Skip to main content
SpringerLink
Log in

Antioxidant Properties of Lactic Acid Bacteria

  • REVIEWS
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Lactic acid bacteria (LAB) are widely used in fermentation processes for the preparation of various foodstuffs, including dairy, meat and vegetable products. In the course of industrial biotechnological processes, lactobacilli are often exposed to oxidative stress, which occurs due to accumulation of reactive oxygen species (ROS) inside the cells. ROS are formed as a result of incomplete reduction of molecular oxygen to superoxide radical \(({\text{O}}_{2}^{{ \bullet - }}),\) hydrogen peroxide (H2O2), or hydroxyl radical (OH•) and cause serious damage to all cellular macromolecules. Since LAB do not possess a complete electron transport chain, it was previously believed that they are incapable of existence under oxic conditions. Nevertheless, a number of LAB strains were found to possess the principal antioxidant defense enzymes with high specific activity. These include two types of catalases and NADH peroxidase. Heme-containing catalase is synthesized in many species of lactobacilli if heme or hematin is present in the culture medium. Both monofunctional catalase and bifunctional catalase-peroxidase were found in the cells of many LAB. Catalases of the second type (Mn-containing), which do not require the presence of heme, are also present in the cells of some lactobacilli species. Many LAB strains are characterized by high intracellular levels of Mn(II). Probiotic LAB cultures with pronounced antioxidant activity are in high demand, since they are potentially able to protect the host organism from the toxic effects of ROS and contribute to the prevention of cardiovascular, inflammatory, and oncologic diseases. In this review, antioxidant defense systems in LAB cells are described based on a thorough analysis of the current scientific data. In particular, the review describes the effect of oxidative stress on the metabolism of lactobacilli, their main antioxidant enzymes (NADH oxidase, NADH peroxidase, catalase, superoxide dismutase, and thioredoxin reductase), as well as the key regulatory proteins and the genes responsible for oxygen uptake as one of the mechanisms for decreasing the ROS concentration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Allocati, N., Federici, L., Masulli, M., and Di Ilio, C., Distribution of glutathione transferases in Gram-positive bacteria and Archaea, Biochimie, 2012, vol. 94, no. 3, pp. 588–596.

    Article  CAS  PubMed  Google Scholar 

  2. Al-Madboly, L.A., Ali, S.M., Fakharany, E.M.E., Ragab, A.E., Khedr, E.G., and Elokely, K.M., Stress-based production, and characterization of glutathione peroxidase and glutathione s-transferase enzymes from Lactobacillus plantarum, Front. Bioeng. Biotechnol., 2020, vol. 8, art. 78.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Amanatidou, A., Bennik, M.H.J., Gorris, L.G.M., and Smid, E.J., Superoxide dismutase plays an important role in the survival of Lactobacillus sake upon exposure to elevated oxygen, Arch. Microbiol., 2001, vol. 176, nos. 1–2, pp. 79–88.

    Article  CAS  PubMed  Google Scholar 

  4. Amaretti, A., di Nunzio, M., Pompei, A., Raimondi, S., Rossi, M., and Bordoni, A., Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities, Appl. Microbiol. Biotechnol., 2013, vol. 97, no. 2, pp. 809–817.

    Article  CAS  PubMed  Google Scholar 

  5. An, H., Zhou, H., Huang, Y., Wang, G., Luan, C., Mou, J., Luo, Y., and Hao, Y., High-level expression of heme-dependent catalase gene katA from Lactobacillus sakei protects Lactobacillus rhamnosus from oxidative stress, Mol. Biotechnol., 2010, vol. 45, no. 2, pp. 155–160.

    Article  CAS  PubMed  Google Scholar 

  6. Arcanjo, N.O., Andrade, M.J., Padilla, P., Rodríguez, A., Madruga, M.S., and Estévez, M., Resveratrol protects Lactobacillus reuteri against H2O2-induced oxidative stress and stimulates antioxidant defenses through upregulation of the dhaT gene, Free Radic. Biol. Med., 2019, vol. 135, pp. 38–45.

    Article  CAS  PubMed  Google Scholar 

  7. Archibald, F.S. and Fridovich, I., Manganese and defenses against oxygen toxicity in Lactobacillus plantarum, J. Bacteriol., 1981a, vol. 145, no. 1, pp. 442–451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Archibald, F.S. and Fridovich, I., Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria, J. Bacteriol., 1981b, vol. 146, no. 3, pp. 928–936.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Arioli, S., Zambelli, D., Guglielmetti, S., De Noni, I., Pedersen, M.B., Pedersen, P.D., Dal Bello, F., and Mora, D., Increasing the heme-dependent respiratory efficiency of Lactococcus lactis by inhibition of lactate dehydrogenase, Appl. Environ. Microbiol., 2013, vol. 79, no. 1, pp. 376–380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Averina, O.V., Poluektova, E.U., Marsova, M.V., and Danilenko, V.N., Biomarkers and utility of the antioxidant potential of probiotic lactobacilli and bifidobacteria as representatives of the human gut microbiota, Biomedicines, 2021, vol. 9, no. 10, art. 1340.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Basu Thakur, P., Long, A.R., Nelson, B.J., Kumar, R., Rosenberg, A.F., and Gray, M.J., Complex responses to hydrogen peroxide and hypochlorous acid by the probiotic bacterium Lactobacillus reuteri, mSystems, 2019, vol. 4, no. 5, e00453–19.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Brioukhanov, A.L. and Netrusov, A.I., Aerotolerance of strictly anaerobic microorganisms and factors of defense against oxidative stress (a review), Appl. Biochem. Microbiol., 2007, vol. 43, no. 6, pp. 567–582.

