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.

Highlights

  • Maintaining optimal and continuous oxygen supply to organs is not universal across the animal kingdom

  • While variance existed between individual samples in the same experimental group, the clustering analysis demonstrated a clear separation of the overall gene expression pattern between control and anoxic turtles

  • T. scripta elegans utilizes a number of different molecular approaches to adapt to a low oxygen environment and is able to avoid anoxia-induced cellular damage through the reprioritization and depression of metabolic processes, such that cellular energy demand can be met by anaerobic metabolism (Storey, 2007)

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Summary

Introduction

Maintaining optimal and continuous oxygen supply to organs (in order to maintain high rates of aerobic metabolism) is not universal across the animal kingdom. Many facultative anaerobic organisms, including a variety of ectothermic vertebrates, are able to survive extended periods without a supply of oxygen (Biggar, Groom & Storey, 2012; Storey, 2007; Nilsson & Renshaw, 2004). A lack of available oxygen is common among turtles, which spend the majority of their lives diving underwater (Clark & Miller, 1973; Jackson, 1968). For bouts of short-term oxygen deprivation, such as during underwater dives for food, increasing anaerobic metabolism is able to meet metabolic demands (Storey & Storey, 2004).

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