qihui Yang Shuyan Chi Shuyan Chi Shuyan Chi Aobo Pang Aobo Pang Aobo Pang Yu Xin Yu Xin Yu Xin Yu Liu Yu Liu Yu Liu Haitao Zhang |
| author_facet | Wei Zhang Wei Zhang Wei Zhang Beiping Tan Beiping Tan Beiping Tan Junming Deng Junming Deng Junming Deng Qihui Yang Qihui Yang Qihui Yang Shuyan Chi Shuyan Chi Shuyan Chi Aobo Pang Aobo Pang Aobo Pang Yu Xin Yu Xin Yu Xin Yu Liu Yu Liu Yu Liu Haitao Zhang |
| author_sort | Wei Zhang |
| collection | DOAJ |
| description | Pattern recognition receptors (PRRs) can recognize microbial-specific pathogen-associated molecular patterns, initiate signal cascade transduction, activate the expressions of host immunity and proinflammatory genes, and, ultimately, trigger an immune response against identified pathogens. The present study focused on two outcomes of feeding pearl gentian groupers with high levels of soybean meal (SBM): (1) growth performance and (2) the intestinal environment, including tissue structure, flora profile, and immune responses. Some 720 groupers were randomly divided into three groups (n = 4): (1) controls, fed a 50% fish meal feed (FM), (2) with 20% of the FM substituted with SBM (SBM20), and (3) 40% of the FM substituted with SBM (SBM40). The fish were fed these iso-nitrogenous and iso-lipidic diets for 10 weeks. They were kept in containers with 1 m3 of water under natural light and temperature levels. The experimental results demonstrate that the SBM diets significantly degraded growth performance and intestinal physiology. Typical enteritis characteristics and immune fluctuations appeared, as reflected by the enzyme activities of total superoxide dismutase and lysozyme, and the contents of immunoglobulin M, complement 3, and complement 4. 16SrDNA high-throughput sequencing showed that the intestinal flora was significantly affected, with the abundance of harmful bacteria, such as Vibrio and Streptococcus, increasing with dietary SBM level. Based on “3 + 2” full-length transcriptome sequencing, three triggered PRRs were found in the intestine: the RIG-like receptor, NOD-like receptor, and Toll-like receptor signaling pathways. The intestinal flora variations were significantly correlated with the activation of the three PRR signaling pathways by canonical correlation analysis. These culminated in the transcriptome activation of NF-κB, IRFs, and costimulatory molecules, ultimately promoting the expressions of proinflammatory cytokines, interferons (IFNs), chemokines, and other molecules vital to the innate and/or adaptive immune responses. This study provides new information for diagnosing and preventing SBMIE in aquaculture fish. |
| first_indexed | 2024-12-20T17:42:38Z |
| format | Article |
| id | doaj.art-c0fbfe4a09a44cbe98e6946a88ba945b |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-20T17:42:38Z |
| publishDate | 2022-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-c0fbfe4a09a44cbe98e6946a88ba945b2022-12-21T19:31:04ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-02-011310.3389/fimmu.2022.814479814479PRR-Mediated Immune Response and Intestinal Flora Profile in Soybean Meal-Induced Enteritis of Pearl Gentian Groupers, Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus♂Wei Zhang0Wei Zhang1Wei Zhang2Beiping Tan3Beiping Tan4Beiping Tan5Junming Deng6Junming Deng7Junming Deng8Qihui Yang9Qihui Yang10Qihui Yang11Shuyan Chi12Shuyan Chi13Shuyan Chi14Aobo Pang15Aobo Pang16Aobo Pang17Yu Xin18Yu Xin19Yu Xin20Yu Liu21Yu Liu22Yu Liu23Haitao Zhang24Laboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, ChinaLaboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, ChinaLaboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, ChinaLaboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, ChinaLaboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, ChinaLaboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, ChinaLaboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, ChinaLaboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, ChinaPattern recognition receptors (PRRs) can recognize microbial-specific pathogen-associated molecular patterns, initiate signal cascade transduction, activate the expressions of host immunity and proinflammatory genes, and, ultimately, trigger an immune response against identified pathogens. The present study focused on two outcomes of feeding pearl gentian groupers with high levels of soybean meal (SBM): (1) growth performance and (2) the intestinal environment, including tissue structure, flora profile, and immune responses. Some 720 groupers were randomly divided into three groups (n = 4): (1) controls, fed a 50% fish meal feed (FM), (2) with 20% of the FM substituted with SBM (SBM20), and (3) 40% of the FM substituted with SBM (SBM40). The fish were fed these iso-nitrogenous and iso-lipidic diets for 10 weeks. They were kept in containers with 1 m3 of water under natural light and temperature levels. The experimental results demonstrate that the SBM diets significantly degraded growth performance and intestinal physiology. Typical enteritis characteristics and immune fluctuations appeared, as reflected by the enzyme activities of total superoxide dismutase and lysozyme, and the contents of immunoglobulin M, complement 3, and complement 4. 