Skip to main content

Advertisement

SpringerLink
Log in

Genetic Variation of pln Loci Among Probiotic Lactobacillus plantarum Group Strains with Antioxidant and Cholesterol-Lowering Ability

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

Abstract

In the present study, 14 different plantaricin-encoding genes of pln loci were studied and compared to available sequences from public domain database of probiotic Lactobacillus plantarum strains. Based upon the presence and absence of selected genes, pln locus was grouped into eight clusters. Further, quantitative real-time PCR (qRT-PCR) analysis for seven genes has discriminated the complex pln locus into five types which includes WCFS1 (in Lactobacillus plantarum subsp. plantarum MCC 2976 and MCC 2974 and Lactobacillus paraplantarum MCC 2978), closely related to J51 (in Lb. paraplantarum MCC 2973 and MCC 2977), J23 (in Lb. plantarum MTCC 5422), NC8 (in Lb. paraplantarum MTCC 9483), and a new E1 type (in Lb. plantarum subsp. plantarum E1). It was observed that the plnA, EF, NC8βα, NC81F, NC8HK, and G were expressed in E1 strain. Further, southern hybridization confirmed the chromosome-encoded plantaricin in Lb. plantarum group (LPG) strains. Several PCR assays and DNA sequence analysis of the regions amplified in pln loci of E1 isolate suggested a hybrid variant of NC8 and J51 plantaritypes. This indicates the wide distribution of plantaricin with remarkable variation, diversity, and plasticity among the LPG strains of vegetable origin. Further, the selected strains were able to reduce the growth of Kocuria rhizophila ATCC 9341 by 40–54% within 6 h of co-incubation under in vitro pathogen exclusion assay. These isolates also possessed cholesterol-lowering and antioxidant activity suggesting their application in the development of functional foods.

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

Similar content being viewed by others

References

  1. Zhang Z-Y, Lui C, Zhu Y-Z, Wei Y-X, Tian F (2012) Safety assessment of Lactobacillus plantarum JDM1 based on the complete genome. Int J Food Microbiol 153:116–170

    Google Scholar 

  2. Ren D, Li C, Qin Y, Yin R, Du S, Ye F, Lui C, Lui H, Wang M, Li Y, Sun Y, Li X, Tian M, Jin N (2014) In vitro evaluation of the probiotic and functional potential of Lactobacillus strains isolated from fermented food and human intestine. Anaerobe 30:1–10

    CAS  PubMed  Google Scholar 

  3. Devi SM, Archer AC, Halami PM (2015) Screening, characterization and in vitro evaluation of probiotic properties among lactic acid bacteria through comparative analysis. Probiotics Antimicro Prot 7:181–192

    CAS  Google Scholar 

  4. Shobharani P, Halami PM (2016) In vitro evaluation of the cholesterol-reducing ability of a potential probiotic Bacillus spp. Ann Microbiol 66:643–651

    CAS  Google Scholar 

  5. Devi SM, Aishwarya S, Halami PM (2016) Discrimination and divergence among Lactobacillus plantarum group (LPG) isolates with reference to their probiotic functionalities from vegetable origin. Syst Appl Microbiol 39:562–570

    CAS  PubMed  Google Scholar 

  6. Pisano MB, Patrignani F, Cosentino S, Guerzoni ME, Franz CMAP, Holzapfel WH (2011) Diversity and functional properties of Lactobacillus plantarum group strains isolated from Italian cheese products. Dairy Sci Technol 91:65–76

    CAS  Google Scholar 

  7. Huang C-H, Huang L, Wu C-P, Chang M-T (2016) Molecular discrimination of Lactobacillus plantarum group using comparative sequence analysis of the dnaJ gene and as a target for developing novel species-specific PCR primers. J Chinese Soc Ani Sci 45:45–55

    Google Scholar 

  8. Castro MP, Palavecino NZ, Herman C, Garro OA, Campo CA (2011) Lactic acid bacteria isolated from artisanal dry sausages: characterization of antibacterial compounds and study of the factors affecting bacteriocin production. Meat Sci 87:321–329

    CAS  PubMed  Google Scholar 

  9. Sabo SS, Vitolo M, Gonzalez JMD, de Souza Oliveira RP (2014) Overview of Lactobacillus plantarum as a promising bacteriocin producer among lactic acid bacteria. Food Res Int 64:27–536

    Google Scholar 

  10. Song D-F, Zhu M-Y, Gu Q (2014) Purification and characterization of plantaricin ZJ5, a new bacteriocin produced by Lactobacillus plantarum ZJ5. PLoS One 9(8):e105549

    PubMed  PubMed Central  Google Scholar 

  11. Diep DB, Straume D, Kjos M, Torres C, Nes IF (2009) An overview of the mosaic bacteriocin pln loci from Lactobacillus plantarum. Peptides 30:1562–1574

