Co-occurrence network of microbes linking growth and immunity parameters with the gut microbiota in Nile tilapia (Oreochromis niloticus) after feeding with fermented soybean meal

The supplementation of fish feed with fermented soybean meal (FSBM) as an additive is widely used to produce aquatic feed. However, the mechanism by which FSBM regulates gut microbes in fish are still largely unknown. In the present work, soybean meal fermented by Lactobacillus fermentum (Lactobacil...

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Main Authors: Lu Li, Jingjing Song, Chunyan Peng, Zicong Yang, Lin Wang, Juncheng Lin, Liangbo Li, Zhicheng Huang, Bin Gong
Format: Article
Language:English
Published: Elsevier 2022-10-01
Series:Aquaculture Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2352513422002769
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author Lu Li
Jingjing Song
Chunyan Peng
Zicong Yang
Lin Wang
Juncheng Lin
Liangbo Li
Zhicheng Huang
Bin Gong
author_facet Lu Li
Jingjing Song
Chunyan Peng
Zicong Yang
Lin Wang
Juncheng Lin
Liangbo Li
Zhicheng Huang
Bin Gong
author_sort Lu Li
collection DOAJ
description The supplementation of fish feed with fermented soybean meal (FSBM) as an additive is widely used to produce aquatic feed. However, the mechanism by which FSBM regulates gut microbes in fish are still largely unknown. In the present work, soybean meal fermented by Lactobacillus fermentum (Lactobacillus group), Bacillus natto (Bacillus group), and Saccharomyces cerevisiae (Saccharomyces group) was added to fish diets, and the effects of these diets on gut microbiota, growth performance [Weight gain rate (WGR) and Specific growth rate (SGR)], and immunity [superoxide dismutase (SOD), lysozyme (LSZ) and alkaline phosphatase (AKP)] of Nile tilapia was assessed. Compared with Nontreated group, Lactobacillus and Saccharomyces fermented soybean meal remarkably improved the WGR, SGR, AKP, and LSZ (p < 0.05). The SOD activity was significantly lower in Bacillus group than other groups (p < 0.05). High-throughput sequencing of the V3-V4 region of the 16S rRNA gene was used to analyze the gut microbiota of Nile tilapia. PCoA and UPGMA showed that the similarity between the Saccharomyces and Lactobacillus groups was higher. Compared with Nontreated group, Lactobacillus fermented soybean meal significantly increased the Chao1 index and number of observed species (p < 0.05), while Bacillus fermented soybean meal remarkably improved the Simpson and Shannon indices (p < 0.01). Corynebacterium and Mycobacterium were significantly enriched in the Saccharomyces and Lactobacillus groups, and Aquabacterium and Acidovorax were significantly enriched in the Bacillus group. LEfSe analysis showed that Rhizobiales, Thermomicrobia, Myxococcales and Gemmatales were the biomarker in Lactobacillus group, Mycobacterium, Clavibacter and Coxiellaceae were the biomarker in Saccharomyces group, and Brevundimonas and Aquabacterium were the biomarker in Bacillus group. More interestingly, the co-occurrence network indicated that fish diets supplemented with L. fermentum or S. cerevisiae fermented soybean meal were more likely to impact some species that played pivotal roles in the network. L. fermentum- or S. cerevisiae- fermented SBM tended to activate similar “big team” species and promote their cooperation to perform certain functions. This research showed that FSBM fermented by L. fermentum, B. natto, and S. cerevisiae exerted different effect on growth, immunity, and gut microbiota of Nile tilapia, and the co-occurrence network of the microbiota could partially explain the relationship between the growth performance and immune parameters and the microbiomic data.
