Abstract
Interest in Antarctic fungi has grown due to their resilience in harsh environments, suggesting the presence of valuable compounds from its organisms, such as those presenting photoprotective potential, since this environment suffers the most dangerous UV exposure in the world. Therefore, this research aimed to assess the photoprotective potential of compounds from sustainable marine sources, specifically seaweed-derived fungi from Antarctic continent. These studies led to discovery of photoprotective and antioxidant properties of metabolites from Arthrinium sp., an endophytic fungus from Antarctic brown algae Phaeurus antarcticus. From crude extract, fractions A-I were obtained and compounds 1–6 isolated from E and F fractions, namely 3-Hydroxybenzyl alcohol (1), (-)-orthosporin (2), norlichexanthone (3), anomalin B (4), anomalin A (5), and agonodepside B (6). Compounds 1, 2, and 6 were not previously reported in Arthrinium. Fraction F demonstrated excellent absorbance in both UVA and UVB regions, while compound 6 exhibited lower UVB absorbance, possibly due to synergistic effects. Fraction F and compound 6 displayed photostability and were non-phototoxic to HaCaT cells. They also exhibited antioxidant activity by reducing intracellular ROS production induced by UVA in keratinocyte monolayers and reconstructed human skin models (resulting in 34.6% and 30.2% fluorescence reduction) and did not show irritation potential in HET-CAM assay. Thus, both are promising candidates for use in sunscreens. It is noted that Fraction F does not require further purification, making it advantageous, although clinical studies are necessary to confirm its potential applicability for sunscreen formulations.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
The raw data supporting the information of this article will be made available by the authors upon request.
References
Abdel-Lateff A, Klemke C, König GM, Wright AD (2003) Two new xanthone derivatives from the algicolous marine fungus Wardomyces anomalus. J Nat Prod 66:706–708. https://doi.org/10.1021/np020518b
Afaq F, Zaid MA, Khan N, Dreher M, Mukhtar H (2009) Protective effect of pomegranate-derived products on UVB-mediated damage in human reconstituted skin. Exp Dermatol 18:553–561. https://doi.org/10.1111/j.1600-0625.2008.00829.x
Afonso S, Horita K, Sousa e Silva JP, Almeida IF, Amaral MH, Lobão PA, Costa PC, Miranda MS, Esteves da Silva JC, Sousa Lobo JM (2014) Photodegradation of avobenzone: stabilization effect of antioxidants. J Photochem Photobiol B 140:36–40. https://doi.org/10.1016/j.jphotobiol.2014.07.004
Alfaro C, Urios A, González MC, Moya P, Blanco M (2003) Screening for metabolites from Penicillium novae-zeelandiae displaying radical-scavenging activity and oxidative mutagenicity: isolation of gentisyl alcohol. Mutat Res 539:187–194. https://doi.org/10.1016/s1383-5718(03)00166-9
Badiali C, Petruccelli V, Brasili E, Pasqua G (2023) Xanthones: biosynthesis and trafficking in plants. Fungi Lichens Plants 12(4):694. https://doi.org/10.3390/plants12040694
Bedi A, Gupta MK, Conlan XA, Cahill DM, Deshmukh SK (2021) Chapter 2 - Endophytic and marine fungi are potential sources of antioxidants. In: Sharma VK, Shah MP, Parmar S, Kumar A (eds) Fungi Bio-Prospects in Sustainable Agriculture, Environment and Nano-technology. Academic Press, Cambridge
