The potency of yellow pigment extract from the marine bacterium Pseudomonas oryzihabitans SAB E-3 as an antioxidant agent

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DELFIANI ANGGIAS PUTRI
RIKA INDRI ASTUTI
ARIS TRI WAHYUDI

Abstract

Abstract. Putri DA, Astuti RI, Wahyudi AT. 2024. The potency of yellow pigment extract from the marine bacterium Pseudomonas oryzihabitans SAB E-3 as an antioxidant agent. Biodiversitas 25: 2565-2575. Metabolic processes in cells can produce byproducts in the form of Reactive Oxygen Species (ROS). Excessive amounts of ROS are one of the causes of oxidative stress. Antioxidants are known to act as free radical-scavenging compounds. Pigment-producing bacteria associated with sponges have been widely reported to have antioxidant compounds. In this study, the marine bacterium Pseudomonas oryzihabitans SAB E-3 produced intracellular yellow pigments with potential antioxidant activity. Therefore, this study aimed to assess the in vitro antioxidant and mitochondrial activity at the cellular level and identify chemical compounds. The intracellular pigments produced by P. oryzihabitans SAB E-3 were extracted using methanol, acetone, chloroform, and ethyl acetate. The methanol pigment extract contained the highest number of phenolic and flavonoid compounds, which may have contributed to its antioxidant activity. Furthermore, the active fraction obtained from the bioautographic TLC and harvested using preparative TLC had stronger antioxidant activity against DPPH radicals (75.71 µg/mL) than the crude pigment extract. However, the ABTS radical-reducing activity was lower (226.59 µg/mL) than the crude pigment extract. The maximum wavelength of the pigment extract was 453 nm, indicating the presence of carotenoids. In addition, the lowest concentration of the crude pigment extract (50 µg/mL) and selected active fractions (18.75 µg/mL) increased yeast Schizosaccharomyces pombe ARC039 tolerance to oxidative stress and induced mitochondrial activity. Active fraction one extract analyzed using LC-MS/MS contained piceatannol, resveratrol, isorhapontigenin, isoliquiritigenin, liquiritin, and 2-Omethylisohemigossylic acid lactone, which may contribute to its antioxidant activity. Therefore, the yellow pigment extract and the active fraction produced by P. oryzihabitans SAB E-3 are potential candidates for natural antioxidant sources.

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References
Abubakar H, Wahyudi AT, Yuhana M. 2011. Skrining bakteri yang berasosiasi dengan spons Jaspis sp. sebagai penghasil senyawa antimikroba. Indones J Mar Sci 16(1): 35-40. DOI: 10.14710/ik.ijms.16.1.35-40. [Indonesian]
Abubakar H, Astuti RI, Listyowati S, Batubara I, Wahyudi AT. 2022. An orange pigment from the marine bacterium Paracoccus haeundaensis SAB E11 as a prospective source of natural antioxidants. Biodiversitas 23(9): 4730–4737. DOI: 10.13057/biodiv/d230940.
Agarwal H, Bajpai S, Mishra A, Kohli I, Varma A, Fouillaud M, Dufossé L, Joshi NC. 2023. Bacterial pigments and their multifaceted roles in contemporary biotechnology and pharmacological applications. Microorganisms 11(3): 614. DOI: 10.3390/microorganisms11030614.
Asati V, Srivastava A, Mukherjee S, Sharma PK. 2021. Comparative analysis of antioxidant and antiproliferative activities of crude and purified flavonoid enriched fractions of pods/seeds of two desert legumes Prosopis cineraria and Cyamopsis tetragonoloba. Heliyon 7(6): e07304. DOI: 10.1016/j.heliyon.2021.e07304.
Ashenafi EL, Nyman MC, Shelley JT, Mattson NS. 2023. Spectral properties and stability of selected carotenoid and chlorophyll compounds in different solvent systems. Food Chem Adv 2(1): 100178. DOI: 10.1016/j.focha.2022.100178.
Astuti RI, Prastya ME, Batubara I, Budiarti E, Ilmiyawati A. 2021. Antiaging and antioxidant bioactivities of asteraceae plant fractions on the cellular functions of the yeast Schizosaccharomyces pombe. Adv Pharmacol Pharm Sci 2021(2): 1-12. DOI: 10.1155/2021/2119634.