    Article  CAS  Google Scholar 

  13. Brooijmans, R.J.W., de Vos, W.M., and Hugenholtz, J., Lactobacillus plantarum WCFS1 electron transport chains, Appl. Environ. Microbiol., 2009a, vol. 75, no. 11, pp. 3580–3585.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Brooijmans, R., Smit, B., Santos, F., van Riel, J., de Vos, W.M., and Hugenholtz, J., Heme and menaquinone induced electron transport in lactic acid bacteria, Microb. Cell Fact., 2009b, vol. 8, art. 28.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Bruno-Bárcena, J.M., Andrus, J.M., Libby, S.L., Klaenhammer, T.R., and Hassan, H.M., Expression of a heterologous manganese superoxide dismutase gene in intestinal lactobacilli provides protection against hydrogen peroxide toxicity, Appl. Environ. Microbiol., 2004, vol. 70, no. 8, pp. 4702–4710.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Calderini, E., Celebioglu, H.U., Villarroel, J., Jacobsen, S., Svensson, B., and Pessione, E., Comparative proteomics of oxidative stress response of Lactobacillus acidophilus NCFM reveals effects on DNA repair and cysteine de novo synthesis, Proteomics, 2017, vol. 17, no. 5, art. 201600178.

    Article  Google Scholar 

  17. Cappa, F., Cattivelli, D., and Cocconcelli, P.S., The uvrA gene is involved in oxidative and acid stress responses in Lactobacillus helveticus CNBL1156, Res. Microbiol., 2005, vol. 156, no. 10, pp. 1039–1047.

    Article  CAS  PubMed  Google Scholar 

  18. Choi, S.S., Kim, Y., Han, K.S., You, S., Oh, S., and Kim, S.H., Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro, Lett. Appl. Microbiol., 2006, vol. 42, no. 5, pp. 452–458.

    Article  CAS  PubMed  Google Scholar 

  19. Chooruk, A., Piwat, S., and Teanpaisan, R., Antioxidant activity of various oral Lactobacillus strains, J. Appl. Microbiol., 2017, vol. 123, no. 1, pp. 271–279.

    Article  CAS  PubMed  Google Scholar 

  20. Condon, S., Responses of lactic acid bacteria to oxygen, FEMS Microbiol. Rev., 1987, vol. 46, no. 3, pp. 269–280.

    Article  CAS  Google Scholar 

  21. Czapski, G., Reaction of OH·, Method. Enzymol., 1984, vol. 105, pp. 209–215.

    Article  CAS  Google Scholar 

  22. Danilenko, V.N. Stavrovskaya, A.V., Voronkov, D.N., Gushchina, A.S., Marsova, M.V., Yamshchikova, N.G., Ol’shanskii, A.S., Ivanov, M.V., and Illarioshkin, S.N., Application of a pharmabiotic based on Lactobacillus fermentum strain U-21 to modulate the neurodegenerative process in experimental Parkinson’s disease, Ann. Clin. Exp. Neurol., 2020, vol. 14, no. 1, pp. 62–69.

    Google Scholar 

  23. De Angelis, M. and Gobbetti, M., Environmental stress responses in Lactobacillus: a review, Proteomics, 2004, vol. 4, no. 1, pp. 106–122.

    Article  CAS  PubMed  Google Scholar 

  24. Derr, A.M., Faustoferri, R.C., Betzenhauser, M.J., Gonzalez, K., Marquis, R.E., and Quivey, R.G., Jr., Mutation of the NADH oxidase gene (nox) reveals an overlap of the oxygen- and acid-mediated stress responses in Streptococcus mutans, Appl. Environ. Microbiol., 2012, vol. 78, no. 4, pp. 1215–1227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Duwat, P., Ehrlich, S.D., and Gruss, A., Effects of metabolic flux on stress response pathways in Lactococcus lactis, Mol. Microbiol., 1999, vol. 31, no. 3, pp. 845–858.

    Article  CAS  PubMed  Google Scholar 

  26. Duwat, P., Ehrlich, S.D., and Gruss, A., The recA gene of Lactococcus lactis: characterization and involvement in oxidative and thermal stress, Mol. Microbiol., 1995, vol. 17, no. 6, pp. 1121–1131.

