The Multifaceted Effects of Short-Term Acute Hypoxia Stress: Insights into the Tolerance Mechanism of Propsilocerus akamusi (Diptera: Chironomidae)

SIMPLE SUMMARY: Eutrophication and global warming have caused acute hypoxia in aquatic ecosystems. However, Propsilocerus akamusi depends on great hypoxia tolerance to become a dominant species in eutrophic lakes, but the mechanism of this hypoxia tolerance is unclear. Thus, we combined physiological indicators and histomorphology observations with metabolome–transcriptome analysis to explore the mechanism comprehensively. The results showed that hypoxia tolerance mainly relies on apoptosis, energy metabolism, and an antioxidant mechanism. P. akamusi derives its energy from glycogen metabolism, lipid metabolism, protein digestion and absorption, and the glyoxydate cycle. Lactate is the end product of glycogen degradation, and HIF-1 plays an important role in promoting glycogenolysis in acute hypoxic conditions. However, ethanol probably originates from symbiodinium and, together with hydrogen peroxide, stimulates the elevation of catalase (CAT) activity and induced apoptosis. Understanding the processes that enable P. akamusi to survive lengthy periods of hypoxia in eutrophic lakes might provide a scientific reference for assessing toxicity and favoring policies to reduce their impact on the environment. ABSTRACT: Plenty of freshwater species, especially macroinvertebrates that are essential to the provision of numerous ecosystem functions, encounter higher mortality due to acute hypoxia. However, within the family Chironomidae, a wide range of tolerance to hypoxia/anoxia is displayed. Propsilocerus akamusi depends on this great tolerance to become a dominant species in eutrophic lakes. To further understand how P. akamusi responds to acute hypoxic stress, we used multi-omics analysis in combination with histomorphological characteristics and physiological indicators. Thus, we set up two groups—a control group (DO 8.4 mg/L) and a hypoxic group (DO 0.39 mg/L)—to evaluate enzyme activity and the transcriptome, metabolome, and histomorphological characteristics. With blue–black chromatin, cell tightness, cell membrane invagination, and the production of apoptotic vesicles, tissue cells displayed typical apoptotic features in the hypoxic group. Although lactate dehydrogenase (LDH), alcohol dehydrogenase (ADH), catalase (CAT), and Na+/K+ -ATPase (NKA) activities were dramatically enhanced under hypoxic stress, glycogen content, and superoxide dismutase (SOD) activities were significantly reduced compared to the control group. The combined analysis of the transcriptome and metabolome, which further demonstrated, in addition to carbohydrates, including glycogen, the involvement of energy metabolism pathways, including fatty acid, protein, trehalose, and glyoxylate cycles, provided additional support for the aforementioned findings. Lactate is the end product of glycogen degradation, and HIF-1 plays an important role in promoting glycogenolysis in acute hypoxic conditions. However, we discovered that the ethanol tested under hypoxic stress likely originates from the symbiodinium of P. akamusi. These results imply that some parameters related to energy metabolism, antioxidant enzyme activities, and histomorphological features may be used as biomarkers of eutrophic lakes in Chironomus riparius larvae. The study also provides a scientific reference for assessing toxicity and favoring policies to reduce their impact on the environment.