At the Edge of Survival: Exploring the Frontiers of Tardigrade Extreme Stress Tolerance

Tardigrades possess extraordinary resilience to extreme environmental conditions, including near-complete desiccation, severe levels of radiation, the vacuum of space and extreme sub-zero temperatures. Despite significant interest in their survival strategies, the molecular mechanisms underlying their survival during extreme stresses have remained elusive. However, recent sequencing approaches and gene expression analyses have significantly expanded our knowledge of tardigrade biology. This review explores how omics technologies, particularly RNA sequencing and other RNA-based methods are currently transforming our understanding of tardigrade survival strategies, identifying genes with proposed significance for tardigrade extreme stress tolerance. We briefly discuss characteristics of tardigrade species with available transcriptome and genome assemblies and, by synthesising insights from recent studies, provide a thorough examination of proposed mechanisms involved in tardigrade resilience. We share our curated data-mining results and also provide a new transcriptome for the species Echiniscus testudo. Proposed mechanisms are addressed from a whole phylum perspective, emphasising evolutionary relationships and the proposed origin of identified genes. These genes encode proteins involved in mechanisms such as antioxidant defence, DNA protection and repair, protein folding and protection of three-dimensional structure from molecular and cellular to whole animal levels. Special focus is on peroxins and also filament-forming proteins, which likely play a vital role in sustaining the so-called tun state-a state that enables desiccated tardigrades to suspend metabolism, yet uphold structural integrity for decades before returning to life following resuspension in water. Finally, we discuss promising future directions for using omics technologies and RNA-based methods in unravelling tardigrade survival strategies.