Exploring Disparities in Gill Physiological Responses to NaHCO<sub>3</sub>-Induced Habitat Stress in Triploid and Diploid Crucian Carp (<i>Carassius auratus</i>): A Comprehensive Investigation Through Multi-Omics and Biochemical Analyses
<b>Background</b>: Owing to the progressive rise in saline waters globally, resulting in detrimental impacts on freshwater aquaculture, the underlying molecular distinctions governing the response to alkaline stress between diploid and triploid crucian carp remain unknown. <b>Metho...
Saved in:
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2024-12-01
|
| Series: | Metabolites |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2218-1989/15/1/5 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1832587976443428864 |
|---|---|
| author | Shicheng Han Lin Han Fangying Yuan Wenzhi Liu Jing Wang Xiaofeng Jin Yanchun Sun |
| author_facet | Shicheng Han Lin Han Fangying Yuan Wenzhi Liu Jing Wang Xiaofeng Jin Yanchun Sun |
| author_sort | Shicheng Han |
| collection | DOAJ |
| description | <b>Background</b>: Owing to the progressive rise in saline waters globally, resulting in detrimental impacts on freshwater aquaculture, the underlying molecular distinctions governing the response to alkaline stress between diploid and triploid crucian carp remain unknown. <b>Methods</b>: This investigation explores the effects of 20 and 60 mmol NaHCO<sub>3</sub> stress over 30 days on the gills of diploid and triploid crucian carp, employing histological, biochemical, and multi-omic analyses. <b>Results</b>: Findings reveal structural damage to gill lamellas in the examined tissue. Diploid crucian carp exhibit heightened activities of superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GSH-Px), and alkaline phosphatase (AKP), alongside lower malondialdehyde (MDA) and urea nitrogen (BUN) levels compared to triploid counterparts. Metabolomic investigations suggest alterations in purine metabolism, lipid metabolism, sphingolipid metabolism, and aminoglycan and nucleotide sugar metabolism following NaHCO<sub>3</sub> exposure. Transcriptomic data indicate differential expression of genes associated with nitrogen metabolism, complement and coagulation cascades, IL-17 signaling pathways, and Toll-like receptor signaling pathways. <b>Conclusions</b>: Overall, NaHCO<sub>3</sub>-induced stress leads to significant gill tissue damage, accompanied by reactive oxygen species (ROS) production causing oxidative stress and disruptions in lipid metabolism in crucian carp. Furthermore, an inflammatory response in gill cells triggers an immune response. Diploid crucian carp exhibit superior antioxidant and immune capacities compared to triploid counterparts, while also displaying reduced inflammatory responses in vivo. Notably, diploid carp efficiently excrete excess BUN through purine metabolism, mitigating protein metabolism and amino acid imbalances caused by BUN accumulation. This enables them to allocate less energy for coping with external environmental stress, redirecting surplus energy toward growth and development. The above results indicate that diploid organisms can better adapt to saline–alkaline environments. Overall, this study provides novel perspectives into species selection of crucian carp of different ploidy in saline–alkaline waters. |
| format | Article |
| id | doaj-art-207c70ac493a42cb8d304f1d83797a0b |
| institution | Kabale University |
| issn | 2218-1989 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Metabolites |
| spelling | doaj-art-207c70ac493a42cb8d304f1d83797a0b2025-01-24T13:41:08ZengMDPI AGMetabolites2218-19892024-12-01151510.3390/metabo15010005Exploring Disparities in Gill Physiological Responses to NaHCO<sub>3</sub>-Induced Habitat Stress in Triploid and Diploid Crucian Carp (<i>Carassius auratus</i>): A Comprehensive Investigation Through Multi-Omics and Biochemical AnalysesShicheng Han0Lin Han1Fangying Yuan2Wenzhi Liu3Jing Wang4Xiaofeng Jin5Yanchun Sun6Laboratory of Quality & Safety Risk Assessment for Aquatic Products (Harbin), Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, ChinaLaboratory of Quality & Safety Risk Assessment for Aquatic Products (Harbin), Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, ChinaLaboratory of Quality & Safety Risk Assessment for Aquatic Products (Harbin), Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, ChinaLaboratory of Quality & Safety Risk Assessment for Aquatic Products (Harbin), Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, ChinaDepartment of Chemical Engineering and Technology, College of Materials and Chemical Engineering, Harbin University of Science and Technology, Harbin 150080, ChinaLaboratory of Quality & Safety Risk Assessment for Aquatic Products (Harbin), Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, ChinaLaboratory of Quality & Safety Risk Assessment for Aquatic Products (Harbin), Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, China<b>Background</b>: Owing to the progressive rise in saline waters globally, resulting in detrimental impacts on freshwater aquaculture, the underlying molecular distinctions governing the response to alkaline stress between diploid and triploid crucian carp remain unknown. <b>Methods</b>: This investigation explores the effects of 20 and 60 mmol NaHCO<sub>3</sub> stress over 30 days on the gills of diploid and triploid crucian carp, employing histological, biochemical, and multi-omic analyses. <b>Results</b>: Findings reveal structural damage to gill