    Article  CAS  PubMed  Google Scholar 

  27. Duwat, P., Sourice, S., Cesselin, B., Lamberet, G., Vido, K., Gaudu, P., Le Loir, Y., Violet, F., Loubière, P., and Gruss, A., Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival, J. Bacteriol., 2001, vol. 183, no. 15, pp. 4509–4516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Fardet, A. and Rock, E., In vitro and in vivo antioxidant potential of milks, yoghurts, fermented milks and cheeses: a narrative review of evidence, Nutr. Res. Rev., 2018, vol. 31, no. 1, pp. 52–70.

    Article  CAS  PubMed  Google Scholar 

  29. Feng, T. and Wang, J., Oxidative stress tolerance and antioxidant capacity of lactic acid bacteria as probiotic: a systematic review, Gut Microbes, 2020, vol. 12, no. 1, art. 1801944.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Flint, D.H., Tuminello, J.F., and Emptage, M.H., The inactivation of Fe-S clusters containing hydro-lyases by superoxide, J. Biol. Chem., 1993, vol. 268, no. 30, pp. 22369–22376.

    Article  CAS  PubMed  Google Scholar 

  31. Frankenberg, L., Brugna, M., and Hederstedt, L., Enterococcus faecalis heme-dependent catalase, J. Bacteriol., 2002, vol. 184, no. 22, pp. 6351–6356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Fridovich, I., Oxygen toxicity: a radical explanation, J. Exp. Biol., 1998, vol. 201, pp. 1203–1209.

    Article  CAS  PubMed  Google Scholar 

  33. Gao, D., Gao, Z., and Zhu, G., Antioxidant effects of Lactobacillus plantarum via activation of transcription factor Nrf2, Food Funct., 2013, vol. 4, no. 6, pp. 982–989.

    Article  CAS  PubMed  Google Scholar 

  34. Garrigues, C., Loubiere, P., Lindley, N.D., and Cocaign-Bousquet, M., Control of the shift from homolactic acid to mixed-acid fermentation in Lactococcus lactis: predominant role of the NADH/NAD+ ratio, J. Bacteriol., 1997, vol. 179, no. 17, pp. 5282–5287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Gaudu, P., Lamberet, G., Poncet, S., and Gruss, A., CcpA regulation of aerobic and respiration growth in Lactococcus lactis, Mol. Microbiol., 2003, vol. 50, no. 1, pp. 183–192.

    Article  CAS  PubMed  Google Scholar 

  36. Glorieux, C. and Calderon, P.B., Catalase, a remarkable enzyme: targeting the oldest antioxidant enzyme to find a new cancer treatment approach, Biol. Chem., 2017, vol. 398, no. 10, pp. 1095–1108.

    Article  CAS  PubMed  Google Scholar 

  37. Goosen, N. and Moolenar, G.F., Role of ATP hydrolysis by UvrA and UvrB during nucleotide excision repair, Res. Microbiol., 2001, vol. 152, nos. 3–4, pp. 401–409.

    Article  CAS  PubMed  Google Scholar 

  38. Grajek, W., Olejnik, A., and Sip, A., Probiotics, prebiotics and antioxidants as functional foods, Acta Biochim. Pol., 2005, vol. 52, no. 3, pp. 665–671.

    Article  CAS  PubMed  Google Scholar 

  39. Guerzoni, M.E., Lanciotti, R., and Cocconcelli, P.S., Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus, Microbiology (Reading), 2001, vol. 147, no. 8, pp. 2255–2264.

    Article  CAS  PubMed  Google Scholar 

  40. Guidone, A., Ianniello, R.G., Ricciardi, A., Zotta, T., and Parente, E., Aerobic metabolism and oxidative stress tolerance in the Lactobacillus plantarum group, World J. Microbiol. Biotechnol., 2013, vol. 29, no. 9, pp. 1713–1722.

    Article  CAS  PubMed  Google Scholar 

  41. Guo, Y., Pan, D., Li, H., Sun, Y., Zeng, X., and Yan, B., Antioxidant and immunomodulatory activity of selenium exopolysaccharide produced by Lactococcus lactis subsp. lactis, Food Chem., 2013, vol. 138, no. 1, pp. 84–89.

    Article  CAS  PubMed  Google Scholar 

  42. Halliwell, B., and Gutteridge, J.M., Role of free radicals and catalytic metal ions in human disease: an overview, Meth. Enzymol., 1990, vol. 186, pp. 1–85.

    Article  CAS  Google Scholar 

  43. Hamon, E., Horvatovich, P., Izquierdo, E., Bringel, F., Marchioni, E., Aoudé-Werner, D., and Ennahar, S., Comparative proteomic analysis of Lactobacillus plantarum for the identification of key proteins in bile tolerance, BMC Microbiol., 2011, vol. 11, art. 63.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ianniello, R.G., Zotta, T., Matera, A., Genovese, F., Parente, E., and Ricciardi, A., Investigation of factors affecting aerobic and respiratory growth in the oxygen-tolerant strain Lactobacillus casei N87, PLoS One, 2016, vol. 11, no. 11, e0164065.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Jänsch, A., Freiding, S., Behr, J., and Vogel, R.F., Contribution of the NADH-oxidase (Nox) to the aerobic life of Lactobacillus sanfranciscensis DSM20451T, Food Microbiol., 2011, vol. 28, no. 1, pp. 29–37.

