Skip to main content
SpringerLink
Log in

Genomic Analysis for Antioxidant Property of Lactobacillus plantarum FLPL05 from Chinese Longevity People

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Antioxidant activity is one of the important probiotic characteristics for lactic acid bacteria including Lactobacillus plantarum, which is used for food fermentation or as a probiotic supplement. L. plantarum FLPL05 is a novel strain originally isolated from a healthy elderly individual of longevity. The organism has been demonstrated to exhibit high antioxidant property. However, there are limited genomic insights into the antioxidant properties of this organism. In this study, we performed whole-genome analysis regarding its antioxidant property. L. plantarum FLPL05 exhibited higher antioxidant activity compared with that of L. plantarum strains ATCC14917, ATCC8014, and WCFS1. The antioxidant capacity of L. plantarum FLPL05 was genetically linked to its antioxidant system, i.e., glutathione and thioredoxin involved in global regulation of defense against hydrogen peroxide challenge. L. plantarum FLPL05 was further examined for its antioxidant potential in d-Gal-induced aging mice and exhibited a significant increase in the activity of serum glutathione peroxidase (GSH-PX) and a decrease in the level of malondialdehyde (MDA). Moreover, our analyses exhibited a complete gene cluster including plnA, plnB, plnC, plnD, plnE, plnF, plnG, plnH, plnI, plnJ, plnK, plnM, plnN, plnO, plnP, plnQ, plnST, plnU, plnV, plnW, plnX, and plnY for production of bacteriocin. Our results suggest that L. plantarum FLPL05 could be a probiotic candidate.

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
Fig. 4

References

  1. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD (2017) Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14:491–502. https://doi.org/10.1038/nrgastro.2017.75

    Article  Google Scholar 

  2. Parvez S, Malik KA, Kang SA, Kim H-Y (2006) Probiotics and their fermented food products are beneficial for health. J Appl Microbiol 100:1171–1185. https://doi.org/10.1111/J.1365-2672.2006.02963.X

    Article  CAS  Google Scholar 

  3. Neef A, Sanz Y (2013) Future for probiotic science in functional food and dietary supplement development. Curr Opin Clin Nutr Metab Care 16:679–687. https://doi.org/10.1097/MCO.0B013E328365C258

    Article  CAS  Google Scholar 

  4. Filannino P, Cardinali G, Rizzello CG, Buchin S, De Angelis M, Gobbetti M, Di Cagno R (2014) Metabolic responses of Lactobacillus plantarum strains during fermentation and storage of vegetable and fruit juices. Appl Environ Microbiol 80:2206–2215. https://doi.org/10.1128/AEM.03885-13

    Article  CAS  Google Scholar 

  5. Bujňáková D, Kmet V (2012) Functional properties of lactobacillus strains isolated from dairy products. Folia Microbiol 57:263–267. https://doi.org/10.1007/S12223-012-0121-X

    Article  Google Scholar 

  6. Cavalheiro CP, Ruiz-Capillas C, Herrero AM, Jiménez-Colmenero F, de Menezes CR, Fries LLM (2015) Application of probiotic delivery systems in meat products. Trends Food Sci Technol 46:120–131. https://doi.org/10.1016/J.TIFS.2015.09.004

    Article  Google Scholar 

  7. Huang R, Pan M, Wan C, Shah NP, Tao X, Wei H (2015) Physiological and transcriptional responses and cross protection of Lactobacillus plantarum ZDY2013 under acid stress. J Dairy Sci 99:1002–1010. https://doi.org/10.3168/jds.2015-9993

    Article  CAS  Google Scholar 

  8. Xiao Y, Wang L, Rui X, Li W, Chen X, Jiang M, Dong M (2015) Enhancement of the antioxidant capacity of soy whey by fermentation with Lactobacillus plantarum B1-6. J Funct Foods 12:33–44. https://doi.org/10.1016/J.JFF.2014.10.033

