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Applied Microbiology and Biotechnology

, Volume 103, Issue 2, pp 917–927 | Cite as

In vitro antioxidant activities of Rhodobacter sphaeroides and protective effect on Caco-2 cell line model

  • Jun An
  • Cui Yang
  • Zuming LiEmail author
  • Patricia W. Finn
  • David L. Perkins
  • Jun Sun
  • Zhihui Bai
  • Liping Gao
  • Michael Zhang
  • Difeng Ren
Applied microbial and cell physiology
  • 103 Downloads

Abstract

The present study aimed to evaluate the in vitro antioxidant activities and the protective effect of Rhodobacter sphaeroides on H2O2-induced oxidative stress in Caco-2 cells. The results showed that the antioxidant action of R. sphaeroides varied with different cell concentrations and treatments. Also, the intact cells and intracellular cell-free extracts showed better antioxidant activities. Caco-2 cell–based oxidative stress model was developed by optimizing H2O2 concentration and culture time with the half lethal dose and methyl thiazolyl tetrazolium. By increasing the activity of endogenous antioxidant enzymes superoxide dismutase, catalase, and glutathione peroxidase, upregulating the antioxidant ability of the anti-superoxide anion and anti-hydroxyl radical, R. sphaeroides, especially the mutant strain R. sphaeroides (CGMCC No. 8513), exhibited significant protective activity against H2O2-induced oxidative stress in Caco-2 cells. Taken together, R. sphaeroides (CGMCC No. 8513) exhibits strong antioxidant activities and is a candidate to be investigated as a potential probiotic in the future.

