Multi-omics analysis revealed the differences in lipid metabolism of the gut between adult and juvenile yellowfin tuna (Thunnus albacares)

Ying Zou; Yanjie Zhang; Di Wu; Zhiyuan Lu; Juan Xiao; Hai Huang; Qiongyao Fu; Zhiqiang Guo

doi:10.3389/fmicb.2023.1326247

Multi-omics analysis revealed the differences in lipid metabolism of the gut between adult and juvenile yellowfin tuna (Thunnus albacares)

Front Microbiol. 2024 Jan 11:14:1326247. doi: 10.3389/fmicb.2023.1326247. eCollection 2023.

Authors

Ying Zou¹, Yanjie Zhang¹, Di Wu¹, Zhiyuan Lu¹, Juan Xiao¹, Hai Huang², Qiongyao Fu³, Zhiqiang Guo¹

Affiliations

¹ School of Life and Health Sciences, School of Marine Science and Engineering, School of Food Science and Engineering, State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China.
² Key Laboratory of Utilization and Conservation for Tropical Marine Bioresources, Hainan Key Laboratory for Conservation and Utilization of Tropical Marine Fishery Resources, College of Fisheries and Life Science, Hainan Tropical Ocean University, Sanya, China.
³ Key Laboratory of Tropical Translational Medicine of Ministry of Education, NHC Key Laboratory of Control of Tropical Diseases, School of Tropical Medicine, Hainan Medical University, Haikou, Hainan, China.

Abstract

Introduction: Tuna has a cost-effective energy supply to support the regional endothermic and high-speed swimming performance. The gut symbiotic microbiotas and their metabolites play essential roles in tuna's diet digestion, absorption, and energy acquirement, which are often highly related to the ontogenetic development of tuna.

Methods: We compared gut microbial compositions and metabolites, as well as mRNA expression of the intestine between juvenile and adult yellowfin tuna using 16S rRNA sequencing, metabolomic and transcriptomic, respectively.

Results and discussion: The results revealed that adults had a significantly higher microbial diversity and abundance of Acinetobacter than juveniles. Regarding the gut microbiota-derived metabolites, fatty acids, especially glycerophospholipid and sphingolipid, were significantly enriched in adults than in juveniles. Moreover, the short-chain fatty acid (butyrate and isobutyrate) contents were significantly higher in adults than in juveniles. To find the relationship between gut microbiotas and host physiology, intestinal transcriptome analysis demonstrated that the enriched pathways of differential expression genes (DEGs) in adult tuna were the lipid metabolism pathway, including "fat digestion and absorption," "cholesterol metabolism," "steroid hormone biosynthesis," "glycerolipid metabolism," and "glycerophospholipid metabolism." However, protein digestion and absorption and pancreatic secretion pathways were significantly enriched in the juveniles. The conjoint analysis indicated that the enriched pathways of both differential metabolites (DMs) and DEGs were remarkably related to the regulation of glycerophospholipids metabolism in adult tunas. This study highlights the role of gut microbiotas in fish nutrition metabolism. These findings provide new insights into the view of ontogenetic shifts of gut microbiotas and their metabolites on host health and gut function in endothermic and high-speed swimming marine fish species.

Keywords: 16S rRNA sequencing; Thunnus albacares; gut microbiota; metabolome; transcriptome.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by the Opening Foundation of Hainan Tropical Ocean University & Yazhouwan Innovation Research Institute (2022RHDKFKT03), the Modern Agricultural Industry Technology System of Grouper in Hainan Province (HNARS2022-3-G4 and HNARS2022-3), and the Hainan University Research Start-up Fund Project (KYQD(ZR)23175).