Bedoux G, Hardouin K, Burlot AS, Bourgougnon N (2014) Bioactive components from seaweeds: cosmetic applications and future development. Adv Bot Res 71:345–378. https://doi.org/10.1016/B978-0-12-408062-1.00012-3
Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2013) GenBank. Nucleic Acids Res 41:D36-424. https://doi.org/10.1093/nar/gks1195
Birch AJ, Donovan FW (1953) Studies in relation to biosynthesis. I. Some possible routes to derivatives of orcinol and phloroglucinol. Aust J Chem 6:360–368. https://doi.org/10.1071/CH9530360
Cao S, Lee AS, Huang Y, Flotow H, Ng S, Butler MS, Buss AD (2002) Agonodepsides A and B: two new depsides from a filamentous fungus F7524. J Nat Prod 65:1037–1038. https://doi.org/10.1021/np010626i
Castenholz RW (1988) [3] Culturing methods for cyanobacteria. Methods Enzymol 167:68. https://doi.org/10.1016/0076-6879(88)67004-2
Ceridono M, Tellner P, Bauer D, Barroso J, Alépée N, Corvi R, De Smedt A, Fellows MD, Gibbs NK, Heisler E, Jacobs A, Jirova D, Jones D, Kandárová H, Kasper P, Akunda JK, Krul C, Learn D, Wilcox P (2012) The 3T3 neutral red uptake phototoxicity test: practical experience and implications for phototoxicity testing-the report of an ECVAM-EFPIA workshop. Regul Toxicol Pharmacol 63:480–488. https://doi.org/10.1016/j.yrtph.2012.06.001
Cordero RR, Feron S, Damiani A, Redondas A, Carrasco J, Sepúlveda E, Jorquera J, Fernandoy F, Llanillo P, Rowe PM, Seckmeyer G (2022) Persistent extreme ultraviolet irradiance in Antarctica despite the ozone recovery onset. Sci Rep 12:1266. https://doi.org/10.1038/s41598-022-05449-8
DiNardo JC, Downs CA (2018) Dermatological and environmental toxicological impact of the sunscreen ingredient oxybenzone/benzophenone-3. J Cosmet Dermatol 17:15–19. https://doi.org/10.1111/jocd.12449
Ding J, Wu B, Chen L (2022) Application of marine microbial natural products in cosmetics. Front Microbiol 13:892505. https://doi.org/10.3389/fmicb.2022.892505
dos Santos GS, Teixeira TR, Colepicolo P, Debonsi HM (2021) Natural products from the poles: structural diversity and biological activities. Rev Bras Farmacog 31(5):531–560. https://doi.org/10.1007/s43450-021-00203-z
El-Seedi HR, El-Barbary MA, El-Ghorab DM, Bohlin L, Borg-Karlson AK, Göransson U, Verpoorte R (2010) Recent insights into the biosynthesis and biological activities of natural xanthones. Curr Med Chem 17:854–901. https://doi.org/10.2174/092986710790712147
Fernandes A, Da S, Alencar AS, Evangelista H, Mazzei JL, Felzenszwalb I (2015) Photoprotective and toxicological activities of extracts from the Antarctic moss Sanionia uncinata. Pharmacogn Mag 11(41):38–43. https://doi.org/10.4103/0973-1296.149701
Fivenson D, Sabzevari N, Qiblawi S, Blitz J, Norton BB, Norton SA (2020) Sunscreens: UV filters to protect us: Part 2-Increasing awareness of UV filters and their potential toxicities to us and our environment. Int J Womens Dermatol 7:45–69. https://doi.org/10.1016/j.ijwd.2020.08.008
Gaspar LR, Maia Campos PMBG (2006) Evaluation of the photostability of different UV filter combinations in a sunscreen. Int J Pharm 307:123–128. https://doi.org/10.1016/j.ijpharm.2005.08.029
Gaspar LR, Tharmann J, Maia Campos PMBG, Liebsch M (2013) Skin phototoxicity of cosmetic formulations containing photounstable and photostable UV-filters and vitamin a palmitate. Toxicol in Vitro 27:418–425. https://doi.org/10.1016/j.tiv.2012.08.006