Keywords

Rhodobacter sphaeroides Antioxidant activities Oxidative stress Caco-2 cell 

Notes

Funding information

This work was supported by the China Scholarship Council Foundation (Grant Number 201708110129), the Beijing Natural Science Foundation (Grant Number 6173033), the National Natural Science Foundation of China (Grant Number 31570494), and the Beijing Municipal Commission of Education (Grant Numbers KM20131141 7007 and PXM2013_ 014209_07_ 000082). We also gratefully acknowledge the financial support of the Scientific Research Project from Facing Characteristic Discipline of Beijing Union University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Bu P, Narayanan S, Dalrymple D, Cheng X, Serajuddin ATM (2016) Cytotoxicity assessment of lipid-based self-emulsifying drug delivery system with Caco-2 cell model: Cremophor EL as the surfactant. Eur J Pharm Sci 91:162–171Google Scholar
  2. Chang CY, Wu KC, Chiang SH (2007) Antioxidant properties and protein compositions of porcine haemoglobin hydrolysates. Food Chem 100:1537–1543Google Scholar
  3. Chen P, Zhang Q, Dang H, Liu X, Tian F, Zhao J, Chen Y, Zhang H, Chen W (2014) Screening for potential new probiotic based on probiotic properties and α-glucosidase inhibitory activity. Food Control 35:65–72Google Scholar
  4. Coombes E, Jiang J, Chu XP, Inoue K, Seeds J, Branigan D, Simon RP, Xiong ZG (2011) Pathophysiologically relevant levels of hydrogen peroxide induce glutamate-independent neurodegeneration that involves activation of transient receptor potential melastatin 7 channels. Antioxid Redox Signal 14:1815–1827Google Scholar
  5. Das D, Goyal A (2015) Antioxidant activity and γ-aminobutyric acid (GABA) producing ability of probiotic Lactobacillus plantarum DM5 isolated from Marcha of Sikkim. LWT - Food Sci Technol 61:263–268Google Scholar
  6. Granafei S, Losito I, Trotta M, Agostiano A, Palmisano F, Cataldi TRI (2017) Unveiling the compositional variety of cardiolipins in Rhodobacter sphaeroides by liquid chromatography with electrospray ionization and multistage collision-induced dissociation mass spectrometry. Anal Bioanal Chem 409:5007–5018Google Scholar
  7. Gu Z, Chen D, Han Y, Chen Z, Gu F (2008) Optimization of carotenoids extraction from Rhodobacter sphaeroides. LWT - Food Sci Technol 41:1082–1088Google Scholar
  8. Han X, Gelein R, Corson N, Wade-Mercer P, Jiang J, Biswas P, Finkelstein JN, Elder A, Oberdörster G (2011) Validation of an LDH assay for assessing nanoparticle toxicity. Toxicology 287:99–104Google Scholar
  9. Han Q, Kong B, Chen Q, Sun F, Zhang H (2017) In vitro comparison of probiotic properties of lactic acid bacteria isolated from Harbin dry sausages and selected probiotics. J Funct Foods 32:391–400Google Scholar
  10. Hifney AF, Fawzy MA, Abdel-Gawad KM, Issa AA, Gomaa M (2016) In vitro comparative evaluation of antioxidant activity of hydrophobic and hydrophilic extracts from Algicolous Fungi. J Aquat Food Prod Technol 26:124–131Google Scholar
  11. Huang QL, Siu KC, Wang WQ, Cheung YC, Wu JY (2013) Fractionation, characterization and antioxidant activity of exopolysaccharides from fermentation broth of a Cordyceps sinensis fungus. Process Biochem 48:380–386Google Scholar
  12. Hutt P, Shchepetova J, Loivukene K, Kullisaar T, Mikelsaar M (2006) Antagonistic activity of probiotic lactobacilli and bifidobacteria against entero- and uropathogens. J Appl Microbiol 100:1324–1332Google Scholar
  13. Kao TH, Chen BH (2006) Functional components in soybean cake and their effects on antioxidant activity. J Agric Food Chem 54:7544–7555Google Scholar
  14. Kasai T, Nakanishi T, Ohno Y, Shimada H, Nakamura Y, Arakawa H, Tamai I (2016) Role of OATP2A1 in PGE2 secretion from human colorectal cancer cells via exocytosis in response to oxidative stress. Exp Cell Res 341:123–131Google Scholar
  15. Kellett ME, Greenspan P, Pegg RB (2018) Modification of the cellular antioxidant activity (CAA) assay to study phenolic antioxidants in a Caco-2 cell line. Food Chem 244:359–363Google Scholar
  16. Kim NY, Yim TB, Lee HY (2015) Skin anti-aging activities of bacteriochlorophyll a from photosynthetic pacteria, Rhodobacter sphaeroide. J Microbiol Biotechnol 25:1589–1598Google Scholar
  17. Kuda T, Kawahara M, Nemoto M, Takahashi H, Kimura B (2014) In vitro antioxidant and anti-inflammation properties of lactic acid bacteria isolated from fish intestines and fermented fish from the Sanriku Satoumi region in Japan. Food Res Int 64:248–255Google Scholar
  18. Laffleur F, Psenner J, Suchaoin W (2015) Permeation enhancement via thiolation: in vitro and ex vivo evaluation of hyaluronic acid-cysteine ethyl ester. J Pharm Sci 104:2153–2160Google Scholar
  19. Leite AM, Miguel MA, Peixoto RS, Ruas-Madiedo P, Paschoalin VM, Mayo B, Delgado S (2015) Probiotic potential of selected lactic acid bacteria strains isolated from Brazilian kefir grains. J Dairy Sci 98:3622–3632Google Scholar
  20. Li S, Shah NP (2016) Anti-inflammatory and anti-proliferative activities of natural and sulphonated polysaccharides from Pleurotus eryngii. J Funct Foods 23:80–86Google Scholar
  21. Li ZM, Kong LN, Hui BD, Shang XY, Gao LP, Luan N, Zhuang XL, Wang D, Bai ZH (2017) Identification and antioxidant activity of carotenoids from superfine powder of Rhodobacter Sphaeroides. Emir J Food Agric 29:833–845Google Scholar
  22. Liang R, Zhang Z, Lin S (2017) Effects of pulsed electric field on intracellular antioxidant activity and antioxidant enzyme regulating capacities of pine nut (Pinus koraiensis) peptide QDHCH in HepG2 cells. Food Chem 237:793–802Google Scholar