16SrDNA high-throughput sequencing showed that the intestinal flora was significantly affected, with the abundance of harmful bacteria, such as Vibrio and Streptococcus, increasing with dietary SBM level. Based on “3 + 2” full-length transcriptome sequencing, three triggered PRRs were found in the intestine: the RIG-like receptor, NOD-like receptor, and Toll-like receptor signaling pathways. The intestinal flora variations were significantly correlated with the activation of the three PRR signaling pathways by canonical correlation analysis. These culminated in the transcriptome activation of NF-κB, IRFs, and costimulatory molecules, ultimately promoting the expressions of proinflammatory cytokines, interferons (IFNs), chemokines, and other molecules vital to the innate and/or adaptive immune responses. This study provides new information for diagnosing and preventing SBMIE in aquaculture fish.https://www.frontiersin.org/articles/10.3389/fimmu.2022.814479/fullEpinephelus fuscoguttatus♀ × E. lanceolatus♂soybean mealintestinal florapattern recognition receptorsenteritis |
| spellingShingle | Wei Zhang Wei Zhang Wei Zhang Beiping Tan Beiping Tan Beiping Tan Junming Deng Junming Deng Junming Deng Qihui Yang Qihui Yang Qihui Yang Shuyan Chi Shuyan Chi Shuyan Chi Aobo Pang Aobo Pang Aobo Pang Yu Xin Yu Xin Yu Xin Yu Liu Yu Liu Yu Liu Haitao Zhang PRR-Mediated Immune Response and Intestinal Flora Profile in Soybean Meal-Induced Enteritis of Pearl Gentian Groupers, Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus♂ Frontiers in Immunology Epinephelus fuscoguttatus♀ × E. lanceolatus♂ soybean meal intestinal flora pattern recognition receptors enteritis |
| title | PRR-Mediated Immune Response and Intestinal Flora Profile in Soybean Meal-Induced Enteritis of Pearl Gentian Groupers, Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus♂ |
| title_full | PRR-Mediated Immune Response and Intestinal Flora Profile in Soybean Meal-Induced Enteritis of Pearl Gentian Groupers, Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus♂ |
| title_fullStr | PRR-Mediated Immune Response and Intestinal Flora Profile in Soybean Meal-Induced Enteritis of Pearl Gentian Groupers, Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus♂ |
| title_full_unstemmed | PRR-Mediated Immune Response and Intestinal Flora Profile in Soybean Meal-Induced Enteritis of Pearl Gentian Groupers, Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus♂ |
| title_short | PRR-Mediated Immune Response and Intestinal Flora Profile in Soybean Meal-Induced Enteritis of Pearl Gentian Groupers, Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus♂ |
| title_sort | prr mediated immune response and intestinal flora profile in soybean meal induced enteritis of pearl gentian groupers epinephelus fuscoguttatus♀ epinephelus lanceolatus♂ |
| topic | Epinephelus fuscoguttatus♀ × E. lanceolatus♂ soybean meal intestinal flora pattern recognition receptors enteritis |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.814479/full |
| work_keys_str_mv | AT weizhang prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT weizhang prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT weizhang prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT beipingtan prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT beipingtan prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT beipingtan prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT junmingdeng prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT junmingdeng prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT junmingdeng prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT qihuiyang prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT qihuiyang prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT qihuiyang prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT shuyanchi prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT shuyanchi prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT shuyanchi prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT aobopang prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT aobopang prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT aobopang prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT yuxin prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT yuxin prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT yuxin prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT yuliu prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT yuliu prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT yuliu prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus AT haitaozhang prrmediatedimmuneresponseandintestinalfloraprofileinsoybeanmealinducedenteritisofpearlgentiangroupersepinephelusfuscoguttatusepinepheluslanceolatus |