Gremaud G, Tabacchi R (1994) Isocoumarins of the Fungus Ceratocystis Fimbriata coffea. Nat Prod Let 5(2):95–103. https://doi.org/10.1080/10575639408044041
He H, Li A, Li S, Tang J, Li L, Xiong L (2021) Natural components in sunscreens: Topical formulations with sun protection factor (SPF). Biomed Pharmacother 134:111161. https://doi.org/10.1016/j.biopha.2020.111161
Heo YM, Kim K, Ryu SM, Kwon SL, Park MY, Kang JE, Kim J-J (2018) Diversity and ecology of marine algicolous arthrinium species as a source of bioactive natural products. Mar Drugs 16(12):508. https://doi.org/10.3390/md16120508
Kalyanaraman B, Darley-Usmar V, Davies KJ, Dennery PA, Forman HJ, Grisham MB, Mann GE, Moore K, Roberts LJ 2nd, Ischiropoulos H (2012) Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med 52:1–6. https://doi.org/10.1016/j.freeradbiomed.2011.09.030
Karlsson I, Hillerström L, Stenfeldt AL, Mårtensson J, Börje A (2009) Photodegradation of dibenzoylmethanes: potential cause of photocontact allergy to sunscreens. Chem Res Toxicol 22(11):1881–1892. https://doi.org/10.1021/tx900284e
Kealey JT, Craig JP, Barr PJ (2021) Identification of a lichen depside polyketide synthase gene by heterologous expression in Saccharomyces cerevisiae. Metab Eng Commun 13:e00172. https://doi.org/10.1016/j.mec.2021.e00172
Le Pogam P, Boustie J (2016) Xanthones of lichen source: a 2016 update. Molecules 21:294. https://doi.org/10.3390/molecules21030294
Lee M, Hwang JH, Lim KM (2017) Alternatives to In Vivo Draize rabbit eye and skin irritation tests with a focus on 3D reconstructed human cornea-like epithelium and epidermis models. Toxicol Res 33:191–203. https://doi.org/10.5487/TR.2017.33.3.191
Legaz EM, de Armas R, Vicente C (2011) Bioproduction of depsidones for pharmaceutical purposes. In: Rundfeldt C (ed) Drug development – a case study based insight into modern strategies. Rijeka, In Tech
Li G, Dickschat JS, Guo YW (2020) Diving into the world of marine 2,11-cyclized cembranoids: a summary of new compounds and their biological activities. Nat Prod Rep 37:1367–1383. https://doi.org/10.1039/D0NP00016G
Liebsch M, Spielmann H, Pape W, Krul C, Deguercy A, Eskes C (2005) UV-induced effects. Altern Lab Anim 33:131–146. https://doi.org/10.1177/026119290503301s14
Maia Campos PMBG, Benevenuto CG, Calixto LS, Melo MO, Pereira KC, Gaspar LR (2019) Spirulina, Palmaria Palmata, Cichorium Intybus, and Medicago Sativa extracts in cosmetic formulations: an integrated approach of in vitro toxicity and in vivo acceptability studies. Cutan Ocul Toxicol 38:1–25. https://doi.org/10.1080/15569527.2019.1579224
Marionnet C, Pierrard C, Golebiewski C, Bernerd F (2014) Diversity of biological effects induced by longwave UVA rays (UVA1) in reconstructed skin. PLoS ONE 9:e105263. https://doi.org/10.1371/journal.pone.0105263
Mitchelmore CL, Burns EE, Conway A, Heyes A, Davies IA (2021) A critical review of organic ultraviolet filter exposure, hazard, and risk to corals. Environ Toxicol Chem 40:967–988. https://doi.org/10.1002/etc.4948
Nash JF (2014) Tanner PR Relevance of UV filter/sunscreen product photostability to human safety. Photodermatol Photoimmunol Photomed 30:88–95. https://doi.org/10.1111/phpp.12113
Noor AO, Almasri DM, Bagalagel AA, Abdallah HM, Mohamed SGA, Mohamed GA, Ibrahim SRM (2020) Naturally occurring isocoumarins derivatives from endophytic fungi: sources, isolation, structural characterization, biosynthesis, and biological activities. Molecules 25:395. https://doi.org/10.3390/molecules25020395
