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

IntroductionTuna 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 on...

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Main Authors: Ying Zou, Yanjie Zhang, Di Wu, Zhiyuan Lu, Juan Xiao, Hai Huang, Qiongyao Fu, Zhiqiang Guo
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1326247/full
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author Ying Zou
Yanjie Zhang
Di Wu
Zhiyuan Lu
Juan Xiao
Hai Huang
Qiongyao Fu
Zhiqiang Guo
author_facet Ying Zou
Yanjie Zhang
Di Wu
Zhiyuan Lu
Juan Xiao
Hai Huang
Qiongyao Fu
Zhiqiang Guo
author_sort Ying Zou
collection DOAJ
description IntroductionTuna 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.MethodsWe 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 discussionThe 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.
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spelling doaj.art-a49517a0ec1d47afa5f7879890bed64f2024-01-11T05:27:37ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-01-011410.3389/fmicb.2023.13262471326247Multi-omics analysis revealed the differences in lipid metabolism of the gut between adult and juvenile yellowfin tuna (Thunnus albacares)Ying Zou0Yanjie Zhang1Di Wu2Zhiyuan Lu3Juan Xiao4Hai Huang5Qiongyao Fu6Zhiqiang Guo7School 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, ChinaSchool 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, ChinaSchool 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, ChinaSchool 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, ChinaSchool 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, ChinaKey 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, ChinaKey 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, ChinaSchool 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, ChinaIntroductionTuna 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.MethodsWe 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 discussionThe 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.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1326247/fullThunnus albacaresgut microbiota16S rRNA sequencingmetabolometranscriptome
spellingShingle Ying Zou
Yanjie Zhang
Di Wu
Zhiyuan Lu
Juan Xiao
Hai Huang
Qiongyao Fu
Zhiqiang Guo
Multi-omics analysis revealed the differences in lipid metabolism of the gut between adult and juvenile yellowfin tuna (Thunnus albacares)
Frontiers in Microbiology
Thunnus albacares
gut microbiota
16S rRNA sequencing
metabolome
transcriptome
title Multi-omics analysis revealed the differences in lipid metabolism of the gut between adult and juvenile yellowfin tuna (Thunnus albacares)
title_full Multi-omics analysis revealed the differences in lipid metabolism of the gut between adult and juvenile yellowfin tuna (Thunnus albacares)
title_fullStr Multi-omics analysis revealed the differences in lipid metabolism of the gut between adult and juvenile yellowfin tuna (Thunnus albacares)
title_full_unstemmed Multi-omics analysis revealed the differences in lipid metabolism of the gut between adult and juvenile yellowfin tuna (Thunnus albacares)
title_short Multi-omics analysis revealed the differences in lipid metabolism of the gut between adult and juvenile yellowfin tuna (Thunnus albacares)
title_sort multi omics analysis revealed the differences in lipid metabolism of the gut between adult and juvenile yellowfin tuna thunnus albacares
topic Thunnus albacares
gut microbiota
16S rRNA sequencing
metabolome
transcriptome
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1326247/full
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