Bardaweel SK, Gul M, Alzweiri M, Ishaqat A, Alsalamat HA, Bashatwah RM. 2018. Reactive oxygen species: The dual role in physiological and pathological conditions of the human body. Eurasian J Med 50(3): 193–201. DOI: 10.5152/eurasianjmed.2018.17397.
Branduardi P, Fossati T, Sauer M, Pagani R, Mattanovich D, Porro D. 2007. Biosynthesis of vitamin C by yeast leads to increased stress resistance. PLoS One 2(10): e1092. DOI: 10.1371/journal.pone.0001092.
Cahlia U, Astuti RI, Nomura J, Wahyudi AT. 2023. Antioxidant properties of active fraction extract derived from yellow-red pigment produced by the marine sponge-associated bacterium Bacillus haikouensis AGS112 and identification of related compounds. Hayati 30(5): 874–884. DOI: 10.4308/hjb.30.5.874-884.
Chandra P, Sharma RK, Arora DS. 2020. Antioxidant compounds from microbial sources: A review. Food Res Int 129(2): 108849. DOI: 10.1016/j.foodres.2019.108849.
Choksi J, Vora J, Shrivastava N. 2020. Bioactive pigments from isolated bacteria and its antibacterial, antioxidant and sun protective application useful for cosmetic products. Indian J Microbiol 60(3): 379–382. DOI: 10.1007/s12088-020-00870-x.
Corinaldesi C, Barone G, Marcellini F, Dell’Anno A, Danovaro R. 2017. Marine microbial-derived molecules and their potential use in cosmeceutical and cosmetic products. Mar Drugs 15(4): 118. DOI: 10.3390/md15040118.
Dai J, Mumper RJ. 2010. Plant phenolics: Extraction, analysis and their antioxidant and anticancer properties. Molecules 15(10): 7313–7352. DOI: 10.3390/molecules15107313.
Dawoud TM, Alharbi NS, Theruvinthalakal AM, Thekkangil A, Kadaikunnan S, Khaled JM, Almanaa TN, Sankar K, Innasimuthu GM, Alanzi KF, et al. 2020. Characterization and antifungal activity of the yellow pigment produced by a Bacillus sp. DBS4 isolated from the lichen Dirinaria agealita. Saudi J Biol Sci 27(5): 1403–1411. DOI: 10.1016/j.sjbs.2019.11.031.
Dilova I, Easlon E, Lin SJ. 2007. Calorie restriction and the nutrient sensing signaling pathways. Cell Mol Life Sci 64(6): 752–767. DOI: 10.1007/s00018-007-6381-y.
Fauzya AF, Astuti RI, Mubarik NR. 2019. Effect of ethanol-derived clove leaf extract on the oxidative stress response in yeast Schizosaccharomyces pombe. Int J Microbiol 2019: 1-7. DOI: 10.1155/2019/2145378.
Furuya T, Imaki N, Shigei K, Sai M, Kino K. 2019. Isolation and characterization of Gram-negative and Gram-positive bacteria capable of producing piceatannol from resveratrol. Appl Microbiol Biotechnol 103(14): 5811–5820. DOI: 10.1007/s00253-019-09875-z.
Hibasami H, Saitoh K, Katsuzaki H, Imai K, Aratanechemuge Y, Komiya T. 2004. 2-O-methylisohemigossylic acid lactone, a sesquiterpene, isolated from roots of mokumen (Gossampinus malabarica) induces cell death and morphological change indicative of apoptotic chromatin condensation in human promyelotic leukemia HL-60 cells. Int J Mol Med 14(6): 1029-1033. DOI: 10.3892/ijmm.14.6.1029.
Kusmita L, Nur Prasetyo Edi A, Dwi Franyoto Y, Mutmainah, Haryanti S, Dwi Retno Nurcahyanti A. 2023. Sun protection and antibacterial activities of carotenoids from the soft coral Sinularia sp. symbiotic bacteria from Panjang Island, North Java Sea. Saudi Pharm J 31(8): 101680. DOI: 10.1016/j.jsps.2023.06.013.
Leonov A, Feldman R, Piano A, Arlia-Ciommo A, Lutchman V, Ahmadi M, Elsaser S, Fakim H, Heshmati-Moghaddam M, Hussain A, et al. 2017. Caloric restriction extends yeast chronological lifespan via a mechanism linking cellular aging to cell cycle regulation, maintenance of a quiescent state, entry into a non-quiescent state and survival in the non-quiescent state. Oncotarget. 8(41): 69328–69350. DOI: 10.18632/oncotarget.20614.
