Enhanced UV-B Photoprotection Activity of Carotenoids from the Novel Sp. Strain LAPM80 Isolated from King George Island, Antarctica

Antarctica's harsh environmental conditions, characterized by high levels of ultraviolet (UV) radiation, pose challenges for microorganisms. To survive in these extreme cold regions with heightened UV exposure, microorganisms employ various adaptive strategies, including photoprotective carotenoid synthesis. Carotenoids are garnering attention in the skin health industry because of their UV photoprotection potential, given the direct relationship between UV exposure and skin burns, and cancer. Also, there is a growing demand for natural and environmentally friendly photoprotectors, such as microbial-based products, in opposition to synthetic photoprotective agents with known adverse effects. In this study, we assessed the carotenoid-producing abilities of strains from Antarctic Peninsula soils and the photoprotective carotenoid action on UV irradiation resistance. Among 20 evaluated strains, one exhibited significant carotenoid production and it was identified through genomic analysis as a likely novel sp. strain, LAPM80. This strain's genome revealed the presence of genes coding for the biosynthesis of decaprenoxanthin C50 carotenoid. The LAPM80 strain exhibited enhanced resistance against UV-B irradiation, correlating with increased total carotenoid production in its stationary growth phase. Chemical characterization of the carotenoid extract identified major components as C50 carotenoids, probably decaprenoxanthin and/or sarcinaxanthin. Scanning electron microscopy revealed minimal surface changes in bacteria during carotenoid-rich phase after UV-B irradiation exposure. These findings highlight the likely ability of LAPM80 strain's C50 carotenoids to improve UV-B iiradiation resistance, indicating their potential for developing natural photoprotective compounds for the dermo-cosmetic industry.

References

Libkind D, Perez P, Sommaruga R, Dieguez M, Ferraro M, Brizzio S . Constitutive and UV-inducible synthesis of photoprotective compounds (carotenoids and mycosporines) by freshwater yeasts. Photochem Photobiol Sci. 2004; 3(3):281-6. DOI: 10.1039/b310608j. View

Bolger A, Lohse M, Usadel B . Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30(15):2114-20. PMC: 4103590. DOI: 10.1093/bioinformatics/btu170. View

Lacour T, Robert E, Lavaud J . Sustained xanthophyll pigments-related photoprotective NPQ is involved in photoinhibition in the haptophyte Tisochrysis lutea. Sci Rep. 2023; 13(1):14694. PMC: 10484918. DOI: 10.1038/s41598-023-40298-z. View

Zhao J, Li Q, Sun T, Zhu X, Xu H, Tang J . Engineering central metabolic modules of Escherichia coli for improving β-carotene production. Metab Eng. 2013; 17:42-50. DOI: 10.1016/j.ymben.2013.02.002. View

Kreft L, Botzki A, Coppens F, Vandepoele K, Van Bel M . PhyD3: a phylogenetic tree viewer with extended phyloXML support for functional genomics data visualization. Bioinformatics. 2017; 33(18):2946-2947. DOI: 10.1093/bioinformatics/btx324. View

Vila E, Hornero-Mendez D, Azziz G, Lareo C, Saravia V . Carotenoids from heterotrophic bacteria isolated from Fildes Peninsula, King George Island, Antarctica. Biotechnol Rep (Amst). 2019; 21:e00306. PMC: 6348148. DOI: 10.1016/j.btre.2019.e00306. View

Margesin R, Miteva V . Diversity and ecology of psychrophilic microorganisms. Res Microbiol. 2010; 162(3):346-61. DOI: 10.1016/j.resmic.2010.12.004. View

Mikheenko A, Prjibelski A, Saveliev V, Antipov D, Gurevich A . Versatile genome assembly evaluation with QUAST-LG. Bioinformatics. 2018; 34(13):i142-i150. PMC: 6022658. DOI: 10.1093/bioinformatics/bty266. View

Silva T, Silva Junior L, de Queiroz A, Alexandre Moreira M, de Carvalho Fraga C, de Menezes G . Pigments from Antarctic bacteria and their biotechnological applications. Crit Rev Biotechnol. 2021; 41(6):809-826. DOI: 10.1080/07388551.2021.1888068. View

10.

Flegler A, Runzheimer K, Kombeitz V, Manz A, Heidler von Heilborn D, Etzbach L . sp. nov., a pink-coloured organism isolated from cheese made of cow's milk. Int J Syst Evol Microbiol. 2020; 70(5):3027-3036. DOI: 10.1099/ijsem.0.004125. View

11.

Barreto J, Casanova L, Junior A, Pinheiro Pereira Reis-Mansur M, Vermelho A . Microbial Pigments: Major Groups and Industrial Applications. Microorganisms. 2023; 11(12). PMC: 10745774. DOI: 10.3390/microorganisms11122920. View

12.

Meier-Kolthoff J, Goker M . TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun. 2019; 10(1):2182. PMC: 6522516. DOI: 10.1038/s41467-019-10210-3. View

13.

Silva L, Crevelin E, Souza D, Lacerda-Junior G, Oliveira V, Ruiz A . Actinobacteria from Antarctica as a source for anticancer discovery. Sci Rep. 2020; 10(1):13870. PMC: 7431910. DOI: 10.1038/s41598-020-69786-2. View

14.

Letunic I, Bork P . Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016; 44(W1):W242-5. PMC: 4987883. DOI: 10.1093/nar/gkw290. View

15.

Wagener S, Volker T, De Spirt S, Ernst H, Stahl W . 3,3'-Dihydroxyisorenieratene and isorenieratene prevent UV-induced DNA damage in human skin fibroblasts. Free Radic Biol Med. 2012; 53(3):457-63. DOI: 10.1016/j.freeradbiomed.2012.05.022. View

16.

Netzer R, Stafsnes M, Andreassen T, Goksoyr A, Bruheim P, Brautaset T . Biosynthetic pathway for γ-cyclic sarcinaxanthin in Micrococcus luteus: heterologous expression and evidence for diverse and multiple catalytic functions of C(50) carotenoid cyclases. J Bacteriol. 2010; 192(21):5688-99. PMC: 2953688. DOI: 10.1128/JB.00724-10. View

17.

Heider S, Peters-Wendisch P, Wendisch V, Beekwilder J, Brautaset T . Metabolic engineering for the microbial production of carotenoids and related products with a focus on the rare C50 carotenoids. Appl Microbiol Biotechnol. 2014; 98(10):4355-68. DOI: 10.1007/s00253-014-5693-8. View

18.

Mohanty S, Mahawar H, Bajpai A, Dubey G, Parmar R, Atoliya N . Methylotroph bacteria and cellular metabolite carotenoid alleviate ultraviolet radiation-driven abiotic stress in plants. Front Microbiol. 2023; 13:899268. PMC: 9853530. DOI: 10.3389/fmicb.2022.899268. View

19.

Styczynski M, Rogowska A, Gieczewska K, Garstka M, Szakiel A, Dziewit L . Genome-Based Insights into the Production of Carotenoids by Antarctic Bacteria, sp. ANT_H30 and sp. ANT_H53B. Molecules. 2020; 25(19). PMC: 7582328. DOI: 10.3390/molecules25194357. View

20.

Mukhia S, Khatri A, Acharya V, Kumar R . Comparative genomics and molecular adaptational analysis of Arthrobacter from Sikkim Himalaya provided insights into its survivability under multiple high-altitude stress. Genomics. 2020; 113(1 Pt 1):151-158. DOI: 10.1016/j.ygeno.2020.12.001. View