A putative bifunctional CPD/ (6-4) photolyase from the cyanobacteria Synechococcus sp. PCC 7335 is encoded by a UV-B inducible operon: New insights into the evolution of photolyases

María Belén Fernández; Lucas Latorre; Natalia Correa-Aragunde; Raúl Cassia

doi:10.3389/fmicb.2022.981788

A putative bifunctional CPD/ (6-4) photolyase from the cyanobacteria Synechococcus sp. PCC 7335 is encoded by a UV-B inducible operon: New insights into the evolution of photolyases

Front Microbiol. 2022 Oct 28:13:981788. doi: 10.3389/fmicb.2022.981788. eCollection 2022.

Authors

María Belén Fernández¹, Lucas Latorre¹, Natalia Correa-Aragunde¹, Raúl Cassia¹

Affiliation

¹ Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Consejo Nacional de Investigaciones Científicas y Técnicas, Mar del Plata, Argentina.

Abstract

Photosynthetic organisms are continuously exposed to solar ultraviolet radiation-B (UV-B) because of their autotrophic lifestyle. UV-B provokes DNA damage, such as cyclobutane pyrimidine dimers (CPD) or pyrimidine (6-4) pyrimidone photoproducts (6-4 PPs). The cryptochrome/photolyase family (CPF) comprises flavoproteins that can bind damaged or undamaged DNA. Photolyases (PHRs) are enzymes that repair either CPDs or 6-4 PPs. A natural bifunctional CPD/(6-4)- PHR (PhrSph98) was recently isolated from the UV-resistant bacteria Sphingomonas sp. UV9. In this work, phylogenetic studies of bifunctional CPD/(6-4)- photolyases and their evolutionary relationship with other CPF members were performed. Amino acids involved in electron transfer and binding to FAD cofactor and DNA lesions were conserved in proteins from proteobacteria, planctomycete, bacteroidete, acidobacteria and cyanobacteria clades. Genome analysis revealed that the cyanobacteria Synechococcus sp. PCC 7335 encodes a two-gene assembly operon coding for a PHR and a bifunctional CPD/(6-4) PHR- like. Operon structure was validated by RT-qPCR analysis and the polycistronic transcript accumulated after 15 min of UV-B irradiation. Conservation of structure and evolution is discussed. This study provides evidence for a UV-B inducible PHR operon that encodes a CPD/(6-4)- photolyase homolog with a putative bifunctional role in the repair of CPDs and 6-4 PPs damages in oxygenic photosynthetic organisms.

Keywords: Synechococcus sp. PCC 7335; UV-B; bifunctional CPD/(6-4) photolyase- like; cryptochrome/photolyase family; cyanobacteria; photolyase operon.