    CAS  PubMed  Google Scholar 

  12. Tsapieva A, Duplik N, Suvorov A (2011) Structure of plantaricin locus of Lactobacillus plantarum 8P-A3. Benefic Microbes 2:255–261

    CAS  Google Scholar 

  13. Tai HF, Foo HL, Rahim RA, Loh TC, Abdullah MP, Yoshinobu K (2015) Molecular characterization of new organization of plnEF and plW loci of bacteriocin genes harbor concomitantly in Lactobacillus plantarum I-UL4. Microb Cell Factories 14:1–13

    CAS  Google Scholar 

  14. Yadav R, Puniya AK, Shukla P (2016) Probiotic properties of Lactobacillus plantarum RYPR1 from an indigenous fermented beverage Rabadi. Front Microbiol 7:1–9

    CAS  Google Scholar 

  15. Liu C, Pan T (2010) In vitro effects of lactic acid bacteria on cancer cell viability and antioxidant activity. J Food Drug Anal 18:77–86

    Google Scholar 

  16. JH Y, Kim H (2014) Oxidative stress and cytokines in the pathogenesis of pancreatic cancer. J Cancer Prev 19:97–102

    Google Scholar 

  17. Xiang J, Wang G, Zhang Q, Liu X, Gu Z, Zhang H, Chen YQ, Chen W (2015) Determining antioxidant activities of lactobacilli cell-free supernatants by cellular antioxidant assay: a comparison with traditional methods. PLoS One 10(3):1–16

    Google Scholar 

  18. Devi SM, Halami PM (2017) Diversity and evolutionary aspects of mucin binding (MucBP) domain repeats among Lactobacillus plantarum group strains through comparative genetic analysis. Syst Appl Microbiol 40(4):237–244

    CAS  PubMed  Google Scholar 

  19. Chung DM, Kim KE, Jeong SY, Park CS, Ahn KH, Kim DH, Do K, Chun HK, Yoon BD, Koh HB, Kim HJ, Choi NS (2011) Rapid concentration of some bacteriocin-like compounds using an organic solvent. Food Sci Biotechnol 20(5):1457–1459

    CAS  Google Scholar 

  20. Devi SM, Halami PM (2011) Detection and characterization of pediocin PA-1/AcH like bacteriocin producing lactic acid bacteria. Curr Microbiol 63:181–185

    CAS  PubMed  Google Scholar 

  21. Saenz Y, Rojo-Bezares B, Navarro L, Diez L, Somalo S, Zarazaga M (2009) Genetic diversity of the pln locus among oenological Lactobacillus plantarum strains. Int J Food Microbiol 134:176–183

    CAS  PubMed  Google Scholar 

  22. Li P, Gu Q, Zhou Q (2016) Complete genome sequence of Lactobacillus plantarum LZ206, a potential probiotic strains with anti-microbial activity against food-borne pathogenic microorganisms. J Biotechnol 238:52–55

    CAS  PubMed  Google Scholar 

  23. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Altschul SF, Maddan TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Devi SM, Halami PM (2013) Detection of mobile genetic elements in pediocin PA-1 like producing lactic acid bacteria. J Basic Microbiol 52:1–7

    Google Scholar 

  26. 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(5):1556–1564

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Walther C, Rossano A, Thomann A, Perreten V (2008) Antibiotic resistance in Lactococcus species from bovine milk: presence of a mutated multidrug transporter mdt(A) gene in susceptible Lactococcus garvieae strains. Vet Microbiol 131:348–357

    CAS  PubMed  Google Scholar 

  28. Ramiah K, Reenen CA, Dicks LMT (2007) Expression of the mucus adhesion genes Mub and MapA, adhesion-like factor EF-Tu and bacteriocin gene plaA of Lactobacillus plantarum 423, monitored with real-time PCR. Int J Food Microbiol 116:405–409

    CAS  PubMed  Google Scholar 

  29. Valeriano VD, Balolong MMP, Kang DK (2014) In vitro evaluation of the mucin-adhesion ability and probiotic potential of Lactobacillus mucosae LM1. J Appl Microbiol 117:485–497

    CAS  PubMed  Google Scholar 

  30. Roopashri AN, Varadaraj MC (2009) Molecular characterization of native isolates of lactic acid bacteria, bifidobacteria and yeasts of beneficial attributes. Appl Microbiol Biotechnol 83:1115–1126

    CAS  PubMed  Google Scholar 

  31. Archer AC, Halami PM (2015) Probiotic attributes of Lactobacillus fermentum isolated from human feces and dairy products. Appl Microbiol Biotechnol 99:8113–8123

    CAS  PubMed  Google Scholar 

  32. Rudel LL, Morris MD (1973) Determination of cholesterol using Ophtaldealdehyde. J Lipid Res 14:364–366

    CAS  PubMed  Google Scholar 

  33. Albright SC, Winston WL, Zappe C (1999) Data analysis and decision making with Microsoft Excel. The engineering economist: A journal devoted to the problems of capital investment. Duxbury Press, Pacific Grove; 2001. 46(3):998. ISBN: 0-534-38932-5