    Article  PubMed  Google Scholar 

  46. Jänsch, A., Korakli, M., Vogel, R.F., and Ganzle, M.G., Glutathione reductase from Lactobacillus sanfranciscensis DSM20451T: contribution to oxygen tolerance and thiol exchange reactions in wheat sourdoughs, Appl. Environ. Microbiol., 2007, vol. 73, no. 14, pp. 4469–4476.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Jastrząb, A. and Skrzydlewska, E., Thioredoxin-dependent system. Application of inhibitors, J. Enzyme Inhib. Med. Chem., 2021, vol. 36, no. 1, pp. 362–371.

    Article  PubMed  Google Scholar 

  48. Kakhlon, O. and Cabantchik, Z.I., The labile iron pool: characterization, measurement, and participation in cellular processes, Free Radic. Biol. Med., 2002, vol. 33, no. 8, pp. 1037–1046.

    Article  CAS  PubMed  Google Scholar 

  49. Kandler, O., Carbohydrate metabolism in lactic acid bacteria, Antonie Van Leeuwenhoek, 1983, vol. 49, no. 3, pp. 209–224.

    Article  CAS  PubMed  Google Scholar 

  50. Kang, T.S., Korber, D.R., and Tanaka, T., Influence of oxygen on NADH recycling and oxidative stress resistance systems in Lactobacillus panis PM1, AMB Express, 2013, vol. 3, no. 1, art. 10.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Kehrer, J.P., Free-radicals as mediators of tissue-injury and disease, Crit. Rev. Toxicol., 1993, vol. 23, no. 1, pp. 21–48.

    Article  CAS  PubMed  Google Scholar 

  52. Keyer, K. and Imlay, J.A., Superoxide accelerates DNA damage by elevating free iron, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, no. 24, pp. 13635–13640.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Kim, J.E., Eom, H.J., Kim, Y., Ahn, J.E., Kim, J.H., and Han, N.S., Enhancing acid tolerance of Leuconostoc mesenteroides with glutathione, Biotechnol. Lett., 2012, vol. 34, no. 4, pp. 683–687.

    Article  CAS  PubMed  Google Scholar 

  54. Kim, K.T., Kim, J.W., Kim, S.I., Kim, S., Nguyen, T.H., and Kang, C.H., Antioxidant and anti-inflammatory effect and probiotic properties of lactic acid bacteria isolated from canine and feline feces, Microorganisms, 2021, vol. 9, no. 9, art. 1971.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Klimko, A.I., Cherdyntseva, T.A., Brioukhanov, A.L., and Netrusov, A.I., In vitro evaluation of probiotic potential of selected lactic acid bacteria strains, Probiotics Antimicrob. Proteins, 2020, vol. 12, no. 3, pp. 1139–1148.

    Article  CAS  PubMed  Google Scholar 

  56. Kobatake, E., Nakagawa, H., Seki, T., and Miyazaki, T., Protective effects and functional mechanisms of Lactobacillus gasseri SBT2055 against oxidative stress, PLoS One, 2017, vol. 12, no. 5, e0177106.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Kono, Y. and Fridovich, I., Isolation and characterization of the pseudocatalase of Lactobacillus plantarum, J. Biol. Chem., 1983, vol. 258, no. 10, pp. 6015–6019.

    Article  CAS  PubMed  Google Scholar 

  58. Kono, Y., Takahashi, M.-A., and Asada, K., Oxidation of manganous pyrophosphate by superoxide radicals and illuminated spinach chloroplasts, Arch. Biochem. Biophys., 1976, vol. 174, no. 2, pp. 454–462.

    Article  CAS  PubMed  Google Scholar 

  59. Kullisaar, T., Songisepp, E., Aunapuu, M., Kilk, K., Arend, A., Mikelsaar, M., Rehema, A., and Zilmer, M., Complete glutathione system in probiotic Lactobacillus fermentum ME-3, Appl. Biochem. Microbiol., 2010, vol. 46, no. 5, pp. 481–486.

    Article  CAS  Google Scholar 

  60. Kumar, S. and Bandyopadhyay, U., Free heme toxicity and its detoxification systems in human, Toxicol. Lett., 2005, vol. 157, no. 3, pp. 175–188.

    Article  CAS  PubMed  Google Scholar 

  61. LeBlanc, J.G., del Carmen, S., Miyoshi, A., Azevedo, V., Sesma, F., Langella, P., Bermúdez-Humarán, L.G., Watterlot, L., Perdigon, G., and de Moreno de LeBlanc, A., Use of superoxide dismutase and catalase producing lactic acid bacteria in TNBS induced Crohn’s disease in mice, J. Biotechnol., 2011, vol. 151, no. 3, pp. 287–293.

