DNA Repair and Photoprotection: Mechanisms of Overcoming Environmental Ultraviolet Radiation Exposure in Halophilic Archaea

Abstract

Halophilic archaea push the limits of life at several extremes. In particular, they are noted for their biochemical strategies in dealing with osmotic stress, low water activity and cycles of desiccation in their hypersaline environments. Another feature common to their habitats is intense ultraviolet (UV) radiation, which is a challenge that microorganisms must overcome. The consequences of high UV exposure include DNA lesions arising directly from bond rearrangement of adjacent bipyrimidines, or indirectly from oxidative damage, which may ultimately result in mutation and cell death. As such, these microorganisms have evolved a number of strategies to navigate the threat of DNA damage, which we differentiate into two categories: DNA repair and photoprotection. Photoprotection encompasses damage avoidance strategies that serve as a "first line of defense," and in halophilic archaea include pigmentation by carotenoids, mechanisms of oxidative damage avoidance, polyploidy, and genomic signatures that make DNA less susceptible to photodamage. Photolesions that do arise are addressed by a number of DNA repair mechanisms that halophilic archaea efficiently utilize, which include photoreactivation, nucleotide excision repair, base excision repair, and homologous recombination. This review seeks to place DNA damage, repair, and photoprotection in the context of halophilic archaea and the solar radiation of their hypersaline environments. We also provide new insight into the breadth of strategies and how they may work together to produce remarkable UV-resistance for these microorganisms.

Keywords: DNA damage; DNA repair; halophilic archaea; photoprotection; ultraviolet radiation.

FIGURE 1

Carotenoid pigmentation in Great Salt Lake (Utah, United States) halophilic archaea (a) embedded in a shoreline salt crust, (b) growing in colonies on salt agar, and (c) coloring the north arm water pink. (d) A Great Salt Lake Halorubrum species was grown in the absence (top) and presence (bottom) of full spectrum light, demonstrating the impact of light on carotenogenesis (Baxter et al., 2007).

FIGURE 2

Bipyrimidine lesions, the primary form of ultraviolet (UV)-induced DNA damage. Shown above are TT photolesions. Similar chemistry occurs at the other bipyrimidine sites, with the exception that 5′-CT-3′ sequences only form CPDs (Sinha and Häder, 2002). Figure adapted from Rastogi et al. (2010).

FIGURE 3

Pathways of photooxidative DNA damage following UV irradiation. DNA damage can occur through two mechanisms: type I involves electron transfer from an excited photosensitizer to a DNA base, while type II is a direct reaction with O₂ that forms ROS. Resulting specific DNA damage is shown in the final column.

FIGURE 4

Chemical structures of bacterioruberin and β-carotene (Yang et al., 2015), two major carotenoids produced by halophilic archaea.

FIGURE 5

Theoretical genomic photoreactivity based on bipyrimidine signature (P_g) vs. G+C content (%) of 29 halophilic archaea and 243 other prokaryotic genomes (adapted from Jones and Baxter, 2016). P_g is calculated as the weighted sum of a genome’s bipyrimidine incidences: P_g = 1.73(TC_i) + 1.19(TT_i) + 0.61(CT_i) + 0.39(CC_i). Bipyrimidine incidence corresponds to bipyrimidine frequency divided by genome size. Weighting coefficients represent the intrinsic photoreactivity of each bipyrimidine sequence, determined experimentally by Matallana-Surget et al. (2008) as the ratio between the frequency of photoproducts (CPDs and (6-4)PPs) and bipyrimidine incidences in DNA with varying G+C content.

FIGURE 6

Ultraviolet-resistance strategies of halophilic archaea. UV irradiation is attenuated by photoprotective mechanisms, lessening the damage to DNA. The damage that does result may be repaired by a suite of DNA repair systems. [UV, ultraviolet radiation; ROS, reactive oxygen species; CPDs, cyclobutane pyrimidine dimers; (6-4)PP, pyrimidine (6-4) pyrimidone photoproducts; PHR, photoreactivation; NER, nucleotide excision repair; BER, base excision repair; HR, homologous recombination].