Lesmana D, Andrianto D, Astuti RI. 2021. Antiaging properties of the ethanol fractions of clove (Syzygium aromaticum L.) bud and leaf at the cellular levels: Study in yeast Schizosaccharomyces pombe. Sci Pharm 89(4): 45. DOI: 10.3390/scipharm89040045.
Li B, Skinner C, Castello PR, Kato M, Easlon E, Xie L, Li T, Lu SP, Wang C, Tsang F, Poyton RO, Lin SJ. 2011. Identification of potential calorie restriction-mimicking yeast mutants with increased mitochondrial respiratory chain and nitric oxide levels. J Aging Res 2011(2): 673185. DOI: 10.4061/2011/673185.
Li Z, Chen X, Liu G, Li J, Zhang J, Cao Y, Miao J. 2021. Antioxidant activity and mechanism of resveratrol and polydatin isolated from mulberry (Morus alba L.). Molecules 26(24): 7574. DOI: 10.3390/molecules26247574.
Lu Y, Wang AH, Shi P, Zhang H. 2017. A theoretical study on the antioxidant activity of piceatannol and isorhapontigenin scavenging nitric oxide and nitrogen dioxide radicals. PLoS One 12(1): e0169773. DOI: 10.1371/journal.pone.0169773.
Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Wade WG. 1998. design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64(2): 795–799. DOI: 10.1128/AEM.64.2.795-799.1998.
Marchut-Miko?ajczyk O, Chlebicz M, Kawecka M, Michalak A, Prucnal F, Nielipinski M, Filipek J, Jankowska M, Perek Z, Dro?d?y?ski P, et al. 2023. Endophytic bacteria isolated from Urtica dioica L.- preliminary screening for enzyme and polyphenols production. Microb Cell Fact 22(1): 169. DOI: 10.1186/s12934-023-02167-2.
Meda A, Lamien CE, Romito M, Millogo J, Nacoulma OG. 2005. Determination of the total phenolic, flavonoid and proline contents in Burkina Fasan honey, as well as their radical scavenging activity. Food Chem 91(3): 571–577. DOI: 10.1016/j.foodchem.2004.10.006.
Mehmood A, Javid S, Khan MF, Ahmad KS, Mustafa A. 2022. In vitro total phenolics, total flavonoids, antioxidant and antibacterial activities of selected medicinal plants using different solvent systems. BMC Chem 16(1). DOI: 10.1186/s13065-022-00858-2.
Mesrian DK, Purwaningtyas WE, Astuti RI, Hasan AEZ, Wahyudi AT. 2021. Methanol pigment extracts derived from two marine actinomycetes exhibit antibacterial and antioxidant activities. Biodiversitas 22(10): 4440–4447. DOI: 10.13057/BIODIV/D221037.
Muflihah YM, Gollavelli G, Ling YC. 2021. Correlation study of antioxidant activity with phenolic and flavonoid compounds in 12 indonesian indigenous herbs. Antioxidants 10(10): 1530. DOI: 10.3390/antiox10101530.
Nakatani Y, Kobe A, Kuriya M, Hiroki Y, Yahagi T, Sakakibara I, Matsuzaki K, Amano T. 2017. Neuroprotective effect of liquiritin as an antioxidant via an increase in glucose-6-phosphate dehydrogenase expression on B65 neuroblastoma cells. Eur J Pharmacol 815: 381–390. DOI: 10.1016/j.ejphar.2017.09.040.
Nowak M, Tryniszewski W, Sarniak A, Wlodarczyk A, Nowak PJ, Nowak D. 2022. Concentration Dependence of Anti-and Pro-Oxidant Activity of Polyphenols as Evaluated with a Light-Emitting Fe2+-Egta-H2O2 System. Molecules 27(11): 3453. DOI: 10.3390/molecules27113453.
de Ondarza J. 2017. Ozone sensitivity and catalase activity in pigmented and non-pigmented strains of Serratia marcescens. Open Microbiol J 11(1): 12–22. DOI:10.2174/1874285801711010012.
Patkar S, Shinde Y, Chindarkar P, Chakraborty P. 2021. Evaluation of antioxidant potential of pigments extracted from Bacillus spp. and Halomonas spp. isolated from mangrove rhizosphere. Biotechnologia 102(2): 157–169. DOI: 10.5114/bta.2021.106522.