  23. Liu S, Zhang G, Li X, Wu P, Zhang J (2015) Enhancement of Rhodobacter sphaeroides growth and carotenoid production through biostimulation. J Environ Sci 33:21–28Google Scholar
  24. Liu XR, Cao L, Li T, Chen LL, Yu YY, Huang WJ, Liu L, Tan XQ (2017) Propofol attenuates H2O2-induced oxidative stress and apoptosis via the mitochondria- and ER-medicated pathways in neonatal rat cardiomyocytes. Apoptosis 22:639–646Google Scholar
  25. Nations FAOO, Organization WH (2006) Probiotics in food : health and nutritional properties and guidelines for evaluation. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  26. Rahal A, Kumar A, Singh V, Yadav B, Tiwari R, Chakraborty S, Dhama K (2014) Oxidative stress, prooxidants, and antioxidants: the interplay. Biomed Res Int 2014:761264:1–19Google Scholar
  27. Sabeena Farvin KH, Baron CP, Nielsen NS, Jacobsen C (2010) Antioxidant activity of yoghurt peptides: part 1-in vitro assays and evaluation in ω-3 enriched milk. Food Chem 123:1081–1089Google Scholar
  28. Sang-Hyun S, Si-Kwan K, Young-Ock K, Hyung-Don K, Yu-Su S, Yang SO, Seung-Yu K, Sang-Won L (2013) A comparison of antioxidant activity of Korean White and Red Ginsengs on H2O2-induced oxidative stress in HepG2 hepatoma cells. J Ginseng Res 37:442–450Google Scholar
  29. Sardaro A, Castagnolo M, Trotta M, Italiano F, Milano F, Cosma P, Agostiano A, Fini P (2013) Isothermal microcalorimetry of the metabolically versatile bacterium Rhodobacter sphaeroides. J Therm Anal Calorim 112:505–511Google Scholar
  30. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336Google Scholar
  31. Su C, Sun F, Cunningham RL, Rybalchenko N, Singh M (2014) ERK5/KLF4 signaling as a common mediator of the neuroprotective effects of both nerve growth factor and hydrogen peroxide preconditioning. Age 36:1–17Google Scholar
  32. Su J, Wang T, Li YY, Li J, Zhang Y, Wang Y, Wang H, Li H (2015) Antioxidant properties of wine lactic acid bacteria: Oenococcus oeni. Appl Microbiol Biotechnol 99:5189–5202Google Scholar
  33. Tang D, Shi Y, Kang R, Li T, Xiao W, Wang H, Xiao X (2007) Hydrogen peroxide stimulates macrophages and monocytes to actively release HMGB1. J Leukoc Biol 81:741–747Google Scholar
  34. Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552:335–344Google Scholar
  35. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160:1–40Google Scholar
  36. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84Google Scholar
  37. Viciano E, Monroig Ó, Barata C, Peña C, Navarro JC (2017) Antioxidant activity and lipid peroxidation in Artemia nauplii enriched with DHA-rich oil emulsion and the effect of adding an external antioxidant based on hydroxytyrosol. Aquac Res 48:1006–1019 Google Scholar
  38. Wang CC, Ding S, Chiu KH, Liu WS, Lin TJ, Wen ZH (2016) Extract from a mutant Rhodobacter sphaeroides as an enriched carotenoid source. Food Nutr Res 60:29580Google Scholar
  39. Wei W, Tong L, Li X, Wang R, Wei Z, Zhao G, Zhao S, Zhou Z (2017) Lysine acetylation regulates the function of the global anaerobic transcription factor FnrL in Rhodobacter sphaeroides. Mol Microbiol 104:278–293Google Scholar
  40. Wu T, Lv H, Wang F, Wang Y (2016) Characterization of polyphenols from Lycium ruthenicum fruit by UPLC-Q-TOF/MS(E) and their antioxidant activity in Caco-2 cells. J Agric Food Chem 64:2280–2288Google Scholar
  41. Xia Y, Bamdad F, Gänzle M, Chen L (2012) Fractionation and characterization of antioxidant peptides derived from barley glutelin by enzymatic hydrolysis. Food Chem 134:1509–1518Google Scholar
  42. Yang W, Wu Y, Wang Y, Fu A, Li G, Li W, Li Y (2017) Bacillus amyloliquefaciens SC06 alleviates the oxidative stress of IPEC-1 via modulating Nrf2/Keap1 signaling pathway and decreasing ROS production. Appl Microbiol Biotechnol 101:3015–3026Google Scholar
  43. Yen HW, Shih TY (2009) Coenzyme Q10 production by Rhodobacter sphaeroides in stirred tank and in airlift bioreactor. Bioprocess Biosyst Eng 32:711–716Google Scholar
  44. Yu R, Yin Y, Yang W, Ma W, Yang L, Chen X, Zhang Z, Ye B, Song L (2009) Structural elucidation and biological activity of a novel polysaccharide by alkaline extraction from cultured Cordyceps militaris. Carbohydr Polym 75:166–171Google Scholar
  45. Zhang H, Mu ZB, Xu LM, Xu GF, Liu M, Shan AS (2009) Dietary lipid level induced antioxidant response in Manchurian trout, Brachymystax lenok (Pallas) larvae. Lipids 44:643–654Google Scholar
  46. Zhuang H, Tang N, Yuan Y (2013) Purification and identification of antioxidant peptides from corn gluten meal. J Funct Foods 5:1810–1821Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Jun An
    • 1
    • 2
  • Cui Yang
    • 1
  • Zuming Li
    • 1
    Email author
  • Patricia W. Finn
    • 3
  • David L. Perkins
    • 3
  • Jun Sun
    • 3
  • Zhihui Bai
    • 4
  • Liping Gao
    • 1
  • Michael Zhang
    • 5
  • Difeng Ren
    • 2
  1. 1.Department of Food Science and Beijing Key Laboratory of Bioactive Substances and Functional Foods, College of Biochemical EngineeringBeijing Union UniversityBeijingChina
  2. 2.Beijing Key Laboratory of Forest Food Processing and Safety, College of Biological Sciences and BiotechnologyBeijing Forestry UniversityBeijingChina
  3. 3.Department of MedicineUniversity of Illinois at ChicagoChicagoUSA
  4. 4.Research Center for Eco-Environmental SciencesChinese Academy of SciencesBeijingChina
  5. 5.Department of Physics and AstronomyUniversity of ManitobaWinnipegCanada

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