    Article  CAS  PubMed  Google Scholar 

  62. Lechardeur, D., Fernandez, A., Robert, B., Gaudu, P., and Trieu-Cuot, P., The 2-cys peroxiredoxin alkyl hydroperoxide reductase c binds heme and participates in its intracellular availability in Streptococcus agalactiae, J. Biol. Chem., 2010, vol. 285, no. 21, pp. 16032–16041.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Lee, K., Kim, H.J., Rho, B.S., Kang, S.K., and Choi, Y.J., Effect of glutathione on growth of the probiotic bacterium Lactobacillus reuteri, Biochemistry (Moscow), 2011, vol. 76, no. 4, pp. 423–426.

    CAS  PubMed  Google Scholar 

  64. Lee, K., Pi, K., Kim, E.B., Rho, B.S., Kang, S.K., Lee, H.G., and Choi, Y.J., Glutathione-mediated response to acid stress in the probiotic bacterium, Lactobacillus salivarius, Biotechnol. Lett., 2010, vol. 32, no. 7, pp. 969–972.

    Article  CAS  PubMed  Google Scholar 

  65. Li, S., Huang, R., Shah, N.P., Tao, X., Xiong, Y., and Wei, H., Antioxidant and antibacterial activities of exopolysaccharides from Bifidobacterium bifidum WBIN03 and Lactobacillus plantarum R315, J. Dairy Sci., 2014, vol. 97, no. 12, pp. 7334–7343.

    Article  CAS  PubMed  Google Scholar 

  66. Li, S., Zhao, Y., Zhang, L., Zhang, X., Huang, L., Li, D., Niu, C., Yang, Z., and Wang, Q., Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods, Food Chem., 2012, vol. 135, no. 3, pp. 1914–1919.

    Article  CAS  PubMed  Google Scholar 

  67. Lin, J., Zou, Y., Cao, K., Ma, C., and Chen, Z., The impact of heterologous catalase expression and superoxide dismutase overexpression on enhancing the oxidative resistance in Lactobacillus casei, J. Ind. Microbiol. Biotechnol., 2016, vol. 43, no. 5, pp. 703–711.

    Article  CAS  PubMed  Google Scholar 

  68. Lo, R., Turner, M.S., Barry, D.G., Sreekumar, R., Walsh, T.P., and Giffard, P.M., Cystathionine γ-lyase is a component of cystine-mediated oxidative defense in Lactobacillus reuteri BR11, J. Bacteriol., 2009, vol. 191, no. 6, pp. 1827–1837.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Lu, J. and Holmgren, A., The thioredoxin antioxidant system, Free Radic. Biol. Med., 2014, vol. 66, pp. 75–87.

    Article  CAS  PubMed  Google Scholar 

  70. Maresca, D., Zotta, T., and Mauriello, G., Adaptation to aerobic environment of Lactobacillus johnsonii/gasseri strains, Front. Microbiol., 2018, vol. 9, art. 157.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Marques Da Silva, W., Oliveira, L.C., Soares, S.C., Sousa, C.S., Tavares, G.C., Resende, C.P., Pereira, F.L., Ghosh, P., Figueiredo, H., and Azevedo, V., Quantitative proteomic analysis of the response of probiotic putative Lactococcus lactis NCDO 2118 strain to different oxygen availability under temperature variation, Front. Microbiol., 2019, vol. 10, art. 759.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Marsova, M., Poluektova, E., Odorskaya, M., Ambaryan, A., Revishchin, A., Pavlova, G., and Danilenko, V., Protective effects of Lactobacillus fermentum U-21 against paraquat-induced oxidative stress in Caenorhabditis elegans and mouse models, World J. Microbiol. Biotechnol., 2020, vol. 36, no. 7, art. 104.

    Article  CAS  PubMed  Google Scholar 

  73. McCord, J.M. and Fridovich, I., Superoxide dismutase: an enzymatic function for erythrocuprein (hemocuprein), J. Biol. Chem., 1969, vol. 244, pp. 6049–6055.

    Article  CAS  PubMed  Google Scholar 

  74. Miller, R.V. and Kokjohn, T.A., General microbiology of recA: environmental and evolutionary significance, Annu. Rev. Microbiol., 1990, vol. 44, no. 1, pp. 365–394.

    Article  CAS  PubMed  Google Scholar 

  75. Miyoshi, A., Rochat, T., Gratadoux, J.J., Le Loir, Y., Oliveira, S.C., Langella, P., and Azevedo, V., Oxidative stress in Lactococcus lactis, Genet. Mol. Res., 2003, vol. 2, no. 4, pp. 348–359.

    CAS  PubMed  Google Scholar 

  76. Molenaar, D., Bringel, F., Schuren, F.H., de Vos, W.M., Siezen, R.J., and Kleerebezem, M., Exploring Lactobacillus plantarum genome diversity by using microarrays, J. Bacteriol., 2005, vol. 187, no. 17, pp. 6119–6127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Murphy, M.G. and Condon, S., Comparison of aerobic and anaerobic growth of Lactobacillus plantarum in a glucose medium, Arch. Microbiol., 1984, vol. 138, no. 1, pp. 49–53.

