Impact of Ultraviolet Radiation on Cyanobacteria: History
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Contributor:
Varsha K. Singh
,
Sapana Jha
,
Palak Rana
,
Sonal Mishra
,
Neha Kumari
,
Suresh C. Singh
,
Shekhar Anand
,
Vijay Upadhye
,
Rajeshwar P. Sinha

Ultraviolet radiation (UVR) tends to damage key cellular machinery. Cells may adapt by developing several defence mechanisms as a response to such damage; otherwise, their destiny is cell death. Since cyanobacteria are primary biotic components and also important biomass producers, any drastic effects caused by UVR may imbalance the entire ecosystem. Cyanobacteria are exposed to UVR in their natural habitats. This exposure can cause oxidative stress which affects cellular morphology and vital processes such as cell growth and differentiation, pigmentation, photosynthesis, nitrogen metabolism, and enzyme activity, as well as alterations in the native structure of biomolecules such as proteins and DNA. The high resilience and several mitigation strategies adopted by a cyanobacterial community in the face of UV stress are attributed to the activation of several photo/dark repair mechanisms, avoidance, scavenging, screening, antioxidant systems, and the biosynthesis of UV photoprotectants, such as mycosporine-like amino acids (MAAs), scytonemin (Scy), carotenoids, and polyamines.

  • mycosporine-like amino acids
  • photoprotection
  • photo repair
  • resilience
  • scytonemin

1. Introduction

Cyanobacteria are a phylogenetically primitive group of Gram-negative photosynthetic prokaryotes with a wide distribution ranging from hot springs to the Arctic and Antarctic regions. These oxygen-evolving organisms appeared during the Precambrian era (between 2.8 and 3.5 × 109 years ago) and provided favourable conditions for the evolution of current aerobic life [1]. Several natural compounds with therapeutic, commercial, and agricultural value are derived from cyanobacteria. They are also used as traditional energy resources and as an alternate source of natural compounds for cosmetics. Some cyanobacterial species are used as non-traditional sources of protein and food [2].
Ultraviolet radiation is divided into three categories: UV-C (100–280 nm), UV-B (280–315 nm), and UV-A (315–400 nm). While UV-A and UV-B rays are transmitted through the atmosphere, all UV-C and some UV-B rays are retained by the ozone layer. UV-C radiation never reaches the Earth’s surface. The continuous release of anthropogenic pollutants such as organobromides (OBs) and chlorofluorocarbons (CFCs) has led to ozone layer depletion. This results in an increased incidence of ultraviolet radiation (UVR; 280–400 nm) on the Earth’s surface, which is absorbed by biomolecules such as proteins and nucleic acids, ultimately resulting in lethal effects on biological systems [3]. Both photosynthesis and nitrogen fixation are energy-dependent processes driven by solar energy. The harvesting of solar radiation exposes cyanobacteria to harmful doses of UV-B and UV-A radiation simultaneously in their natural habitats.
High exposure to UV-B radiation negatively impacts the production of food, ecological systems, and human well-being [4][5]. High-energy UV-B radiation has the greatest potential for cell damage caused by both its direct effects on DNA and proteins and its indirect effects via the production of reactive oxygen species (ROS) [6][7][8]. There are several targets for these potentially toxic ROS, including lipids, DNA, and proteins. Moreover, damage to the photosynthetic apparatus is also partially mediated by ROS, resulting in the inhibition of photosynthesis [1]. In contrast, UV-A radiation that is not absorbed directly by DNA can still induce DNA damage either by producing a secondary photoreaction of existing DNA photoproducts or via indirect photosensitizing reactions [8]. UVR has been reported to affect DNA and its morphological characteristics as well as cells’ differentiation, elastic properties, phycobiliprotein composition, protein profile, development, survival, pigmentation, orientation, metabolic processes, and 14CO2 uptake [9][10].
In response to the devastating effects of UVR, cyanobacteria have evolved a number of defence strategies, including migration and mat formation, efficient DNA repair mechanisms, including photoreactivation, excision repair, the SOS response, the production of antioxidants, the biosynthesis of UV-absorbing compounds such as MAAs and scytonemin, and apoptosis (or programmed cell death, PCD) [2]. However, little information is available regarding the molecular mechanisms of UV-absorbing compounds, the detection of UV signals, and UV-induced PCD in cyanobacteria.

