UV radiation-induced biosynthesis, stability and antioxidant activity of mycosporine-like amino acids (MAAs) in a unicellular cyanobacterium Gloeocapsa sp. CU2556

Highlights

• HPLC analysis revealed the presence of two MAAs, shinorine and M-307 in Gloeocapsa sp.

• UV-B radiation can induce the biosynthesis of MAAs.

• The MAAs, shinorine and M-307 are highly stable against some abiotic stressors.

• The MAAs (shinorine + M-307) shows strong antioxidant activity.

Abstract

The biosynthesis of natural sunscreening compounds as influenced by ultraviolet radiation, their stability and antioxidant activity were studied in the cyanobacterium Gloeocapsa sp. CU-2556. An analysis by high-performance liquid chromatography (HPLC) with photodiode-array (PDA) detection revealed the biosynthesis of two MAAs, shinorine (UVλ_max 333 nm) and an unknown MAA designated as M-307 (UVλ_max 307 nm) with retention times of 5.9 and 6.4 min, respectively. Induction of the synthesis of MAAs was studied under 395 (PAR), 320 (PAR + UV-A) and 295 (PAR + UV-A + UV-B) nm cut-off filters. MAAs induction was significantly increased with an increase in exposure time up to 72 h in the samples covered with 295 nm cut-off filters. Contrary to shinorine, the biosynthesis of M-307 was more dominant in this unicellular cyanobacterium. Both MAAs were highly stable to some physico-chemical stressors such as UV radiation, heat and a strong oxidizing agent. The MAA M-307 was more stable under strong oxidative stress than shinorine. Moreover, UV-C radiation drastically decreased the stability of both MAAs. The MAAs (shinorine + M-307) also exhibited efficient antioxidant activity which was dose-dependent. The results indicate that MAAs may perform a vital role in survival and sustainability of Gloeocapsa sp. CU-2556 in harsh environmental conditions by its ability to absorb/screen short wavelength UV radiation and antioxidant function.

Introduction

Cyanobacteria are one of the most dominant photoautotrophic prokaryotes and are major biomass producers in both aquatic and terrestrial ecosystems. The obligate requirement of solar light to perform some energy-dependent processes exposes them simultaneously to harmful doses of short wavelength ultraviolet (UV) radiation in their natural habitats. The increase in solar UV radiation on the Earth’s surface due to ozone depletion [1] is now recognized as a major environmental factor deleterious to all sun-exposed organisms [2], [3], [4], [5]. The high-energetic UV (mainly UV-B: 280–315 nm) radiation has great potential for cell damage either through direct effects on biologically relevant molecules (e.g., DNA and proteins) or indirect effects via the production of reactive oxygen species (ROS) [6], [7], [8], [9]. UV-B radiation is a highly active component of the solar radiation that brings about chemical modifications in DNA by the formation of pyrimidine dimers and strand breaks leading to mutagenesis and loss of normal cellular metabolic functions [8]. Several key physiological processes such as morphology, cell division and differentiation, growth, survival, motility and orientation, buoyancy, N₂ fixation, CO₂ uptake, photosynthesis, pigmentation and enzyme activity have been reported to be affected by UV radiation [10], [11], [12]. Consequently, several organisms including cyanobacteria that are exposed to solar radiation in their brightly lit habitats have evolved a number of mitigation strategies such as migration and mat formation, active repair mechanisms, production of quenching agents and synthesis/accumulation of UV radiation-absorbing/screening secondary compounds to counteract the negative effects of UV radiation [9], [12], [13], [14], [15], [16].

Biosynthesis of several UV-absorbing compounds in diverse organisms has received much attention for their putative role in UV photoprotection. In the past few years, some MAAs isolated from cyanobacteria and other taxonomic groups [13], [17] have become one of the most promising natural substances in the field of biotechnology and biomedical research [18] due to their strong UV absorption maxima (between 307 and 362 nm), high molar extinction coefficients (ε = 28,100–50,000 M⁻¹ cm⁻¹) and potential antioxidant properties. MAAs are colorless, water-soluble compounds composed of a cyclohexenone or cyclohexenimine chromophore conjugated with the nitrogen substituent of an amino acid or its imino alcohol [19]. The occurrence and/or UV-induced biosynthesis of MAAs is very limited or was not known in the unicellular cyanobacterium, Gloeocapsa sp. There are few reports on the stability of MAAs under different environmental conditions [20], [21], [22]. Moreover, the antioxidant activities of different MAAs in terms of scavenging of free radicals have been scarcely investigated which limits the specific use of MAAs. In the present study, we have investigated the presence of MAAs and its inducibility by UV stress, stability under different physicochemical stressors and total antioxidant potential in a unicellular cyanobacterium Gloeocapsa sp. isolated from stone monuments in the vicinity of Bangkok, facing high irradiation all year round especially during hot summers in their natural habitat.