Dietary supplementation with probiotics regulates gut microbiota structure and function in Nile tilapia exposed to aluminum

Leilei Yu; Nanzhen Qiao; Tianqi Li; Ruipeng Yu; Qixiao Zhai; Fengwei Tian; Jianxin Zhao; Hao Zhang; Wei Chen

doi:10.7717/peerj.6963

Dietary supplementation with probiotics regulates gut microbiota structure and function in Nile tilapia exposed to aluminum

PeerJ. 2019 Jun 3:7:e6963. doi: 10.7717/peerj.6963. eCollection 2019.

Authors

Leilei Yu^{1

2

3}, Nanzhen Qiao^{1

2}, Tianqi Li^{1

2

3}, Ruipeng Yu², Qixiao Zhai^{1

2

3}, Fengwei Tian^{1

2

3}, Jianxin Zhao^{1

2}, Hao Zhang^{1

2

4

5}, Wei Chen^{1

2

4

6}

Affiliations

¹ School of Food Science and Technology, Jiangnan University, Wuxi, China.
² State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, China.
³ International Joint Research Laboratory for Probiotics, Jiangnan University, Wuxi, China.
⁴ National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, China.
⁵ (Yangzhou) Institute of Food Biotechnology, Jiangnan University, Yangzhou, China.
⁶ Beijing Innovation Centre of Food Nutrition and Human Health, Beijing Technology & Business University, Beijing, China.

Abstract

Backgrounds and aims: Aluminum contamination of water is becoming increasingly serious and threatens the health status of fish. Lactobacillus plantarum CCFM639 was previously shown to be a potential probiotic for alleviation aluminum toxicity in Nile tilapia. Considering the significant role of the gut microbiota on fish health, it seems appropriate to explore the relationships among aluminum exposure, probiotic supplementation, and the gut microbiota in Nile tilapia and to determine whether regulation of the gut microbiota is related to alleviation of aluminum toxicity by a probiotic in Nile tilapia.

Methods and results: The tilapia were assigned into four groups, control, CCFM639 only, aluminum only, and aluminum + CCFM639 groups for an experimental period of 4 weeks. The tilapia in the aluminum only group were grown in water with an aluminum ion concentration of 2.73 mg/L. The final concentration of CCFM639 in the diet was 10⁸ CFU/g. The results show that environmental aluminum exposure reduced the numbers of L. plantarum in tilapia feces and altered the gut microbiota. As the predominant bacterial phyla in the gut, the abundances of Bacteroidetes and Proteobacteria in aluminum-exposed fish were significantly elevated and lowered, respectively. At the genus level, fish exposed to aluminum had a significantly lower abundance of Deefgea, Plesiomonas, and Pseudomonas and a greater abundance of Flavobacterium, Enterovibrio, Porphyromonadaceae uncultured, and Comamonadaceae. When tilapia were exposed to aluminum, the administration of a probiotic promoted aluminum excretion through the feces and led to a decrease in the abundance of Comamonadaceae, Enterovibrio and Porphyromonadaceae. Notably, supplementation with a probiotic only greatly decreased the abundance of Aeromonas and Pseudomonas.

Conclusion: Aluminum exposure altered the diversity of the gut microbiota in Nile tilapia, and probiotic supplementation allowed the recovery of some of the diversity. Therefore, regulation of gut microbiota with a probiotic is a possible mechanism for the alleviation of aluminum toxicity in Nile tilapia.

Keywords: Aluminum; Aquaculture; Gut microbiota; Lactobacillus plantarum; Nile tilapia; Probiotic.

Grants and funding

This work was supported by the Natural Science Foundation of Jiangsu Province (BK20180603), the National Natural Science Foundation of China Key Program (No. 31530056, 31772090, 31601452), the Postdoctoral Science Foundation of China (2018M642166), the General Financial Grant from the Jiangsu Postdoctoral Science Foundation (2018K016A), the Self-determined Research Program of Jiangnan University (JUSRP11847), BBSRC Newton Fund Joint Centre Award, the National First-Class Discipline Program of Food Science and Technology (JUFSTR20180102), and the Collaborative Innovation Center of Food Safety and Quality Control in Jiangsu Province. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.