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spelling doaj.art-89c24732e6d243b0bd8765fce9abf54b2022-12-22T03:13:45ZengElsevierAquaculture Reports2352-51342022-10-0126101280Co-occurrence network of microbes linking growth and immunity parameters with the gut microbiota in Nile tilapia (Oreochromis niloticus) after feeding with fermented soybean mealLu Li0Jingjing Song1Chunyan Peng2Zicong Yang3Lin Wang4Juncheng Lin5Liangbo Li6Zhicheng Huang7Bin Gong8The Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, College of Marine Sciences, Beibu Gulf University, Qinzhou 535011, ChinaThe Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, College of Marine Sciences, Beibu Gulf University, Qinzhou 535011, ChinaThe Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, College of Marine Sciences, Beibu Gulf University, Qinzhou 535011, ChinaThe Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, College of Marine Sciences, Beibu Gulf University, Qinzhou 535011, ChinaThe Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, College of Marine Sciences, Beibu Gulf University, Qinzhou 535011, ChinaThe Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, College of Marine Sciences, Beibu Gulf University, Qinzhou 535011, ChinaGuangxi Aohua Agriculture and Animal Husbandry Technology Co., Ltd., Qinzhou 535011, ChinaHuobaoyuan Biotechnology Co., Ltd., Foshan 528000, ChinaThe Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, College of Marine Sciences, Beibu Gulf University, Qinzhou 535011, China; Corresponding author.The supplementation of fish feed with fermented soybean meal (FSBM) as an additive is widely used to produce aquatic feed. However, the mechanism by which FSBM regulates gut microbes in fish are still largely unknown. In the present work, soybean meal fermented by Lactobacillus fermentum (Lactobacillus group), Bacillus natto (Bacillus group), and Saccharomyces cerevisiae (Saccharomyces group) was added to fish diets, and the effects of these diets on gut microbiota, growth performance [Weight gain rate (WGR) and Specific growth rate (SGR)], and immunity [superoxide dismutase (SOD), lysozyme (LSZ) and alkaline phosphatase (AKP)] of Nile tilapia was assessed. Compared with Nontreated group, Lactobacillus and Saccharomyces fermented soybean meal remarkably improved the WGR, SGR, AKP, and LSZ (p < 0.05). The SOD activity was significantly lower in Bacillus group than other groups (p < 0.05). High-throughput sequencing of the V3-V4 region of the 16S rRNA gene was used to analyze the gut microbiota of Nile tilapia. PCoA and UPGMA showed that the similarity between the Saccharomyces and Lactobacillus groups was higher. Compared with Nontreated group, Lactobacillus fermented soybean meal significantly increased the Chao1 index and number of observed species (p < 0.05), while Bacillus fermented soybean meal remarkably improved the Simpson and Shannon indices (p < 0.01). Corynebacterium and Mycobacterium were significantly enriched in the Saccharomyces and Lactobacillus groups, and Aquabacterium and Acidovorax were significantly enriched in the Bacillus group. LEfSe analysis showed that Rhizobiales, Thermomicrobia, Myxococcales and Gemmatales were the biomarker in Lactobacillus group, Mycobacterium, Clavibacter and Coxiellaceae were the biomarker in Saccharomyces group, and Brevundimonas and Aquabacterium were the biomarker in Bacillus group. More interestingly, the co-occurrence network indicated that fish diets supplemented with L. fermentum or S. cerevisiae fermented soybean meal were more likely to impact some species that played pivotal roles in the network. L. fermentum- or S. cerevisiae- fermented SBM tended to activate similar “big team” species and promote their cooperation to perform certain functions. This research showed that FSBM fermented by L. fermentum, B. natto, and S. cerevisiae exerted different effect on growth, immunity, and gut microbiota of Nile tilapia, and the co-occurrence network of the microbiota could partially explain the relationship between the growth performance and immune parameters and the microbiomic data.http://www.sciencedirect.com/science/article/pii/S2352513422002769Lactobacillus fermentumBacillus nattoSaccharomyces cerevisiaeIntestinal tractMicrobial communityHigh-throughput sequencing
spellingShingle Lu Li
Jingjing Song
Chunyan Peng
Zicong Yang
Lin Wang
Juncheng Lin
Liangbo Li
Zhicheng Huang
Bin Gong
Co-occurrence network of microbes linking growth and immunity parameters with the gut microbiota in Nile tilapia (Oreochromis niloticus) after feeding with fermented soybean meal
Aquaculture Reports
Lactobacillus fermentum
Bacillus natto
Saccharomyces cerevisiae
Intestinal tract
Microbial community
High-throughput sequencing
title Co-occurrence network of microbes linking growth and immunity parameters with the gut microbiota in Nile tilapia (Oreochromis niloticus) after feeding with fermented soybean meal
title_full Co-occurrence network of microbes linking growth and immunity parameters with the gut microbiota in Nile tilapia (Oreochromis niloticus) after feeding with fermented soybean meal
title_fullStr Co-occurrence network of microbes linking growth and immunity parameters with the gut microbiota in Nile tilapia (Oreochromis niloticus) after feeding with fermented soybean meal
title_full_unstemmed Co-occurrence network of microbes linking growth and immunity parameters with the gut microbiota in Nile tilapia (Oreochromis niloticus) after feeding with fermented soybean meal
title_short Co-occurrence network of microbes linking growth and immunity parameters with the gut microbiota in Nile tilapia (Oreochromis niloticus) after feeding with fermented soybean meal
title_sort co occurrence network of microbes linking growth and immunity parameters with the gut microbiota in nile tilapia oreochromis niloticus after feeding with fermented soybean meal
topic Lactobacillus fermentum
Bacillus natto
Saccharomyces cerevisiae
Intestinal tract
Microbial community
High-throughput sequencing
url http://www.sciencedirect.com/science/article/pii/S2352513422002769
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