2. Impact of UVR on Cyanobacteria

The surface of the Earth receives very small amounts of solar UVR (UV-C, 0%; UV-B, <1%; UV-A, <7%), but this part of the solar spectrum is extremely energetically active [1]. In cyanobacteria, there are several direct targets for harmful UV-B radiation, such as proteins and DNA, which have absorption maxima in this region, whereas UV-A irradiation has indirect effects through energy transfer from UV-A-stimulated chromophores to the DNA target [1]. After being exposed to UV-B radiation for 9 h, the levels of photosynthetic pigments, total chlorophyll, total carotenoids, and c-phycocyanin were reduced in Arthrospira platensis [11]. According to Vega et al. [12], numerous cyanobacteria and microalgae are affected by UV-B exposure in terms of their development, survival, pigmentation, orientation, growth, general metabolism, photosynthesis, nitrogen fixation, and nitrogen uptake (Figure 1).
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Figure 1. Schematic representation of possible effects of UVR on cyanobacteria: UVR exposure triggers the production of ROS which negatively affects the morphology, physiology, and biochemistry of cyanobacteria (modified from Rastogi et al. [2]).

2.1. Photosynthesis

UVR inhibits a number of photosynthetic processes in cyanobacteria, including the uptake of 14CO2, O2 evolution, and ribulose-1,5 bisphosphate carboxylase (RuBISCO) activity. RuBISCO, a holoenzyme, consists of two subunits: the 55 kDa larger subunit (LSU) and the 14 kDa smaller subunit (SSU) [13]. When exposed to UV-B radiation, RuBISCO becomes susceptible to a variety of modifications, including photo-degradation, polypeptide chain fragmentation, denaturation, active site modification, and the enhanced solubility of membrane proteins [14]. The availability of ATP and NADPH2 may also be reduced, which could prevent the fixation of carbon dioxide. Additionally, UV-B radiation negatively impacts tyrosine electron donors, quinine electron acceptors, and D1 and D2 proteins of photosystem II (PSII) [15]. Damage to the water-oxidizing Mn cluster in the PSII reaction centre (RC) leads to electron transport chain (ETC) inactivation [16]. The cyanobacterium Anabaena variabilis PCC 7937, when exposed to UVR, showed a reduction in the overall photosynthetic yield because of a reduction in the relative electron transport rate (rETR) [17]. Under UV-B radiation, Spirulina platensis showed a distorted thylakoid membrane with decreased Chl a content [18]. After exposing a Phormidium strain to UV radiation for only a few minutes, Häder [19] observed a reduction in O2 evolution. Additionally, UV-B radiation causes oxidative damage which leads to the lipid peroxidation of polyunsaturated fatty acids (PUFAs), which in turn weaken the strength of cells and thylakoid membranes and harm photosynthetic components [20].

2.2. Growth, Cell Differentiation, and Motility

UV-B irradiation severely affects cyanobacteria’s biochemical and physiological life processes, such as morphology, survival, cell differentiation, growth, development, pigmentation, orientation, and motility [21]. Döhler et al. [22], Häder et al. [23], and Newton et al. [24] reported the inhibitory effects of UV-B radiation on certain cyanobacteria, such as Anabaena flos-aquae, Synechococcus leopoliensis, and Phormidium uncinatum. It has been suggested that UV-B radiation damages cellular components that absorb radiation between 280 and 320 nm, leading to cell death. The tolerance of different species to UV-B radiation varies, and even strains that are closely related exhibit differences in sensitivity. In Antarctica cyanobacterium, Oscillatoria priestleyi growth was completely suppressed, whereas it was 62% in the case of Phormidium murrayi following a similar dosage of UV exposure. UVR significantly reduces the proportion of motile filaments and reduces the linear velocity of cyanobacterial cells, which affects their capacity to protect themselves from harmful UVR [2]. After 10–30 min of UVR exposure, a study has shown a significant reduction in the number of motile filaments of Anabaena variabilis, Oscillatoria tenuis, and Phormidium uncinatum. UV-B radiation hinders the ability of cyanobacteria to establish themselves in their photo environment, which ultimately leads to their premature death [25]. The differentiation of vegetative cells into heterocysts or akinetes and the fragmentation of filaments have been reported in the cyanobacterium Anabaena siamensis TISTR-8012 due to exposure to UV-B radiation [2]. Under UV-B radiation, the cyanobacterium Anabaena sp. PCC 7120 showed heterocyst differentiation of vegetative cells and a reduction of up to 49% in trichome length [9]. The three main heterocyst polypeptides (26, 54, and 55 kDa) are believed to be depleted after UV-B treatment as a result of the breakdown of the multi-layered heterocyst wall, which is crucial for maintaining the active form of the enzyme nitrogenase [26].

