Over-Expression of UV-Damage DNA Repair Genes and Ribonucleic Acid Persistence Contribute to the Resilience of Dried Biofilms of the Desert Cyanobacetrium Chroococcidiopsis Exposed to Mars-Like UV Flux and Long-Term Desiccation.

Claudia Mosca,Daniela Billi,Alessandro Napoli,Lynn J Rothschild,Claudia Fagliarone,Elke Rabbow,Fabrizio Ferré,Marco Pietrosanto,Petra Rettberg,Mickael Baqué

doi:10.3389/fmicb.2019.02312

Abstract

The survival limits of the desert cyanobacterium Chroococcidiopsis were challenged by rewetting dried biofilms and dried biofilms exposed to 1.5 × 103 kJ/m2 of a Mars-like UV, after 7 years of air-dried storage. PCR-stop assays revealed the presence of DNA lesions in dried biofilms and an increased accumulation in dried-UV-irradiated biofilms. Different types and/or amounts of DNA lesions were highlighted by a different expression of uvrA, uvrB, uvrC, phrA, and uvsE genes in dried-rewetted biofilms and dried-UV-irradiated-rewetted biofilms, after rehydration for 30 and 60 min. The up-regulation in dried-rewetted biofilms of uvsE gene encoding an UV damage endonuclease, suggested that UV-damage DNA repair contributed to the repair of desiccation-induced damage. While the phrA gene encoding a photolyase was up-regulated only in dried-UV-irradiated-rewetted biofilms. Nucleotide excision repair genes were over-expressed in dried-rewetted biofilms and dried-UV-irradiated-rewetted biofilms, with uvrC gene showing the highest increase in dried-UV-irradiated-rewetted biofilms. Dried biofilms preserved intact mRNAs (at least of the investigated genes) and 16S ribosomal RNA that the persistence of the ribosome machinery and mRNAs might have played a key role in the early phase recovery. Results have implications for the search of extra-terrestrial life by contributing to the definition of habitability of astrobiologically relevant targets such as Mars or planets orbiting around other stars.

Highlights

Our knowledge of the limit of life’s adaptability to extreme environments is mandatory for identifying habitable planets and moons in the Solar System and planetary systems orbiting around other stars (Schulze-Makuch et al, 2017)
In order to unravel the mechanisms underlying such endurance, the role of both protection mechanisms taking place upon desiccation and repair mechanisms triggered upon rehydration must be taken into consideration
Chroococcidiopsis adopts efficient countermeasures to avoid the otherwise lethal effects of water removal, its endurance when air-dried can be limited by the oxidative damage accumulated even in the absence of metabolic activity (Billi, 2009)

Summary

Introduction

Our knowledge of the limit of life’s adaptability to extreme environments is mandatory for identifying habitable planets and moons in the Solar System and planetary systems orbiting around other stars (Schulze-Makuch et al, 2017). A few organisms called anhydrobiotes, survive desiccation by stabilizing their sub-cellular structures and entering a metabolic dormancy until water is available again (Crowe et al, 1992). Despite the interest in anhydrobiotes, it is not yet known how long they can persist in the air-dried state and which levels of radiation doses they can experience without dying. Knowing their desiccation endurance threshold is relevant to understanding the limits of life on Earth and to assessing the potential habitability of astrobiologically relevant targets such as Mars and rocky exoplanets with transient availability of liquid water (Wilhelm et al, 2018). The identification of their UV resistance threshold has implications when tackling the surface habitability of rocky planets with elevated UV radiation fluxes (O’Malley-James and Kaltenegger, 2017)

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