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Peer-reviewedCC BYWater Biology and Security

Integrated analysis of transcriptomics and metabolomics reveals the role of hypoxia-inducible factor HIF-1α in the regulation of pathogenic

  1. 1Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao, China; State Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
  2. 2State Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China; Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Qingdao, China
  3. 3Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao, China; Corresponding author.

Abstract

Vibriosis is one of the most prevalent and severe bacterial diseases in shrimp aquaculture. Shrimp gills are important for respiration, making them vulnerable to hypoxia, and they also serve as entry sites for pathogenic bacteria. Hypoxia-inducible factor-1 (HIF-1) is a central transcription factor in cellular oxygen sensing and regulation, however, its function in Vibrio infection remains unclear. In this study, a new gill-specific expressed HIF-1α ( LvHIFn-1α ) was identified in the Pacific white shrimp Litopenaeus vannamei . To investigate the roles of HIF-1α in Vibrio infection, LvHIFn-1α was knocked down by RNA interference (RNAi) and comparative transcriptome and metabolome analyses were conducted on gills of the LvHIFn-1α -interfered shrimp and control shrimp at 0 and 6 h after immersion infection with V. parahaemolyticus . Integrated analysis showed that knockdown of LvHIFn-1α led to remarkable dysregulation of several pathways at both transcriptional and metabolic levels, including glycolysis/gluconeogenesis, glutathione metabolism, nicotinate and nicotinamide metabolism and arachidonic acid metabolism. Most immune-related genes, such as C-type lectins, anti-lipopolysaccharide factors (ALFs) and prophenoloxidase (proPO) system-related genes, were highly expressed in the dsHIFn-1α group. After V. parahaemolyticus infection, LvHIFn-1α knockdown further exacerbated alterations in redox balance, carbohydrate metabolism and immune response of gills (dsEGFP-Vp vs dsHIFn-1α-Vp). In dsHIFn-1α-Vp group, nicotinic acid and nicotinamide metabolism and arachidonic acid metabolism were significantly upregulated, while the pentose phosphate pathway was significantly downregulated. In addition, more immune DEGs, including C-type lectins, NLRs, penaeidins, ALFs, prophenoloxidases and kazal-type proteinase inhibitors were highly expressed in the dsHIFn-1α-Vp group. Notably, key antioxidant and immune parameters, including copper/zinc superoxide dismutase (SOD), peroxidase (POD) and phenoloxidase (PO) activities, as well as total glutathione levels, were reduced in LvHIFn-1α -knockdown shrimp. Our findings suggest that knockdown of LvHIFn-1α induced oxidative damage, altered glycolysis and exacerbated inflammation in gills, thereby facilitating V. parahaemolyticus infection.

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BibTeX
@article{hu2026integrated,
  title = {{Integrated analysis of transcriptomics and metabolomics reveals the role of hypoxia-inducible factor HIF-1α in the regulation of pathogenic}},
  author = {Jie Hu and Yuan Liu and Yang Yu and Shihao Li and Guangxing Liu and Fuhua Li},
  journal = {Water Biology and Security},
  year = {2026},
  month = nov,
  doi = {10.1016/j.watbs.2026.100587},
  url = {https://doi.org/10.1016/j.watbs.2026.100587},
  note = {CC BY},
}
RIS
TY  - JOUR
TI  - Integrated analysis of transcriptomics and metabolomics reveals the role of hypoxia-inducible factor HIF-1α in the regulation of pathogenic
AU  - Jie Hu
AU  - Yuan Liu
AU  - Yang Yu
AU  - Shihao Li
AU  - Guangxing Liu
AU  - Fuhua Li
PY  - 2026
DA  - 2026/11/01
JO  - Water Biology and Security
DO  - 10.1016/j.watbs.2026.100587
UR  - https://doi.org/10.1016/j.watbs.2026.100587
AB  - Vibriosis is one of the most prevalent and severe bacterial diseases in shrimp aquaculture. Shrimp gills are important for respiration, making them vulnerable to hypoxia, and they also serve as entry sites for pathogenic bacteria. Hypoxia-inducible factor-1 (HIF-1) is a central transcription factor in cellular oxygen sensing and regulation, however, its function in Vibrio infection remains unclear. In this study, a new gill-specific expressed HIF-1α ( LvHIFn-1α ) was identified in the Pacific white shrimp Litopenaeus vannamei . To investigate the roles of HIF-1α in Vibrio infection, LvHIFn-1α was knocked down by RNA interference (RNAi) and comparative transcriptome and metabolome analyses were conducted on gills of the LvHIFn-1α -interfered shrimp and control shrimp at 0 and 6 h after immersion infection with V. parahaemolyticus . Integrated analysis showed that knockdown of LvHIFn-1α led to remarkable dysregulation of several pathways at both transcriptional and metabolic levels, including glycolysis/gluconeogenesis, glutathione metabolism, nicotinate and nicotinamide metabolism and arachidonic acid metabolism. Most immune-related genes, such as C-type lectins, anti-lipopolysaccharide factors (ALFs) and prophenoloxidase (proPO) system-related genes, were highly expressed in the dsHIFn-1α group. After V. parahaemolyticus infection, LvHIFn-1α knockdown further exacerbated alterations in redox balance, carbohydrate metabolism and immune response of gills (dsEGFP-Vp vs dsHIFn-1α-Vp). In dsHIFn-1α-Vp group, nicotinic acid and nicotinamide metabolism and arachidonic acid metabolism were significantly upregulated, while the pentose phosphate pathway was significantly downregulated. In addition, more immune DEGs, including C-type lectins, NLRs, penaeidins, ALFs, prophenoloxidases and kazal-type proteinase inhibitors were highly expressed in the dsHIFn-1α-Vp group. Notably, key antioxidant and immune parameters, including copper/zinc superoxide dismutase (SOD), peroxidase (POD) and phenoloxidase (PO) activities, as well as total glutathione levels, were reduced in LvHIFn-1α -knockdown shrimp. Our findings suggest that knockdown of LvHIFn-1α induced oxidative damage, altered glycolysis and exacerbated inflammation in gills, thereby facilitating V. parahaemolyticus infection.
SN  - 2772-7351
ER  -