Identification of a Novel Class of Photolyases as Possible Ancestors of Their Family

• Published in: Molecular biology and evolution Vol. 38; no. 10; pp. 4505 - 4519
• Main Authors: Xu, Lei, Chen, Simeng, Wen, Bin, Shi, Hao, Chi, Changbiao, Liu, Chenxi, Wang, Kangyu, Tao, Xianglin, Wang, Ming, Lv, Jun, Yan, Liang, Ling, Liefeng, Zhu, Guoping
• Format: Journal Article
• Language: English
• Published: United States Oxford University Press 01.10.2021
• Subjects: Cryptochromes - genetics; Deoxyribodipyrimidine Photo-Lyase - chemistry; Deoxyribodipyrimidine Photo-Lyase - genetics; Deoxyribodipyrimidine Photo-Lyase - metabolism; Discoveries; DNA Repair; Enzymes; Iron compounds; Phylogeny; Protein binding; Pyrimidine Dimers - chemistry; Pyrimidine Dimers - metabolism; Sulfur compounds; Ultraviolet Rays; China; phylogenetic analysis; iron–sulfur cluster; photolyase; cyclobutane pyrimidine dimer; cryptochrome
• ISSN: 1537-1719; 0737-4038; 1537-1719
• DOI: 10.1093/molbev/msab191

Abstract UV irradiation induces the formation of cyclobutane pyrimidine dimers (CPDs) and 6-4 photoproducts in DNA. These two types of lesions can be directly photorepaired by CPD photolyases and 6-4 photolyases, respectively. Recently, a new class of 6-4 photolyases named iron–sulfur bacterial cryptochromes and photolyases (FeS-BCPs) were found, which were considered as the ancestors of all photolyases and their homologs—cryptochromes. However, a controversy exists regarding 6-4 photoproducts only constituting ∼10–30% of the total UV-induced lesions that primordial organisms would hardly survive without a CPD repair enzyme. By extensive phylogenetic analyses, we identified a novel class of proteins, all from eubacteria. They have relatively high similarity to class I/III CPD photolyases, especially in the putative substrate-binding and FAD-binding regions. However, these proteins are shorter, and they lack the “N-terminal α/β domain” of normal photolyases. Therefore, we named them short photolyase-like. Nevertheless, similar to FeS-BCPs, some of short photolyase-likes also contain four conserved cysteines, which may also coordinate an iron–sulfur cluster as FeS-BCPs. A member from Rhodococcus fascians was cloned and expressed. It was demonstrated that the protein contains a FAD cofactor and an iron–sulfur cluster, and has CPD repair activity. It was speculated that this novel class of photolyases may be the real ancestors of the cryptochrome/photolyase family.