  34. Seddik HA, Bendali F, Gancel F, Fliss I, Spano G, Drider D (2017) Lactobacillus plantarum and its probiotic and food potentialities. Probiotics Antimicro Prot 9(2):111–122

    Google Scholar 

  35. Zhang H, Liu L, Hao Y, Zhong S, Liu H, Han T, Xie Y (2013a) Isolation and partial characterization of a bacteriocin produced by Lactobacillus plantarum BM-1 isolated from a traditionally fermented Chinese meat product. Microbiol Immunol 57:746–755

    CAS  PubMed  Google Scholar 

  36. Rojo-Bezares B, Saenz Y, Navarro L, Jimenez-Diaz R, Zarazaga M, Ruiz-Larrea F, Torres C (2008) Characterization of a new organization of the plantaricin locus in the inducible bacteriocin-producing Lactobacillus plantarum J23 of grape must origin. Arch Microbiol 189:491–499

    CAS  PubMed  Google Scholar 

  37. Rizzello CG, Filannino P, Di Cagno R, Calasso M, Gobbetti M (2014) Quorum-sensing regulation of constitutive plantaricin by Lactobacillus plantarum strains under a model system for vegetables and fruits. Appl Environ Microbiol 80:777–787

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Zhang X, Shang N, Zhang X, Gui M, Li P (2013b) Role of plnB gene in the regulation of bacteriocin production in Lactobacillus paraplantarum L-XM1. Microbiol Res 168:305–310

    CAS  PubMed  Google Scholar 

  39. Ben Omar N, Abriouel H, Keleke S, Sanchez Valenzuela A, Martinez-Canamero M, Lucas Lopez R, Ortega E, Galvez A (2008) Bacteriocin producing Lactobacillus strains isolated from poto poto, a Congolese fermented maize product, and genetic fingerprinting of their plantaricin operons. Int J Food Microbiol 30:18–25

    Google Scholar 

  40. Kandi V, Palange P, Vaish R, Bhatti AB, Kale V, Kandi MR, Bhoomagiri MR (2016) Emerging bacterial infection: identification and clinical significance of Kocuria species. Cureus 8(8):1–6

    Google Scholar 

  41. Bordoni A, Amaretti A, Leonardi A, Boschetti E, Danesi F, Matteuzzi D, Roncaglia L, Raimondi S, Rossi M (2013) Cholesterol-lowering probiotics: in vitro selection and in vivo testing of Bifidobacteria. Appl Microbiol Biotechnol 97:8273–8281

    CAS  PubMed  Google Scholar 

  42. Tomaro-Duchesneau C, Jones ML, Shah D, Jain P, Saha S, Prakash S (2014) Cholesterol assimilation by Lactobacillus probiotic bacteria: an in vitro investigation. Biomed Res Int 2014:1–9

  43. Zhang Y, Lu Y, Wang J, Jang L, Pan C, Huang Y (2013) Probiotic properties of Lactobacillus strains isolated from Tibetan kefir grains. PLoS One 8(7):e69868

    Google Scholar 

  44. Kuda T, Kawahara M, Nemoto M, Takahashi H, Kimura B (2014) In vitro antioxidant and anti-inflammation properties of lactic acid bacteria from fish intestines and fermented fish from the Sanriku Satoumi region in Japan. Food Res Int 64:248–255

    CAS  PubMed  Google Scholar 

  45. Russo P, de Chiara MLV, Vernile A, Amodio ML, Arena MP, Capozzi V, Massa S, Spano G (2014) Fresh-cut pineapple as a new carrier of probiotic lactic acid bacteria. Biomed Res Int 2014:1–9

Download references

Acknowledgements

We express our gratitude to the Director, CSIR-CFTRI, for encouragement and facilities. SMD extend her thanks to SERB-Department of Science and Technology, New Delhi, for endorsing the study under start-up grant scheme (Project No. SB/YS/LS-353/2013).

Author information

Authors and Affiliations

  1. Microbiology and Fermentation Technology Department, CSIR—Central Food Technological Research Institute, Mysuru, 570020, India

    Sundru Manjulata Devi & Prakash M. Halami

Authors
  1. Sundru Manjulata Devi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Prakash M. Halami
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Prakash M. Halami.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic Supplementary Material

ESM 1

List of primers used in the present study (DOC 93 kb)

Fig. S1

Zone of inhibition of K. rhizophila by Lb. plantarum E1 under A) un-induced and B) induced conditions. (GIF 17 kb)

High resolution image (TIFF 851 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Devi, S.M., Halami, P.M. Genetic Variation of pln Loci Among Probiotic Lactobacillus plantarum Group Strains with Antioxidant and Cholesterol-Lowering Ability. Probiotics & Antimicro. Prot. 11, 11–22 (2019). https://doi.org/10.1007/s12602-017-9336-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-017-9336-0

Keywords

Search

Navigation