    Article  CAS  Google Scholar 

  78. Naraki, S., Igimi, S., and Sasaki, Y., NADH peroxidase plays a crucial role in consuming H2O2 in Lactobacillus casei IGM394, Biosci. Microbiota Food Health, 2020, vol. 39, no. 2, pp. 45–56.

    Article  CAS  PubMed  Google Scholar 

  79. Nie, Y., Hu, J., Hou, Q., Zheng, W., Zhang, X., Yang, T., Ma, L., and Yan, X., Lactobacillus frumenti improves antioxidant capacity via nitric oxide synthase 1 in intestinal epithelial cells, FASEB J., 2019, vol. 33, no. 10, pp. 10705–10716.

    Article  CAS  PubMed  Google Scholar 

  80. Noonpakdee, W., Sitthimonchai, S., Panyim, S., and Lertsiri, S., Expression of the catalase gene katA in starter culture Lactobacillus plantarum TISTR850 tolerates oxidative stress and reduces lipid oxidation in fermented meat product, Int. J. Food Microbiol., 2004, vol. 95, no. 2, pp. 127–135.

    Article  CAS  PubMed  Google Scholar 

  81. Noureen, S., Riaz, A., Arshad, M., and Arshad, N., In vitro selection and in vivo confirmation of the antioxidant ability of Lactobacillus brevis MG000874, J. Appl. Microbiol., 2019, vol. 126, no. 4, pp. 1221–1232.

    Article  CAS  PubMed  Google Scholar 

  82. Pedersen, M.B., Gaudu, P., Lechardeur, D., Petit, M.A., and Gruss, A., Aerobic respiration metabolism in lactic acid bacteria and uses in biotechnology, Annu. Rev. Food Sci. Technol., 2012, vol. 3, pp. 37–58.

    Article  CAS  PubMed  Google Scholar 

  83. Petrat, F., Paluch, S., Dogruöz, E., Dörfler, P., Kirsch, M., Korth, H.G., Sustmann, R., and de Groot, H., Reduction of Fe(III) ions complexed to physiological ligands by lipoyl dehydrogenase and other flavoenzymes in vitro: implications for an enzymatic reduction of Fe(III) ions of the labile iron pool, J. Biol. Chem., 2003, vol. 278, no. 47, pp. 46403–46413.

    Article  CAS  PubMed  Google Scholar 

  84. Pittman, M.S., Robinson, H.C., and Poole, R.K., A bacterial glutathione transporter (Escherichia coli CydDC) exports reductant to the periplasm, J. Biol. Chem., 2005, vol. 280, no. 37, pp. 32254–32261.

    Article  CAS  PubMed  Google Scholar 

  85. Poluektova, E., Yunes, R., and Danilenko, V., The putative antidepressant mechanisms of probiotic bacteria: relevant genes and proteins, Nutrients, 2021, vol. 13, no. 5, art. 1591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Pophaly, S.D., Poonam, S., Pophaly, S.D., Kapila, S., Nanda, D.K., Tomar, S.K., and Singh, R., Glutathione biosynthesis and activity of dependent enzymes in food-grade lactic acid bacteria harbouring multidomain bifunctional fusion gene (gshF), J. Appl. Microbiol., 2017, vol. 123, no. 1, pp. 194–203.

    Article  CAS  PubMed  Google Scholar 

  87. Pridmore, R.D., Pittet, A.C., Praplan, F., and Cavadini, C., Hydrogen peroxide production by Lactobacillus johnsonii NCC 533 and its role in anti-Salmonella activity, FEMS Microbiol. Lett., 2008, vol. 283, no. 2, pp. 210–215.

    Article  CAS  PubMed  Google Scholar 

  88. Rezaïki, L., Lamberet, G., Derré, A., Gruss, A., and Gaudu, P., Lactococcus lactis produces short-chain quinones that cross-feed Group B Streptococcus to activate respiration growth, Mol. Microbiol., 2008, vol. 67, no. 5, pp. 947–957.

    Article  PubMed  Google Scholar 

  89. Ricciardi, A., Ianniello, R.G., Parente, E., and Zotta, T., Factors affecting gene expression and activity of heme- and manganese-dependent catalases in Lactobacillus casei strains, Int. J. Food Microbiol., 2018, vol. 280, pp. 66–77.

