The Evolution of Temperature and Desiccation-Related Protein Families in Tardigrada Reveals a Complex Acquisition of Extremotolerance

Abstract

Tardigrada is an ecdysozoan lineage most famous for its resilience. Tardigrades can tolerate high doses of radiation, low oxygen environments, desiccation and both high and low temperatures under a dormant state called anhydrobiosis, which is a reversible halt of metabolism upon almost complete desiccation. A large amount of research has focused on the genetic pathways related to these capabilities, and a number of genes have been identified and linked to tardigrade’s extremotolerant response. However, the history of these genes is unclear, and the origins and history of extremotolerant genes within Tardigrada remain a mystery. Here, we generate the first phylogenies of six separate gene families linked with desiccation and radiation tolerance in Tardigrada: Cytosolic Abundant Heat Soluble Protein (CAHS), Mitochondrial Abundant Heat Soluble Protein (MAHS), Secretory Abundant Heat Soluble Protein (SAHS), Meiotic Recombination 11 Homolog (MRE11) and the newly discovered Echiniscus testudo Abundant Heat Soluble Proteins (EtAHS Alpha and Beta). Our study of the gene duplications suggests a link between the evolution of these genes and aquatic to limno-terrestrial transitions within tardigrades. Our results suggest that tardigrades likely transitioned from the marine to limno-terrestrial environment only twice, once in stem-Eutardigrada and once in Heterotardigrada, which explains the unique adaptations to anhydrobiosis present in both classes.

Sexual dimorphism in the tardigradeParamacrobiotus metropolitanustranscriptome

“…Interestingly, all three CAHS orthologs induced in males were the only three among the 13 CAHS orthologs that were not differentially expressed during anhydrobiosis ( Supplementary Table S6 ). Phylogenetic analysis indicated that these CAHS orthologs were CAHS1 (PARRI_0016931), putative CAHS5 (PARRI_0006576), and CAHS5 (PARRI_0002229) orthologs, following the proposed naming scheme of Fleming et al (53). In contrast, the SAHS ortholog, detected as differentially expressed, was induced in the females.…”

“…Similarly, we conducted a phylogenetic analysis of CAHS genes. We obtained annotated CAHS sequences from our previous report (53) and pooled the amino acid sequences of P. metropolitanus CAHS candidate orthologs. A phylogenetic tree was constructed using the same procedure.…”

Transcriptome analysis of the tardigradeHypsibius exemplarisexposed to the DNA-damaging agent bleomycin

“…The core machinery of tardigrade DNA repair does not differ significantly from that of other eukaryotes 27) , with the exception of the duplication of several genes in Ramazzottius varieornatus, e.g. MRE11 28) . Other DNA repair Omics analysis of bleomycin exposed tardigrades 3 3 factors regulated during anhydrobiosis include the regulation of RAD51 in Milnesium cf.…”