2.3. Nitrogen Metabolism

Nitrogenase is the key enzyme for nitrogen fixation, and UV-B radiation also significantly inhibits the process of nitrogen fixation, either directly or indirectly, due to the highly sensitive nature of the nitrogenase enzyme to UVR [27]. The activity of nitrogenase in a Nostoc species was lost after 45 min of exposure to UV-B, but nitrate reductase and the glutamine synthetase activity were found to be unaffected [28]. Strong protection against nitrogenase inactivation was provided by ascorbic acid or reduced glutathione. By preserving the sulfhydryl groups or disulfide bonds, reducing agents are known to maintain the native structure of various proteins in their original condition. Nitrogenase is extremely sensitive to oxygen and is likely to exhibit changes in its sulfhydryl groups. In different species, different levels of UV-B protection mechanisms have been observed, which may account for the variation in the amount of time needed to completely kill and inactivate nitrogenase activity [29]. Many researchers believe that the high susceptibility of nitrogenase to UV-B radiation is caused by either the presence of aromatic amino acids or the enzyme’s native structure [25].

2.4. Biomolecules

UV radiation has been shown to have an effect on the structural and functional integrity of accessory photo-harvesting pigments, such as phycocyanin, phycoerythrin, and allophycocyanin, in the marine cyanobacterium Lyngbya sp. A09DM [30]. UV-B radiation severely affects low-molecular-weight proteins. In Nostoc sp., αβ monomers of phycocyanin with a very low size (approximately 20 kDa) were the most affected. When Nostoc carmium and Anabaena sp. were exposed to UV-B radiation for 90 or 120 min, proteins with a size of 14.5–45 kDa were completely lost, but proteins with a size of about 55–66 kDa were unaffected, even after 120 min of UV-B irradiation. After 150 min of exposure to UV-B radiation, the proteins in Nostoc commune and Scytonema sp. completely disappeared [31]. The total protein profile of Nostoc spongiaeforme and Phormidium corium was changed both qualitatively and quantitatively after UV-B radiation and high light treatment [32]. The number and quantity of protein bands in various cyanobacteria were found to decrease linearly with the increased duration of UV exposure.
When cyanobacteria are directly exposed to UVR, their DNA is subjected to several kinds of damage and their cells also suffer from oxidative stress. One such type of damage that is specifically caused by UV-B radiation is covalent linkage between the bases, which results in lesions such as cyclobutane pyrimidine dimers (CPDs), pyrimidine photoproducts (6-4PPs), and their Dewar isomers. These CPDs and 6-4PPs DNA lesions produced by UV-B radiation can produce primary and secondary breaks in DNA, respectively [33]. These breaks stall the DNA polymerase and prevent it from progressing, thus inhibiting transcription and translation machinery [33], which eventually results in mutations or the death of the organism [34]. Numerous filamentous and unicellular cyanobacterial species such as Anabaena sp., Nostoc sp., and Scytonema sp. produce thymine dimers (T< >T) when exposed to UV radiation [35]. Thymine dimers appear more frequently under continuous UVR exposure. A cyanobacterium, Arthrospira platensis, formed CPD under UV stress in a way that was dependent on the temperature and its biomass. UV-induced DNA damage is reported in Anabaena variabilis PCC7937 and Synechocystis PCC 6308. Mosca et al. [36] observed an increased accumulation of DNA lesions in dried UV-irradiated biofilms compared to dried biofilms of the desert cyanobacterium Chroococcidiopsis.

This entry is adapted from the peer-reviewed paper 10.3390/ijms241512381

References

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