    Article  CAS  PubMed  Google Scholar 

  90. Ricciardi, A., Zotta, T., Ianniello, R.G., Boscaino, F., Matera, A., and Parente, E., Effect of respiratory growth on the metabolite production and stress robustness of Lactobacillus casei N87 cultivated in cheese whey permeate medium, Front. Microbiol., 2019, vol. 10, art. 851.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Rochat, T., Gratadoux, J.-J., Gruss, A., Corthier, G., Maguin, E., Langella, P., and van de Guchte, M., Production of a heterologous nonheme catalase by Lactobacillus casei: an efficient tool for removal of H2O2 and protection of Lactobacillus bulgaricus from oxidative stress in milk, Appl. Environ. Microbiol., 2006, vol. 72, no. 8, pp. 5143–5149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Satoh, T., Todoroki, M., Kobayashi, K., Niimura, Y., and Kawasaki, S., Purified thioredoxin reductase from O2-sensitive Bifidobacterium bifidum degrades H2O2 by interacting with alkyl hydroperoxide reductase, Anaerobe, 2019, vol. 57, pp. 45–54.

    Article  CAS  PubMed  Google Scholar 

  93. Scharf, C., Riethdorf, S., Ernst, H., Engelmann, S., Volker, U., and Hecker, M., Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis, J. Bacteriol., 1998, vol. 180, no. 7, pp. 1869–1877.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Serata, M., Yasuda, E., and Sako, T., Effect of superoxide dismutase and manganese on superoxide tolerance in Lactobacillus casei strain Shirota and analysis of multiple manganese transporters, Biosci. Microbiota Food Health, 2018, vol. 37, no. 2, pp. 31–38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Serrano, L.M., Molenaar, D., Wels, M., Teusink, B., Bron, P.A., de Vos, W.M., and Smid, E.J., Thioredoxin reductase is a key factor in the oxidative stress response of Lactobacillus plantarum WCFSI, Microb. Cell Fact., 2007, vol. 6, art. 29.

    Article  PubMed  PubMed Central  Google Scholar 

  96. Shi, W., Li, Y., Gao, X., and Fu, R., Improvement of the respiration efficiency of Lactococcus lactis by decreasing the culture pH, Biotechnol. Lett., 2016, vol. 38, no. 3, pp. 495–501.

    Article  CAS  PubMed  Google Scholar 

  97. Siciliano, R.A., Pannella, G., Lippolis, R., Ricciardi, A., Mazzeo, M.F., and Zotta, T., Impact of aerobic and respirative life-style on Lactobacillus casei N87 proteome, Int. J. Food Microbiol., 2019, vol. 298, pp. 51–62.

    Article  CAS  PubMed  Google Scholar 

  98. Stevens, M.J.A., Molenaar, D., de Jong, A., de Vos, W.M., and Kleerebezem, M., Involvement of the mannose phosphotransferase system of Lactobacillus plantarum WCFS1 in peroxide stress tolerance, Appl. Environ. Microbiol., 2010, vol. 76, no. 11, pp. 3748–3752.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Storz, G. and Imlay, J.A., Oxidative stress, Curr. Opin. Microbiol., 1999, vol. 2, no. 2, pp. 188–194.

    Article  CAS  PubMed  Google Scholar 

  100. Tachon, S., Brandsma, J.B., and Yvon, M., NoxE NADH oxidase and the electron transport chain are responsible for the ability of Lactococcus lactis to decrease the redox potential of milk, Appl. Environ. Microbiol., 2010, vol. 76, no. 5, pp. 1311–1319.

    Article  CAS  PubMed  Google Scholar 

  101. Tachon, S., Chambellon, E., and Yvon, M., Identification of a conserved sequence in flavoproteins essential for the correct conformation and activity of the NADH oxidase NoxE of Lactococcus lactis, J. Bacteriol., 2011, vol. 193, no. 12, pp. 3000–3008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Tachon, S., Michelon, D., Chambellon, E., Cantonnet, M., Mezange, C., Henno, L., Cachon, R., and Yvon, M., Experimental conditions affect the site of tetrazolium violet reduction in the electron transport chain of Lactococcus lactis, Microbiology, 2009, vol. 155, no. 9, pp. 2941–2948.

    Article  CAS  PubMed  Google Scholar 

  103. Talwalkar, A. and Kailasapathy, K., Metabolic and biochemical responses of probiotic bacteria to oxygen, J. Dairy Sci., 2003, vol. 86, no. 8, pp. 2537–2546.

    Article  CAS  PubMed  Google Scholar 

  104. Tanaka, K., Satoh, T., Kitahara, J., Uno, S., Nomura, I., Kano, Y., Suzuki, T., Niimura, Y., and Kawasaki, S., O2-inducible H2O2-forming NADPH oxidase is responsible for the hyper O2 sensitivity of Bifidobacterium longum subsp. infantis, Sci. Rep., 2018, vol. 8, no. 1, art. 10750.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Tang, W., Xing, Z., Hu, W., Li, C., Wang, J., and Wang, Y., Antioxidative effects in vivo and colonization of Lactobacillus plantarum MA2 in the murine intestinal tract, Appl. Microbiol. Biotechnol., 2016, vol. 100, no. 16, pp. 7193–7202.

    Article  CAS  PubMed  Google Scholar 

  106. Tian, X., Wang, Y., Chu, J., Zhuang, Y., and Zhang, S., Metabolite profiling coupled with metabolic flux analysis reveals physiological and metabolic impacts on Lactobacillus paracasei oxygen metabolism, Process Biochem., 2018, vol. 68, pp. 1–11.