    Article  CAS  Google Scholar 

  9. Zhang L, Liu C, Li D, Zhao Y, Zhang X, Zeng X, Yang Z, Li S (2013) Antioxidant activity of an exopolysaccharide isolated from Lactobacillus plantarum C88. Int J Biol Macromol 54:270–275. https://doi.org/10.1016/J.IJBIOMAC.2012.12.037

    Article  Google Scholar 

  10. Tang W, Xing Z, Li C, Wang J, Wang Y (2017) Molecular mechanisms and in vitro antioxidant effects of Lactobacillus plantarum MA2. Food Chem 221:1642–1649. https://doi.org/10.1016/J.FOODCHEM.2016.10.124

    Article  CAS  Google Scholar 

  11. Cheng X, Huang L, Li K-T (2019) Antioxidant activity changes of exopolysaccharides with different carbon sources from Lactobacillus plantarum LPC-1 and its metabolomic analysis. World J Microbiol Biotechnol 35:68. https://doi.org/10.1007/S11274-019-2645-6

    Article  Google Scholar 

  12. Arena MP, Silvain A, Normanno G, Grieco F, Drider D, Spano G, Fiocco D (2016) Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Front Microbiol 7:464. https://doi.org/10.3389/FMICB.2016.00464

    Article  Google Scholar 

  13. Wang Y, Shang N, Qin Y, Zhang Y, Zhang J, Li P (2018) The complete genome sequence of Lactobacillus plantarum LPL-1, a novel antibacterial probiotic producing class IIa bacteriocin. J Biotechnol 266:84–88. https://doi.org/10.1016/J.JBIOTEC.2017.12.006

    Article  CAS  Google Scholar 

  14. Diep DB, Håvarstein LS, Nes IF (1995) A bacteriocin-like peptide induces bacteriocin synthesis in Lactobacillus plantarum C11. Mol Microbiol 18:631–639. https://doi.org/10.1111/J.1365-2958.1995.MMI_18040631.X

    Article  CAS  Google Scholar 

  15. Liu H, Zhang L, Yi H, Han X, Chi C (2016) Identification and characterization of plantaricin Q7, a novel plantaricin produced by Lactobacillus plantarum Q7. LWT-Food Sci Technol 71:386–390. https://doi.org/10.1016/J.LWT.2016.04.009

    Article  CAS  Google Scholar 

  16. Zhao S, Han J, Bie X, Lu Z, Zhang C, Lv F (2016) Purification and characterization of plantaricin JLA-9: a novel bacteriocin against Bacillus spp. produced by Lactobacillus plantarum JLA-9 from Suan-Tsai, a traditional Chinese fermented cabbage. J Agric Food Chem 64:2754–2764. https://doi.org/10.1021/ACS.JAFC.5B05717

    Article  CAS  Google Scholar 

  17. Liu L, Li P (2016) Complete genome sequence of Lactobacillus paraplantarum L-ZS9, a probiotic starter producing class II bacteriocins. J Biotechnol 222:15–16. https://doi.org/10.1016/J.JBIOTEC.2016.02.003

    Article  CAS  Google Scholar 

  18. Kuipers OP, Pascalle GGAD, Ruyter MK, Vos WMD (1998) Quorum sensing-controlled gene expression in lactic acid bacteria. J Biotechnol 64:15–21. https://doi.org/10.1016/S0168-1656(98)00100-X

    Article  CAS  Google Scholar 

  19. Liu H, Yin S, An L, Zhang G, Cheng H, Xi Y, Cui G, Zhang F, Zhang L (2016) Complete genome sequence of Bacillus subtilis BSD-2, a microbial germicide isolated from cultivated cotton. J Biotechnol 230:26–27. https://doi.org/10.1016/J.JBIOTEC.2016.05.019

    Article  CAS  Google Scholar 

  20. Mccarthy A (2010) Third generation DNA sequencing: Pacific biosciences’ single molecule real time technology. Chem Biol 17:675–676. https://doi.org/10.1016/J.CHEMBIOL.2010.07.004

    Article  CAS  Google Scholar 

  21. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 5:955–964. https://doi.org/10.1093/NAR/25.5.0955