Núñez-Pons L, Avila C, Romano G, Verde C, Giordano D (2018) UV-protective compounds in marine organisms from theSouthern Ocean. Mar Drugs 16(9):336. https://doi.org/10.3390/md16090336
Ogaki MB, de Paula MT, Ruas D, Pellizzari FM, García-Laviña CX, Rosa LH (2019) Marine fungi associated with Antarctic Macroalgae. In: Castro-Sowinski S (ed) The ecological role of micro-organisms in the Antarctic environment. Springer, Cham
OECD- Organization for Economic Co-operation and Development, OECD guidelines for testing of chemicals test n°. 432: In vitro 3T3 NRU Phototoxicity Test (2019b) Available at: https://doi.org/10.1787/9789264071162-en Accessed: 22 Jun 22
Overgaard ML, Aalborg T, Zeuner EJ, Westphal KR, Lau F, Nielsen VS, Carstensen KB, Hundebøll EA, Westermann TA, Rathsach GG, Sørensen JL, Frisvad JC, Wimmer R, Sondergaard TE (2023) Quick guide to secondary metabolites from Apiospora and Arthrinium. Fungal Biol Rev 43:100288. https://doi.org/10.1016/j.fbr.2022.10.001
Pal S, Chatare V, Pal M (2011) Isocoumarin and its derivatives: an overview on their synthesis and applications. Curr Org Chem 15:782. https://doi.org/10.2174/138527211794518970
Pennacchi PC, de Almeida ME, Gomes OL, Faião-Flores F, de Araújo Crepaldi MC, Dos Santos MF, de Moraes Barros SB, Maria-Engler SS (2015) Glycated reconstructed human skin as a platform to study the pathogenesis of skin aging. Tissue Eng Part A 21:2417–2425. https://doi.org/10.1089/ten.tea.2015.0009
Pinto da Silva L, Ferreira PJ, Duarte DJ, Miranda MS, Esteves da Silva JC (2014) Structural, energetic, and UV-Vis spectral analysis of UVA filter 4-tert-butyl-4’-methoxydibenzoylmethane. J Phys Chem A 118:1511–1518. https://doi.org/10.1021/jp4123375
Pintos Á, Alvarado P (2021) Phylogenetic delimitation of Apiospora and Arthrinium. Fungal Sys and Evolution 7(1):197–221. https://doi.org/10.3114/fuse.2021.07.10
Pivetta TP, Silva LBD, Kawakami CM, Araújo MM, Del Lama MPF, de M, Naal RMZG, Maria-Engler SS, Gaspar LR, Marcato PD, (2019) Topical formulation of quercetin encapsulated in natural lipid nanocarriers: Evaluation of biological properties and phototoxic effect. J Drug Deliv Sci Technol 53:1–11. https://doi.org/10.1016/j.jddst.2019.101148
Rangel KC, Villela LZ, de Pereira K, C, Colepicolo P, Debonsi HM, Gaspar LR, (2020) Assessment of the photoprotective potential and toxicity of Antarctic red macroalgae extracts from Curdiea racovitzae and Iridaea cordata for cosmetic use. Algal Res 50:1–13. https://doi.org/10.1016/j.algal.2020.101984
Rasmussen C, Gratz K, Liebel F, Southall M, Garay M, Bhattacharyya S, Simon N, Vander Zanden M, Van Winkle K, Pirnstill J, Pirnstill S, Comer A, Allen-Hoffmann BL (2010) The StrataTest® human skin model, a consistent in vitro alternative for toxicological testing. Toxicol in Vitro 24:2021–2029. https://doi.org/10.1016/j.tiv.2010.07.027
Roberts JC (1961) Naturally occurring xanthones. Chem Rev 61:591–605. https://doi.org/10.1021/cr60214a003
Roguet R, Régnier M, Cohen C, Dossou KG, Rougier A (1994) The use of in vitro reconstituted human skin in dermotoxicity testing. Toxicol in Vitro 8:635–639. https://doi.org/10.1016/0887-2333(94)90033-7
Rosic NN (2021) Recent advances in the discovery of novel marine natural products and mycosporine-like amino acid UV-absorbing compounds. Appl Microbiol Biotechnol 105(19):7053–7067. https://doi.org/10.1007/s00253-021-11467-9
