Transcriptome and 16S rRNA Analyses Reveal That Hypoxic Stress Affects the Antioxidant Capacity of Largemouth Bass (Micropterus salmoides), Resulting in Intestinal Tissue Damage and Structural Changes in Microflora

Abstract

Dissolved oxygen (DO) is a key factor affecting the health of aquatic organisms in an intensive aquaculture environment. In this study, largemouth bass (Micropterus salmoides) were subjected to acute hypoxic stress for 96 h (DO: 1.00 mg/L) followed by recovery under sufficient DO conditions (DO: 7.50 mg/L) for 96 h. Serum biochemical indices, intestinal histomorphology, the transcriptome, and intestinal microbiota were compared between hypoxia-treated fish and those in a control group. The results showed that hypoxia caused oxidative stress, exfoliation of the intestinal villus epithelium and villus rupture, and increased cell apoptosis. Transcriptome analyses revealed that antioxidant-, inflammation-, and apoptosis-related pathways were activated, and that the MAPK signaling pathway played an important role under hypoxic stress. In addition, 16S rRNA sequencing analyses revealed that hypoxic stress significantly decreased bacterial richness and identified the dominant phyla (Proteobacteria, Firmicutes) and genera (Mycoplasma, unclassified Enterobacterales, Cetobacterium) involved in the intestinal inflammatory response of largemouth bass. Pearson’s correlation analyses showed that differentially expressed genes in the MAPK signaling pathway were significantly correlated with some microflora. The results of this study will help to develop strategies to reduce damage caused by hypoxic stress in aquacultured fish.

Effects of Stocking Density on Intestinal Health of Juvenile Micropterus salmoides in Industrial Aquaponics

“…It is also a potential pathogenic bacterium that can cause intestinal-related diseases such as enteritis [61]. Based on these findings, it is speculated that elevated stocking density may augment the abundance of potentially pathogenic bacteria, consequently instigating intestinal damage, which aligns with prior research outcomes concerning M. salmoides [62]. Thus, it is advisable to exercise heightened vigilance pertaining to pathogenic microorganisms such as Chlamydia during the farming process to preclude disease outbreaks and mitigate fish mortality.…”

Oxidative Stress in Aquatic Organisms

“…Taxonomically, these papers cover freshwater fish ( Carassius auratus [ 4 ], Monopterus albus [ 5 ], Ictalurus punctatus [ 6 ], Megalobrama amblycephala [ 7 ], Micropterus salmoides [ 8 ], Lateolabrax maculatus [ 9 , 10 , 11 , 12 ], Carassius gibelio [ 13 , 14 ], Aplodinotus grunniens [ 15 ], Pangasianodon hypophthalmus [ 16 ], Danio rerio [ 17 ], and hybrid grouper [ 18 ]), marine fish ( Scophthalus maximus [ 19 ]), crustaceans ( Macrobrachium rosenbergii [ 20 , 21 , 22 ], Litopenaeus vannamei [ 23 , 24 , 25 ], Penaeus monodon [ 26 ], Scylla paramamosain [ 27 ], and Eriocheir sinensis [ 28 ]), and molluscs ( Crassostrea hongkongensis [ 29 ], Trachinotus ovatus [ 30 ], and Pacific abalone [ 31 ]). Meanwhile, these papers reveal several endogenous and exogenous factors that induce oxidative stress, such as environmental factors (water hardness [ 4 ], chronic hyperthermia [ 6 ], acute hypoxic stress [ 10 ], acute ammonia nitrogen [ 12 ], hypothermia [ 15 ], low salinity [ 23 ], and ammonia-N-stress [ 26 ]), nutritional factors (high carbohydrate levels [ 5 ], oxidized lipids [ 7 ], high-fat diet [ 12 , 20 ], and lipopolysaccharide [ 29 ...…”

“…To uncover the relationship between oxidative stress inducers and response mechanisms, tissue or cell morphology, antioxidant and immunity enzymes and related gene expression, metabolic homeostasis, and cell fate related autophagy and apoptosis, as well as mortality, have been extensively studied in these papers. Mechanically, some key molecular signaling processes were studied, such as Nrf2 signaling [ 7 , 9 , 22 , 27 ], Notch signaling [ 7 ], PPAR signaling [ 8 ], MAPK signaling [ 10 ], NF-κB signaling [ 15 , 20 , 30 ], Relish-Imd signaling [ 22 ], TLR2-MyD88-NF-κB [ 28 ], and epigenetic regulator m6A methylation [ 17 ]. Additionally, the regulation of gut microbiota on oxidative stress resistance was also investigated in some papers [ 5 , 10 , 11 , 14 , 24 , 25 ].…”

“…Mechanically, some key molecular signaling processes were studied, such as Nrf2 signaling [ 7 , 9 , 22 , 27 ], Notch signaling [ 7 ], PPAR signaling [ 8 ], MAPK signaling [ 10 ], NF-κB signaling [ 15 , 20 , 30 ], Relish-Imd signaling [ 22 ], TLR2-MyD88-NF-κB [ 28 ], and epigenetic regulator m6A methylation [ 17 ]. Additionally, the regulation of gut microbiota on oxidative stress resistance was also investigated in some papers [ 5 , 10 , 11 , 14 , 24 , 25 ]. A brief summary of each paper is shown below for reference.…”

“…Specifically, Nrf2 signaling was involved in the regulation. Song et al [ 10 ] showed that hypoxia caused oxidative stress, exfoliation of the intestinal villus epithelium, and villus rupture, and increased cell apoptosis in largemouth bass ( M. salmoides ). Mechanically, MAPK signaling pathway and inflammatory related microbiota played an important role under hypoxic stress.…”