    Article  Google Scholar 

  22. Karin L, Peter H, Andreas RE, Hans-Henrik S, Torbjørn R, Ussery DW (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108. https://doi.org/10.1093/NAR/GKM160

    Article  Google Scholar 

  23. Gardner PP, Jennifer D, Tate JG, Nawrocki EP, Kolbe DL, Stinus L, Wilkinson AC, Finn RD, Sam GJ, Eddy SR (2008) Rfam: updates to the RNA families database. Nucleic Acids Res 37:136–140. https://doi.org/10.1093/NAR/GKN766

    Article  Google Scholar 

  24. Ashburner M, Ball CA, Blake JA, Botstein D, Cherry JM (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29. https://doi.org/10.1038/75556

    Article  CAS  Google Scholar 

  25. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34:354–357. https://doi.org/10.1093/NAR/GKJ102

    Article  Google Scholar 

  26. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41–41. https://doi.org/10.1186/1471-2105-4-41

    Article  Google Scholar 

  27. Li W, Jaroszewski L, Godzik A (2002) Tolerating some redundancy significantly speeds up clustering of large protein databases. Bioinformatics 18:77–82. https://doi.org/10.1093/BIOINFORMATICS/18.1.77

    Article  CAS  Google Scholar 

  28. Saier MH, Reddy VS, Tamang DG, Ake V (2013) The transporter classification database. Nucleic Acids Res 42:251–258. https://doi.org/10.1093/NAR/GKT1097

    Article  Google Scholar 

  29. Amos B, Rolf A (2000) The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res 28:45–48. https://doi.org/10.1093/NAR/27.1.49

    Article  Google Scholar 

  30. Blin K, Shaw S, Steinke K, Villebro R, Ziemert N, Lee SY, Weber T (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47:81–87. https://doi.org/10.1093/NAR/GKZ310

    Article  Google Scholar 

  31. Van Heel AJ, de Jong A, Montalban-Lopez M, Kok J, Kuipers OP (2013) BAGEL3: automated identification of genes encoding bacteriocins and (non-) bactericidal posttranslationally modified peptides. Nucleic Acids Res 41:448–453. https://doi.org/10.1093/NAR/GKT391

    Article  Google Scholar 

  32. Li S, Zhao Y, Zhang L, Zhang X, Huang L, Li D, Niu C, Yang Z, Wang Q (2012) Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chem 135:1914–1919. https://doi.org/10.1016/J.FOODCHEM.2012.06.048

    Article  CAS  Google Scholar 

  33. Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△Ct method. Methods 25:402–408. https://doi.org/10.1006/METH.2001.1262

    Article  CAS  Google Scholar 

  34. Yu X, Li S, Yang D, Qiu L, Wu Y, Wang D, Shah NP, Xu F, Wei H (2016) A novel strain of Lactobacillus mucosae isolated from a Gaotian villager improves in vitro and in vivo antioxidant as well as biological properties in D-galactose-induced aging mice. J Dairy Sci 99:903–914. https://doi.org/10.3168/JDS.2015-10265

    Article  CAS  Google Scholar 

  35. Arnér ESJ, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102–6109. https://doi.org/10.1046/J.1432-1327.2000.01701.X

    Article  Google Scholar 

  36. Serrano L (2008) Oxidative stress response in Lactobacillus plantarum WCFS1: a functional genomics approach. Dissertation, Wageningen University. https://library.wur.nl/WebQuery/wurpubs/365432. Accessed 13 Aug 2019

  37. Sies H (1999) Glutathione and its role in cellular functions. Free Radic Biol Med 27:916–921. https://doi.org/10.1016/S0891-5849(99)00177-X

    Article  CAS  Google Scholar 

  38. Kullisaar T, Songisepp E, Aunapuu M, Kilk K, Arend A, Mikelsaar M, Rehema A, Zilmer M (2010) Complete glutathione system in probiotic Lactobacillus fermentum ME-3. Appl Biochem Microbiol 46:481–486. https://doi.org/10.1134/S0003683810050030

