Skip to main content
SpringerLink
Log in

Probiotic Potential and Wide-spectrum Antimicrobial Activity of Lactic Acid Bacteria Isolated from Infant Feces

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

Abstract

In this study, we aimed to characterize lactic acid bacteria strains derived from infants’ feces, to evaluate the probiotic potential and explore the wide-spectrum antimicrobial activity. Of 800 isolates, 20 inhibited the growth of enterotoxigenic Escherichia coli K88 and Salmonella enterica ATCC 13076. On the basis of 16S rRNA sequence analysis, the 20 isolates were assigned to Lactobacillus casei (7), Lactobacillus paracasei (2), Lactobacillus plantarum (4), Lactobacillus rhamnosus (2), Enterococcus avium (3), Enterococcus faecium (1), and Enterococcus lactis (1) species. In addition, 12 strains with high antimicrobial activity were investigated for the presence of probiotic properties such as physiological-biochemical characteristics, antimicrobial susceptibility, hemolytic activity, hydrophobicity, and aggregation activity. Wide-spectrum antimicrobial activity analysis revealed that approximately all tested strains inhibited the ten pathogens, and four strains (ZX221, ZX633, ZX3131, and ZX3875) had good probiotic properties and survived after being exposed to simulated gastrointestinal tract conditions. Moreover, we investigated the influence of pH on the wide-spectrum antimicrobial activity and found that four strains inhibited most pathogens at pH 4.5 and pH 5, whereas only ZX633 had an inhibitory effect on Bacillus subtilis ATCC 6633 and Micrococcus luteus ATCC 4698 at pH 5.5. Overall, Lact. casei ZX633 had wide-spectrum antimicrobial activity and could be considered a potential probiotic.

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. Tarrah A, da Silva DV, de Castilhos J, Pakroo S, Lemos Junior WJF, Luchese RH, Fioravante Guerra A, Rossi RC, Righetto Ziegler D, Corich V, Giacomini A (2019) Probiotic potential and biofilm inhibitory activity of Lactobacillus casei group strains isolated from infant feces. J Funct Foods 54:489–497. https://doi.org/10.1016/j.jff.2019.02.004

    Article  CAS  Google Scholar 

  2. Castilho NPA, Colombo M, Oliveira LL, Todorov SD, Nero LA (2019) Lactobacillus curvatus UFV-NPAC1 and other lactic acid bacteria isolated from calabresa, a fermented meat product, present high bacteriocinogenic activity against Listeria monocytogenes. BMC Microbiol 19(1):63–76. https://doi.org/10.1186/s12866-019-1436-4

    Article  PubMed  PubMed Central  Google Scholar 

  3. Muhammad Z, Ramzan R, Abdelazez A, Amjad A, Afzaal M, Zhang S, Pan S (2019) Assessment of the antimicrobial potentiality and functionality of Lactobacillus plantarum strains isolated from the conventional inner Mongolian fermented cheese against foodborne pathogens. Pathog 8(2):71–91. https://doi.org/10.3390/pathogens8020071

    Article  CAS  Google Scholar 

  4. Sharma K, Attri S, Goel G (2019) Selection and evaluation of probiotic and functional characteristics of autochthonous lactic acid bacteria isolated from fermented wheat flour dough babroo. Probiotics Antimicrob Proteins 11(3):774–784. https://doi.org/10.1007/s12602-018-9466-z

    Article  CAS  PubMed  Google Scholar 

  5. Kim HJ, Lee HJ, Lim B, Kim E, Kim HY, Suh M, Hur M (2018) Lactobacillus terrae sp. nov., a novel species isolated from soil samples in the Republic of Korea. Int J Syst Evol Microbiol 68(9):2906–2911. https://doi.org/10.1099/ijsem.0.002918

