Navigating oxygen deprivation: liver transcriptomic responses of the red eared slider turtle to environmental anoxia

Abstract

The best facultative anaerobes among vertebrates are members of the genera Trachemys (pond slider turtles) and Chrysemys (painted turtles), and are able to survive without oxygen for up to 12 to 18 weeks at ∼3 °C. In this study, we utilized RNAseq to profile the transcriptomic changes that take place in response to 20 hrs of anoxia at 5 °C in the liver of the red eared slide turtle (Trachemys scripta elegans). Sequencing reads were obtained from at least 18,169 different genes and represented a minimum 49x coverage of the C. picta bellii exome. A total of 3,105 genes showed statistically significant changes in gene expression between the two animal groups, of which 971 also exhibited a fold change equal to or greater than 50% of control normoxic values. This study also highlights a number of anoxia-responsive molecular pathways that are may be important to navigating anoxia survival. These pathways were enriched in mRNA found to significantly increase in response to anoxia and included molecular processes such as DNA damage repair and metabolic reprogramming. For example, our results indicate that the anoxic turtle may utilize succinate metabolism to yield a molecule of GTP in addition to the two molecules that results from lactate production, and agrees with other established models of anoxia tolerance. Collectively, our analysis provides a snapshot of the molecular landscape of the anoxic turtle and may provide hints into the how this animal is capable of surviving this extreme environmental stress.

mTOR Signaling in Metabolic Stress Adaptation

“…Studies with naked mole rats indicate that mTORC1 activation may serve to promote anaerobic glycolysis as a means to provide ATP to essential tissues including the heart and brain during periods of oxygen deprivation. A similar increase in glycolytic flux is also observed in turtles, as supported by a recent transcriptomic study showing that gene expression of several glycolytic enzymes was highly up-regulated after 20 hours of anoxia exposure [ 70 ]. Consistent with an increase in anaerobic glycolysis, levels of lactate were also highly elevated in tissues of both naked mole rats and turtles during periods of anoxia exposure [ 64 , 71 ].…”

The Metabolomic Response of Crucian Carp (Carassius carassius) to Anoxia and Reoxygenation Differs between Tissues and Hints at Uncharacterized Survival Strategies

“…Alpha-ketoglutarate may be further processed in the TCA cycle to generate NADH and succinyl-CoA, leading to ATP/GTP generating hydrolysis of succinyl-CoA into succinate as an end product. In ischemic mice hearts, succinyl-CoA has been suggested to be the main contributor to succinate accumulation [ 45 ], and notably, succinate-CoA ligase transcription increased in the liver of anoxic turtles [ 55 ].…”

Comparative Analysis of the Growth, Physiological Responses, and Gene Expression of Chinese Soft-Shelled Turtles Cultured in Different Modes

“…Gene expression profiles also reveal differences in immunity in turtles cultured in different habitats [ 56 , 57 ]. PI3K/Akt pathways can be activated by stressors and regulate transcription, translation, proliferation, growth, and survival [ 58 ].…”