Platzer M, Kiese S, Herfellner T, Schweiggert-Weisz U, Miesbauer O, Eisner P. 2021. Common trends and differences in antioxidant activity analysis of phenolic substances using single electron transfer based assays. Molecules 26(5): 1244. DOI: 10.3390/molecules26051244.
Poddar K, Padhan B, Sarkar D, Sarkar A. 2021. Purification and optimization of pink pigment produced by newly isolated bacterial strain Enterobacter sp. PWN1. SN Appl Sci 3(1). DOI: 10.1007/s42452-021-04146-x.
Prastya ME, Astuti RI, Batubara I, Wahyudi AT. 2018. Bacillus sp. SAB E-41-derived extract shows antiaging properties via ctt1-mediated oxidative stress tolerance response in yeast Schizosaccharomyces pombe. Asian Pac J Trop Biomed 8(11): 533–539. DOI: 10.4103/2221-1691.245958.
Prastya ME, Astuti RI, Batubara I, Wahyudi AT. 2019. Antioxidant, antiglycation and in vivo antiaging effects of metabolite extracts from marine sponge-associated bacteria. Indian J Pharm Sci 81(2): 344-353. DOI: 10.36468/pharmaceutical-sciences.516.
Prastya ME, Astuti RI, Batubara I, Takagi H, Wahyudi AT. 2020a. Chemical screening identifies an extract from marine Pseudomonas sp.-PTR-08 as an anti-aging agent that promotes fission yeast longevity by modulating the Pap1–ctt1+ pathway and the cell cycle. Mol Biol Rep 47(1): 33–43. DOI: 10.1007/s11033-019-05102-0.
Prastya ME, Astuti RI, Batubara I, Takagi H, Wahyudi AT. 2020b. Natural extract and its fractions isolated from the marine bacterium Pseudoalteromonas flavipulchra STILL-33 have antioxidant and antiaging activities in Schizosaccharomyces pombe. FEMS Yeast Res 20(3): foaa014. DOI: 10.1093/femsyr/foaa014.
Rafi M, Febriany S, Wulandari P, Suparto IH, Ridwan T, Rahayu S, Siswoyo DM. 2018. Total phenolics, flavonoids, and anthocyanin contents of six Vireya Rhododendron from Indonesia and evaluation of their antioxidant activities. J Appl Pharm Sci 8(9): 49–54. DOI: 10.7324/JAPS.2018.8908.
Reddy VP, Zhu X, Perry G, Smith MA. 2009. Oxidative stress in diabetes and Alzheimer’s disease. J Alzheimers Dis 16(4): 763–774. DOI: 10.3233/JAD-2009-1013.
Riahi K, Hosni K, Raies A, Oliveira R. 2019. Unique secondary metabolites of a Streptomyces strain isolated from extreme salty wetland show antioxidant and antibacterial activities. J Appl Microbiol 127(6): 1727–1740. DOI: 10.1111/jam.14428.
Shi D, Yang J, Jiang Y, Wen L, Wang Z, Yang B. 2020. The antioxidant activity and neuroprotective mechanism of isoliquiritigenin. Free Radic Biol Med 152: 207–215. DOI: 10.1016/j.freeradbiomed.2020.03.016.
Shields HJ, Traa A, Van Raamsdonk JM. 2021. Beneficial and detrimental effects of reactive oxygen species on lifespan: A comprehensive review of comparative and experimental studies. Front Cell Dev Biol 9: 628157. DOI: 10.3389/fcell.2021.628157.
Utami LA, Wahyuni WT, Mubarik NR, Astuti RI. 2023. Endophytic bacteria of clove (Syzygium aromaticum L.) leaves produce metabolites with antioxidant and anti-aging properties. J Appl Pharm Sci 13(7): 241–250. DOI: 10.7324/JAPS.2023.93258.
Venil CK, Zakaria ZA, Ahmad WA. 2013. Bacterial pigments and their applications. Process Biochem 48(7): 1065–1079. DOI: 10.1016/j.procbio.2013.06.006.
Vladkova T, Georgieva N, Staneva A, Gospodinova D. 2022. Recent progress in antioxidant active substances from marine biota. Antioxidants 11(3): 1–27. DOI: 10.3390/antiox11030439.

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