lamellas in the examined tissue. Diploid crucian carp exhibit heightened activities of superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GSH-Px), and alkaline phosphatase (AKP), alongside lower malondialdehyde (MDA) and urea nitrogen (BUN) levels compared to triploid counterparts. Metabolomic investigations suggest alterations in purine metabolism, lipid metabolism, sphingolipid metabolism, and aminoglycan and nucleotide sugar metabolism following NaHCO<sub>3</sub> exposure. Transcriptomic data indicate differential expression of genes associated with nitrogen metabolism, complement and coagulation cascades, IL-17 signaling pathways, and Toll-like receptor signaling pathways. <b>Conclusions</b>: Overall, NaHCO<sub>3</sub>-induced stress leads to significant gill tissue damage, accompanied by reactive oxygen species (ROS) production causing oxidative stress and disruptions in lipid metabolism in crucian carp. Furthermore, an inflammatory response in gill cells triggers an immune response. Diploid crucian carp exhibit superior antioxidant and immune capacities compared to triploid counterparts, while also displaying reduced inflammatory responses in vivo. Notably, diploid carp efficiently excrete excess BUN through purine metabolism, mitigating protein metabolism and amino acid imbalances caused by BUN accumulation. This enables them to allocate less energy for coping with external environmental stress, redirecting surplus energy toward growth and development. The above results indicate that diploid organisms can better adapt to saline–alkaline environments. Overall, this study provides novel perspectives into species selection of crucian carp of different ploidy in saline–alkaline waters.https://www.mdpi.com/2218-1989/15/1/5crucian carp (<i>Carassius auratus</i>)diploidtriploidcarbonate alkalinitymetabolomicstranscriptomics |
| spellingShingle | Shicheng Han Lin Han Fangying Yuan Wenzhi Liu Jing Wang Xiaofeng Jin Yanchun Sun Exploring Disparities in Gill Physiological Responses to NaHCO<sub>3</sub>-Induced Habitat Stress in Triploid and Diploid Crucian Carp (<i>Carassius auratus</i>): A Comprehensive Investigation Through Multi-Omics and Biochemical Analyses Metabolites crucian carp (<i>Carassius auratus</i>) diploid triploid carbonate alkalinity metabolomics transcriptomics |
| title | Exploring Disparities in Gill Physiological Responses to NaHCO<sub>3</sub>-Induced Habitat Stress in Triploid and Diploid Crucian Carp (<i>Carassius auratus</i>): A Comprehensive Investigation Through Multi-Omics and Biochemical Analyses |
| title_full | Exploring Disparities in Gill Physiological Responses to NaHCO<sub>3</sub>-Induced Habitat Stress in Triploid and Diploid Crucian Carp (<i>Carassius auratus</i>): A Comprehensive Investigation Through Multi-Omics and Biochemical Analyses |
| title_fullStr | Exploring Disparities in Gill Physiological Responses to NaHCO<sub>3</sub>-Induced Habitat Stress in Triploid and Diploid Crucian Carp (<i>Carassius auratus</i>): A Comprehensive Investigation Through Multi-Omics and Biochemical Analyses |
| title_full_unstemmed | Exploring Disparities in Gill Physiological Responses to NaHCO<sub>3</sub>-Induced Habitat Stress in Triploid and Diploid Crucian Carp (<i>Carassius auratus</i>): A Comprehensive Investigation Through Multi-Omics and Biochemical Analyses |
| title_short | Exploring Disparities in Gill Physiological Responses to NaHCO<sub>3</sub>-Induced Habitat Stress in Triploid and Diploid Crucian Carp (<i>Carassius auratus</i>): A Comprehensive Investigation Through Multi-Omics and Biochemical Analyses |
| title_sort | exploring disparities in gill physiological responses to nahco sub 3 sub induced habitat stress in triploid and diploid crucian carp i carassius auratus i a comprehensive investigation through multi omics and biochemical analyses |
| topic | crucian carp (<i>Carassius auratus</i>) diploid triploid carbonate alkalinity metabolomics transcriptomics |
| url | https://www.mdpi.com/2218-1989/15/1/5 |
| work_keys_str_mv | AT shichenghan exploringdisparitiesingillphysiologicalresponsestonahcosub3subinducedhabitatstressintriploidanddiploidcruciancarpicarassiusauratusiacomprehensiveinvestigationthroughmultiomicsandbiochemicalanalyses AT linhan exploringdisparitiesingillphysiologicalresponsestonahcosub3subinducedhabitatstressintriploidanddiploidcruciancarpicarassiusauratusiacomprehensiveinvestigationthroughmultiomicsandbiochemicalanalyses AT fangyingyuan exploringdisparitiesingillphysiologicalresponsestonahcosub3subinducedhabitatstressintriploidanddiploidcruciancarpicarassiusauratusiacomprehensiveinvestigationthroughmultiomicsandbiochemicalanalyses AT wenzhiliu exploringdisparitiesingillphysiologicalresponsestonahcosub3subinducedhabitatstressintriploidanddiploidcruciancarpicarassiusauratusiacomprehensiveinvestigationthroughmultiomicsandbiochemicalanalyses AT jingwang exploringdisparitiesingillphysiologicalresponsestonahcosub3subinducedhabitatstressintriploidanddiploidcruciancarpicarassiusauratusiacomprehensiveinvestigationthroughmultiomicsandbiochemicalanalyses AT xiaofengjin exploringdisparitiesingillphysiologicalresponsestonahcosub3subinducedhabitatstressintriploidanddiploidcruciancarpicarassiusauratusiacomprehensiveinvestigationthroughmultiomicsandbiochemicalanalyses AT yanchunsun exploringdisparitiesingillphysiologicalresponsestonahcosub3subinducedhabitatstressintriploidanddiploidcruciancarpicarassiusauratusiacomprehensiveinvestigationthroughmultiomicsandbiochemicalanalyses |