Differential mechanisms of tolerance to extreme environmental conditions in tardigrades

Dido Carrero,Víctor Quesada,José G. Pérez-Silva,Carlos López-Otín

doi:10.1038/s41598-019-51471-8

Abstract

Tardigrades, also known as water bears, are small aquatic animals that inhabit marine, fresh water or limno-terrestrial environments. While all tardigrades require surrounding water to grow and reproduce, species living in limno-terrestrial environments (e.g. Ramazzottius varieornatus) are able to undergo almost complete dehydration by entering an arrested state known as anhydrobiosis, which allows them to tolerate ionic radiation, extreme temperatures and intense pressure. Previous studies based on comparison of the genomes of R. varieornatus and Hypsibius dujardini - a less tolerant tardigrade - have pointed to potential mechanisms that may partially contribute to their remarkable ability to resist extreme physical conditions. In this work, we have further annotated the genomes of both tardigrades using a guided approach in search for novel mechanisms underlying the extremotolerance of R. varieornatus. We have found specific amplifications of several genes, including MRE11 and XPC, and numerous missense variants exclusive of R. varieornatus in CHEK1, POLK, UNG and TERT, all of them involved in important pathways for DNA repair and telomere maintenance. Taken collectively, these results point to genomic features that may contribute to the enhanced ability to resist extreme environmental conditions shown by R. varieornatus.

Highlights

Among all genes involved in base excision repair (BER) analysed in R. varieornatus and H. dujardini, we found a variant in an active site and UGI interface site (p.P177R) in the protein encoded by UNG that is www.nature.com/scientificreports exclusive of R. varieornatus[57] (Fig. 4a)
Among all the genes involved in NER, XPC appears to be duplicated in R. varieornatus but not in H. dujardini (Supplementary Table 4)
We describe several gene expansions of pivotal elements in DNA repair pathways observed in the genomes of R. varieornatus and H. dujardini through manual annotation, including previously described expansions, such as XPC, LIG4, ERCC4 and MRE119,11

Summary

Introduction

These data suggest an important role of MRE11 ortholog in R. varieornatus in promoting DNA repair after exposure to ionizing radiation. According to our data, we propose that one of the four copies annotated in this tardigrade’s genome by Hashimoto et al corresponds to the XRCC2 ortholog, as assessed by performing blast of these sequences (deposited in the NCBI database) against the human genome. Expansion of the DNA repair endonuclease XPF (encoded by the gene ERCC4), involved in HR56, was reported in H. dujardini, since five copies of this gene were found in its genome[11].

Results

Conclusion