“High‐altitude Andean Lakes” (HAAL) are pristine environments harboring poly‐extremophilic microbes that show combined adaptations to physical and chemical stress such as large daily ambient thermal amplitude, extreme solar radiation levels, intense dryness, alkalinity, high concentrations of arsenic (up to 200 ppm) and dissolved salts. In this work, we compared the UV resistance profiles, pigment content and photoreactivation abilities of three UV‐resistant bacteria isolated from distinct niches from HAALs, that is Acinetobacter sp. Ver3 (water, Lake Verde; 4400 m), Exiguobacterium sp. S17 (stromatolite, Lake Socompa, 3570 m) and Nesterenkonia sp. Act20 (soil, Lake Socompa, 3570 m). UV resistance ability of HAAL's strains indicate a clear adaptation to high radiation exposure encountered in their original habitat, which can be explained by genetic and physiological mechanisms named as the UV‐resistome. Thus, the UV‐resistome depends on the expression of a diverse set of genes devoted to evading or repairing the damage it provoked direct or indirectly. As pigment extraction and photoreactive assays indicate the presence of photoactive molecules, we characterized more in detail proteins with homology to photolyases/cryptochromes members (CPF). Phylogenetic analyses, sequence comparison and 3D modeling with bona fide CPF members were used to prove the presence of functional domains and key residues in the novel proteins.

During evolution, microorganisms exposed to high amounts of UV-B irradiation developed fine-tuned photo-enzymes called ‘photolyases’ to cope with DNA damage caused by UV-B. These photoreceptors, belonging to the cryptochrome/photolyase family (CPF), have been well characterized at the genomic and proteomic level in bacteria isolated from a wide range of environments. In this work, we go further towards studying the abundance of CPF in aquatic microbial communities from different geographic regions across the globe. Metagenomics data combined with geo-referenced solar irradiation measurements indicated that the higher the UV-B level in the microbiome’s environment, the higher the abundance of CPF genes and lower the microbial diversity. A connection between CPF abundance and radiation intensity/photoperiod was found. Likewise, cryptochrome-like genes were found to be abundant in most exposed microbiomes, indicating a complementary role to standard photolyases. We observed that CPFs are more likely to be present in dominant taxa of the highly irradiated microbiomes, suggesting an evolutionary force for survival and dominance under extreme solar exposure. This work reports 3 novel CPF clades, proving the potential of global metagenomic analyses in detecting novel proteins.