The impact of crowding stress on growth and intestinal integrity in largemouth bass (Micropterus salmoides): Insights into ER stress, autophagy and apoptosis

Dadong Yan; Lei Gan; Xianghong Dong; Huaimao Tie; Chao Luo; Zhenlu Wang; Haibo Jiang; Jiangfeng Chen; Miao An; Chuanjie Qin; Zhiyuan Lu

doi:10.1016/j.fsi.2024.109955

The impact of crowding stress on growth and intestinal integrity in largemouth bass (Micropterus salmoides): Insights into ER stress, autophagy and apoptosis

Fish Shellfish Immunol. 2024 Oct 8:109955. doi: 10.1016/j.fsi.2024.109955. Online ahead of print.

Authors

Dadong Yan¹, Lei Gan², Xianghong Dong¹, Huaimao Tie³, Chao Luo⁴, Zhenlu Wang¹, Haibo Jiang⁵, Jiangfeng Chen¹, Miao An¹, Chuanjie Qin⁶, Zhiyuan Lu⁷

Affiliations

¹ Breeding and Reproduction in The Plateau Mountainous Region, Ministry of Education (Guizhou University), Guiyang 550025, China; College of Animal Science, Guizhou University, Guiyang 550025, China.
² Breeding and Reproduction in The Plateau Mountainous Region, Ministry of Education (Guizhou University), Guiyang 550025, China; College of Animal Science, Guizhou University, Guiyang 550025, China. Electronic address: lgan3@gzu.edu.cn.
³ College of Liquor and Food Engineering, Guizhou University, Guiyang, 550025, China.
⁴ College of Forestry, Guizhou University, Guiyang 550025, China.
⁵ Breeding and Reproduction in The Plateau Mountainous Region, Ministry of Education (Guizhou University), Guiyang 550025, China; College of Animal Science, Guizhou University, Guiyang 550025, China. Electronic address: jhb99412@126.com.
⁶ Key Laboratory of Sichuan Province for Fishes Conservation and Utilization in the Upper Reaches of the Yangtze River, Neijiang Normal University, Neijiang, 641112, China.
⁷ School of Marine Science and Engineering, Hainan University, Haikou, 570228, China; State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, 570228, China.

PMID: 39389174
DOI: 10.1016/j.fsi.2024.109955

Abstract

Crowding stress is a common abiotic stressor in intensive aquaculture that negatively impacts fish species, leading to growth depression. This study primarily explored the effects of crowding stress on the growth and intestinal integrity of largemouth bass (Micropterus salmoides). A 10-week feeding experiment was conducted with two groups: a control group (0.55 kg/m³) and a crowding stress group (1.10 kg/m³). The results showed that crowding stress significantly impaired fish growth and compromised intestinal integrity. To further elucidate the underlying mechanisms, we investigated the effects of crowding stress on endoplasmic reticulum (ER) stress, autophagy and apoptosis. Our findings revealed an increased proportion of terminal deoxynucleotidyl transferase (TdT) dUTP Nick-End Labeling (TUNEL)-positive cells and ER swelling in the intestines of stressed fish, along with a higher number of autophagosomes. Furthermore, there was a significant upregulation in the mRNA expression of genes related to ER stress, autophagy and apoptosis, including GRP78, eIF2α, IRE1, atg3, LC3-2, ulk1α, P62, and caspase-8. In conclusion, crowding stress negatively affects fish growth and intestinal integrity, potentially through the induction of apoptosis and autophagy associated with ER stress-mediated unfolded protein response (UPR). These findings provided critical insights into how intensive aquaculture disrupts intestinal integrity and inhibits growth in fish, offering a valuable reference for future research aimed at enhancing stress resistance in fish under intensive aquaculture conditions.

Keywords: Autophagy; ER stress; Intestinal integrity; TUNEL; UPR.