    Article  CAS  Google Scholar 

  39. Serrano LM, Molenaar D, Wels M, Teusink B, Bron PA, Vos WMD, Smid EJ (2007) Thioredoxin reductase is a key factor in the oxidative stress response of Lactobacillus plantarumWCFS1. Microb Cell Factories 6:29. https://doi.org/10.1186/1475-2859-6-29

    Article  CAS  Google Scholar 

  40. Marnett LJ (1999) Lipid peroxidation-DNA damage by malondialdehyde. Mutat Res-fund Mol M 424:83–95. https://doi.org/10.1016/S0027-5107(99)00010-X

    Article  CAS  Google Scholar 

  41. Lin X, Yongjun X, Guangqiang W, Zhiqiang X, Hui Z, Fengxi L, Lianzhong A (2018) Lactobacillus plantarum AR501 alleviates the oxidative stress of D-Galactose-induced aging mice liver by upregulation of Nrf2-mediated antioxidant enzyme expression. J Food Sci 83:1990–1998. https://doi.org/10.1111/1750-3841.14200

    Article  CAS  Google Scholar 

  42. Saxelin M, Tynkkynen S, Mattila-Sandholm T, Vos WMD (2005) Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol 16:204–211. https://doi.org/10.1016/J.COPBIO.2005.02.003

    Article  CAS  Google Scholar 

  43. Maldonado A, Jimenez-Diaz R, Ruiz-Barba JL (2004) Induction of plantaricin production in Lactobacillus plantarum NC8 after coculture with specific gram-positive bacteria is mediated by an autoinduction mechanism. J Bacteriol 186:1556–1564. https://doi.org/10.1128/JB.186.5.1556-1564.2004

    Article  CAS  Google Scholar 

  44. Rojo-Bezares B, Saenz Y, Navarro L, Zarazaga M, Ruiz-Larrea F, Torres C (2007) Coculture-inducible bacteriocin activity of Lactobacillus plantarum strain J23 isolated from grape must. Food Microbiol 24:482–491. https://doi.org/10.1016/J.FM.2006.09.003

    Article  CAS  Google Scholar 

  45. Corr SC, Li Y, Riedel CU, O’Toole PW, Hill C, Gahan CGM (2007) Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc Natl Acad Sci U S A 104:7617–7621. https://doi.org/10.1073/PNAS.0700440104

    Article  CAS  Google Scholar 

Download references

Funding

This work was sponsored by the National Natural Science Foundation of China (NSF31260363, 31000048, 31260263).

Author information

Authors and Affiliations

  1. State Key Laboratory of Food Science and Technology, Nanchang University, Nanchang, 330047, People’s Republic of China

    Xiaomin Yu, Yijuan Li, Hua Wei & Feng Xu

  2. Department of Pathology and Immunology, Baylor College of Medicine, Houston, TX, 77030, USA

    Qinglong Wu

  3. Food and Nutritional Science, School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Hong Kong, China

    Nagendra P. Shah

Authors
  1. Xiaomin Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yijuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qinglong Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nagendra P. Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hua Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Feng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F.X. and H.W. performed and designed experiments; X.Y. analyzed data and wrote the manuscript; Y.L. and X.Y. performed experiments; N.P.S. and Q.W. edited the manuscript and provided advice. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Feng Xu.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All applicable institutional guidelines for the care and use of animals were followed.

Additional information

Nucleotide Sequence Accession Number

The complete genome sequence of L. plantarum FLPL05 was deposited in GenBank under the accession number CP046119. This strain has been deposited to China Center for Type Culture Collection under the accession number CCTCC No. M2017763.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

ESM 1

(PDF 278 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, X., Li, Y., Wu, Q. et al. Genomic Analysis for Antioxidant Property of Lactobacillus plantarum FLPL05 from Chinese Longevity People. Probiotics & Antimicro. Prot. 12, 1451–1458 (2020). https://doi.org/10.1007/s12602-020-09704-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-020-09704-0

Keywords

Search

Navigation