    Article  CAS  Google Scholar 

  107. van Niel, E.W.J., Hofvendahl, K., and Hahn-Hägerdal, B., Formation and conversion of oxygen metabolites by Lactococcus lactis subsp. lactis ATCC 19435 under different growth conditions, Appl. Environ. Microbiol., 2002, vol. 68, no. 9, pp. 4350–4356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Vasquez, E.C., Pereira, T.M.C., Peotta, V.A., Baldo, M.P., and Campos-Toimil, M., Probiotics as beneficial dietary supplements to prevent and treat cardiovascular diseases: uncovering their impact on oxidative stress, Oxid. Med. Cell. Longev., 2019, art. 3086270.

  109. Vido, K., Le Bars, D., Mistou, M.Y., Anglade, P., Gruss, A., and Gaudu, P., Proteome analyses of heme-dependent respiration in Lactococcus lactis: involvement of the proteolytic system, J. Bacteriol., 2004, vol. 186, no. 6, pp. 1648–1657.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Walker, G.C., The SOS response of Escherichia coli. In: Escherichia coli and Salmonella typhimurium, Cell. Mol. Bi-ol., 1996, pp. 1400–1416.

    Google Scholar 

  111. Watanabe, M., van der Veen, S., Nakajima, H., and Abee, T., Effect of respiration and manganese on oxidative stress resistance of Lactobacillus plantarum WCFS1, Microbiology, 2012, vol. 158, no. 1, pp. 293–300.

    Article  CAS  PubMed  Google Scholar 

  112. Wolf, G., Strahl, A., Meisel, J., and Hammes, W.P., Heme-dependent catalase activity of lactobacilli, Int. J. Food Microbiol., 1991, vol. 12, nos. 2–3, pp. 133–140.

    Article  CAS  PubMed  Google Scholar 

  113. Xiong, Z.Q., Kong, L.H., Wang, G.Q., Xia, Y.J., Zhang, H., Yin, B.X., and Ai, L.Z., Functional analysis and heterologous expression of bifunctional glutathione synthetase from Lactobacillus, J. Dairy Sci., 2018, vol. 101, no. 8, pp. 6937–6945.

    Article  CAS  PubMed  Google Scholar 

  114. Yamamoto, N., Shoji, M., Hoshigami, H., Watanabe, K., Watanabe, K., Takatsuzu, T., Yasuda, S., Igoshi, K., and Kinoshita, H., Antioxidant capacity of soymilk yogurt and exopolysaccharides produced by lactic acid bacteria, Biosci. Microbiota Food Health, 2019, vol. 38, no. 3, pp. 97–104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Zhang, Y. and Li, Y., Engineering the antioxidative properties of lactic acid bacteria for improving its robustness, Curr. Opin. Biotech., 2013, vol. 24, no. 2, pp. 142–147.

    Article  PubMed  Google Scholar 

  116. Zheng, J., Wittouck, S., Salvetti, E., Franz, C.M.A.P., Harris, H.M.B., Mattarelli, P., O’Toole, P.W., Pot, B., Vandamme, P., Walter, J., Watanabe, K., Wuyts, S., Felis, G.E., Gänzle, M.G., and Lebeer, S., A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae, Int. J. Syst. Evol. Microbiol., 2020, vol. 70, no. 4, pp. 2782–2858.

    Article  CAS  PubMed  Google Scholar 

  117. Zotta, T., Parente, E., and Ricciardi, A., Aerobic metabolism in the genus Lactobacillus: impact on stress response and potential applications in the food industry, J. Appl. Microbiol., 2017, vol. 122, no. 4, pp. 857–869.

    Article  CAS  PubMed  Google Scholar 

  118. Zuo, F., Yu, R., Feng, X., Khaskheli, G.B., Chen, L., Ma, H., and Chen, S., Combination of heterogeneous catalase and superoxide dismutase protects Bifidobacterium longum strain NCC2705 from oxidative stress, Appl. Microbiol. Biotechnol., 2014, vol. 98, no. 17, pp. 7523–7534.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The work was carried out within the framework of the state task on the topic of the Department of Micro-biology of MSU “Physiology and Biochemistry of Phototrophic and Chemotrophic Microorganisms” (CITIS no. 121032300094-7).

Author information

Authors and Affiliations

  1. Faculty of Biology, Moscow State University, 119991, Moscow, Russia

    A. L. Bryukhanov, A. I. Klimko & A. I. Netrusov

Authors
  1. A. L. Bryukhanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. I. Klimko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. I. Netrusov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. I. Klimko.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by D. Timchenko

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bryukhanov, A.L., Klimko, A.I. & Netrusov, A.I. Antioxidant Properties of Lactic Acid Bacteria. Microbiology 91, 463–478 (2022). https://doi.org/10.1134/S0026261722601439

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261722601439

Keywords:

Search

Navigation