Saeed A (2016) Isocoumarins, miraculous natural products blessed with diverse pharmacological activities. Eur J Med Chem 116:290–317. https://doi.org/10.1016/j.ejmech.2016.03.025
Saewan N, Jimtaisong A (2015) Natural products as photoprotection. J Cosmet Dermatol 14:47–63. https://doi.org/10.1111/jocd.12123
Sarasan M, Puthumana J, Job N, Han J, Lee JS, Philip R (2017) Marine algicolous endophytic fungi—a promising drug resource of the era. J Microbiol Biotechnol 27:1039–1052. https://doi.org/10.4014/jmb.1701.01036
Scarpin MS, Kawakami CM, Rangel KC, Pereira KC, Benevenuto CG, Gaspar LR (2021) Effects of UV-filter photostabilizers in the photostability and phototoxicity of vitamin A palmitate combined with avobenzone and octyl methoxycinnamate. Photochem Photobiol 97:700–709. https://doi.org/10.1111/php.13407
SCCS - Scientific Committee on Consumer Safety, The SCCS notes of guidance for the testing of cosmetic ingredients and their safety evaluation (2018). https://ec.europa.eu/health/sites/health/files/scientific_committees/consumer_safety/docs/sccs_o_224.pdf Accessed: 22 Jun 22
Silva EP, Herminio VLdQ, Motta DN, Soares MBP, Rodrigues LdAP, Viana JD, Freitas FA, Silva APG, Souza FDCdA, Vilas Boas EVdB (2022) The role of phenolic compounds in metabolism and their antioxidant potential. Res Soc Dev. 11(10):297111031750. https://doi.org/10.33448/rsd-v11i10.31750
Souza EL, Albuquerque TMR, Santos AS, Massa NML, De Alves JLB (2019) Potential interactions among phenolic compounds and probiotics for mutual boosting of their health-promoting properties and food functionalities—a review. Crit Rev Food Sci Nutr 59(10):1–15. https://doi.org/10.1080/10408398.2018.1425285
Tavares RSN, Kawakami CM, Pereira KC, Amaral do GT, Benevenuto CG, Maria-Engler SS, Colepicolo P, Debonsi HM, Gaspar LR (2020a) Fucoxanthin for topical administration, a phototoxic vs photoprotective potential in a tiered strategy assessed by in vitro methods. Antioxidants 9:328. https://doi.org/10.3390/antiox9040328
Tavares RSN, Maria-Engler SS, Colepicolo P, Debonsi HM, Schäfer-Korting M, Marx U, Gaspar LR, Zoschke C (2020b) Skin irritation testing beyond tissue viability: fucoxanthin effects on inflammation, homeostasis, and metabolism. Pharmaceutics 12:136. https://doi.org/10.3390/pharmaceutics12020136
Teixeira TR, dos Santos GS, Turatti ICC, Paziani MH, von Kress MR, Z, Colepicolo P, Debonsi HM, (2019) Characterization of the lipid profile of Antarctic brown seaweeds and their endophytic fungi by gas chromatography–mass spectrometry (GC–MS). Polar Biol 42:1431–1444. https://doi.org/10.1007/s00300-019-02529-w
Thiesen LC, Baccarin T, Fischer-Muller AF, Meyre-Silva C, Couto AG, Bresolin TM, Santin JR (2017a) Photochemoprotective effects against UVA and UVB irradiation and photosafety assessment of Litchi chinensis leaves extract. J Photochem Photobiol B 167:200–207. https://doi.org/10.1016/j.jphotobiol.2016.12.033
Vega J, Schneider G, Moreira BR, Herrera C, Bonomi-Barufi J, Figueroa FL (2021) Mycosporine-like amino acids from red macroalgae: UV-photoprotectors with potential cosmeceutical applications. App Sci 11(11):5112. https://doi.org/10.3390/app11115112
