Hypoxia Stress Induces Tissue Damage, Immune Defense, and Oxygen Transport Change in Gill of Silver Carp (Hypophthalmichthys molitrix): Evaluation on Hypoxia by Using Transcriptomics

Abstract

The silver carp (Hypophthalmichthys molitrix) is an economically, as well as environmentally, important fish that harbors low environmental hypoxia tolerance and frequently contributes to a loss of aquaculture productivity. The gill is the first tissue attacked by hypoxia; however, the response of the gills of H. molitrix to hypoxia stress at the tissue, cellular, and molecular levels has not been clearly established. The influence of hypoxia on histological features along with gene expression in silver carp gills were explored in this research. The hematoxylin and eosin-stained sections and electron microscopy examinations of gills indicated that the gill lamellae were seriously twisted, gill filaments were dehisced, and the swelling and shedding of epithelial cell layer in the gill tissue were intensified along with the degree of hypoxia. In the hypoxia, semi-asphyxia, and asphyxia groups, the gill transcriptomic assessment of shifts in key genes, as well as modulatory networks in response to hypoxic conditions revealed 587, 725, and 748 differentially expressed genes, respectively. These genes are abundant in immune response signaling cascades (e.g., complement and coagulation cascades, Nucleotide-binding and oligomerization domain (NOD)-like receptor signaling cascade, and differentiation of Th1 along with Th2 cells) and oxygen transport [e.g., MAPK, PI3K-Akt, and hypoxia-inducible factor 1 (HIF-1) signaling cascades]. Genes linked to immune response (e.g., c2, c3, c6, klf4, cxcr4, cd45, and cd40) and oxygen transport (e.g., egln1, egln3, epo, ldh, and vegfa) were additionally identified. According to our findings, the silver carp may be using “HIF-1” to obtain additional oxygen during hypoxia. These findings illustrate that hypoxia stress might damage gill tissue, trigger an immunological response, and activate HIF-1 signaling to increase oxygen availability under hypoxic situations. The findings of this work will help scientists better understand the molecular mechanisms driving hypoxia responses in hypoxia-sensitive fish and speed up the development of hypoxia-resistant varieties.

A high-quality chromosome-level genome assembly of Pelteobagrus vachelli provides insights into its environmental adaptation and population history

“…KEGG analysis showed that 14 pathways were significantly enriched (FDR <0.05), which were mainly involved in carbohydrate metabolism, endocrine system, endocrine and metabolic disease ( Supplementary Table S8 ). Notably, the HIF-1 signaling pathway, a key pathway in the hypoxia response, was also significantly enriched ( Li et al, 2022 ). In high temperature stress transcriptome, 18,832 unique genes were identified from six DNA libraries (WC1, WC2, WC3, WT1, WT2, WT3), including 2,718 DEGs (foldchange >2, p < 0.05).…”

“…The mapping rate, coverage, and sequencing depth of the filtered data were analyzed. We further filtered the calls using GATK VariantFiltration (Lin et al, 2022) with the following parameters: QD < 2.0, FS > 60.0, MQ < 40.0, MQRankSum < −12.5, ReadPosRankSum < −8.0. Mutational positions, genomic regions, and potential amino acid changes were assessed using ANNOVAR (v2019).…”

Gill disorders in fish: Lessons from poxvirus infections

“…However, the need for this type of intervention (e.g., increased aeration or oxygenation) may be greater in fish species with higher oxygen requirements (e.g., salmonids). Furthermore, it is worth noting that exposure of both, oxygen sensitive salmonids 95 and less oxygen sensitive cyprinids 96 or pike perch 97 to hypoxia modulates immune responses and reduces or delays them. For example, during peritonitis hypoxia impaired the influx of lymphocytes to the peritoneal niche in the later phases of the immune reaction in pikeperch while pro‐inflammatory immune responses manifested as mobilisation of myeloid cells, and expression of pro‐inflammatory mediators was less severely affected 97 …”

Acute Hypoxia Stress-Induced Apoptosis in Gill of Japanese Flounder (Paralichthys olivaceus) by Modulating the Epas1/Bad Pathway

“…Fish gills acted as an important role in physiological functions including gaseous exchange, osmoregulation, acid–base regulation, excretion of nitrogenous waste, and hormone production [ 3 , 4 ]. Gills are also the main organs that respond to the change in dissolved oxygen in the aquatic environment [ 5 ]. It was reported that the morphological structures of gills in many fish showed significant changes during hypoxia [ 6 ].…”