Vitale GA, Coppola D, Palma Esposito F, Buonocore C, Ausuri J, Tortorella E, de Pascale D (2020) Antioxidant molecules from marine fungi: methodologies and perspectives. Antioxidants 9(12):1183. https://doi.org/10.3390/antiox9121183
Wang SQ, Stanfield JW, Osterwalder U (2008) In vitro assessments of UVA protection by popular sunscreens available in the United States. J Am Acad Dermatol 59(6):934–942. https://doi.org/10.1016/j.jaad.2008.07.043
Watkins YSD, Sallach JB (2021) Investigating the exposure and impact of chemical UV filters on coral reef ecosystems: review and research gap prioritization. Integr Environ Assess Manag 17:967–981. https://doi.org/10.1002/ieam.4411
White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: a guide to methods and applications. Academic Press, Cambridge, pp 315–322
Zhang Y, Shah P, Wu F, Liu P, You J, Goss G (2021) Potentiation of lethal and sub-lethal effects of benzophenone and oxybenzone by UV light in zebrafish embryos. Aquat Toxicol 235:105835. https://doi.org/10.1016/j.aquatox.2021.105835
Acknowledgements
The authors are thankful to University of São Paulo for providing access to necessary resources, the financial and fellowship support from the Brazilian research funding agencies Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de desenvolvimento Científico e Tecnológico (CNPq). The Department of Biomolecular Sciences and the Núcleo de Pesquisas em Produtos Naturais e Sintéticos–NPPNS are acknowledged. In the final review of the manuscript, the authors utilized an AI-powered language model known as CHAT-GPT for assistance, primarily focusing on English grammar, vocabulary, and minor content review.
Funding
This study had financial and logistic support from the Brazilian Antarctic Program PROANTAR/MCTI/CNPq N°64/2013), Brazilian Marine Force, National Institute of Science and Technology (INCT:BioNat), Grant #465637/2014-0, and the State of São Paulo Research Foundation (FAPESP), Grant #2014/50926-0 and 2017/03552-5.
Author information
Authors and Affiliations
Contributions
ACJ: Conceptualization, Methodology, Formal analysis, Investigation, Data Curation, Writing—Original Draft, Review and Editing, Visualization GSS, TRT, AJPG, CBSA, LT and KCP: Methodology, Formal analysis, Data Curation, Review and Editing MRZK: Conceptualization, Resources, Supervision LRG: Conceptualization, Resources, Supervision, Review and Editing, Project Administration PC: Resources, Project administration, Funding Acquisition HMD: Conceptualization, Resources, Review and Editing, Supervision, Project administration, Funding acquisition.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethics approval
All experimental procedures involving humans were performed in accordance with the principles of the Declaration of Helsinki and were approved by the Human Research Ethics Committee of School of Pharmaceutical Sciences of Ribeirão Preto, São Paulo, Brazil (CAAE number 31758619.5.0000.5403). The written informed consent was signed by all the donors or their parents or legal guardian.
Additional information
Communicated by Yusuf Akhter.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Jordão, A.C., dos Santos, G.S., Teixeira, T.R. et al. Assessment of the photoprotective potential and structural characterization of secondary metabolites of Antarctic fungus Arthrinium sp.. Arch Microbiol 206, 35 (2024). https://doi.org/10.1007/s00203-023-03756-w
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-023-03756-w