    Article  CAS  PubMed  Google Scholar 

  6. Joghataei M, Shahidi F, Pouladfar G, Mortazavi SA, Ghaderi A (2019) Probiotic potential comparison of Lactobacillus strains isolated from Iranian traditional food products and human feces with standard probiotic strains. J Sci Food Agric 99(15):6680–6688. https://doi.org/10.1002/jsfa.9945

    Article  CAS  PubMed  Google Scholar 

  7. Gheziel C, Russo P, Arena MP, Spano G, Ouzari HI, Kheroua O, Saidi D, Fiocco D, Kaddouri H, Capozzi V (2019) Evaluating the probiotic potential of Lactobacillus plantarum strains from Algerian infant feces: towards the design of probiotic starter cultures tailored for developing countries. Probiotics Antimicrob Proteins 11(1):113–123. https://doi.org/10.1007/s12602-018-9396-9

    Article  CAS  PubMed  Google Scholar 

  8. Liu C, Zhang ZY, Dong K, Yuan JP, Guo XK (2009) Antibiotic resistance of probiotic strains of lactic acid bacteria isolated from marketed foods and drugs. Biomed Environ Sci 22(5):401–412. https://doi.org/10.1016/S0895-3988(10)60018-9

    Article  CAS  PubMed  Google Scholar 

  9. Coman MM, Verdenelli MC, Cecchini C, Bela B, Gramenzi A, Orpianesi C, Cresci A, Silvi S (2019) Probiotic characterization of Lactobacillus isolates from canine faeces. J Appl Microbiol 126(4):1245–1256. https://doi.org/10.1111/jam.14197

    Article  CAS  PubMed  Google Scholar 

  10. Halimi S, Mirsalehian A (2016) Assessment and comparison of probiotic potential of four Lactobacillus species isolated from feces samples of Iranian infants. Microbiol Immunol 60(2):73–81. https://doi.org/10.1111/1348-0421.12352

    Article  CAS  PubMed  Google Scholar 

  11. Oguntoyinbo FA, Narbad A (2015) Multifunctional properties of Lactobacillus plantarum strains isolated from fermented cereal foods. J Funct Foods 17:621–631. https://doi.org/10.1016/j.jff.2015.06.022

    Article  CAS  Google Scholar 

  12. Cervantes-Elizarrarás A, Cruz-Cansino N, Ramírez-Moreno E, Vega-Sánchez V, Velázquez-Guadarrama N, Zafra-Rojas Q, Piloni-Martini J (2019) In vitro probiotic potential of lactic acid bacteria isolated from aguamiel and pulque and antibacterial activity against pathogens. Appl Sci 9(3):601. https://doi.org/10.3390/app9030601

    Article  CAS  Google Scholar 

  13. Al Kassaa I, Hamze M, Hober D, Chihib NE, Drider D (2014) Identification of vaginal Lactobacilli with potential probiotic properties isolated from women in North Lebanon. Microb Ecol 67(3):722–734. https://doi.org/10.1007/s00248-014-0384-7

    Article  PubMed  Google Scholar 

  14. Wang Y, Li A, Jiang X, Zhang H, Mehmood K, Zhang L, Jiang J, Waqas M, Iqbal M, Li J (2018) Probiotic potential of Leuconostoc pseudomesenteroides and Lactobacillus strains isolated from yaks. Front Microbiol 9:2987. https://doi.org/10.3389/fmicb.2018.02987

    Article  PubMed  PubMed Central  Google Scholar 

  15. Zhang M, Wang YP, Tan ZF, Li ZW, Li Y, Lv HX, Zhang B, Jin QS (2017) Microorganism profile, fermentation quality and rumen digestibility in vitro of maize-stalk silages produced at different maturity stages. Crop Pasture Sci 68(3):225–233. https://doi.org/10.1071/CP16324

    Article  CAS  Google Scholar 

  16. Zhang M, Wang X, Cui M, Wang Y, Jiao Z, Tan Z (2018) Ensilage of oats and wheatgrass under natural alpine climatic conditions by indigenous lactic acid bacteria species isolated from high-cold areas. PLoS One 13(2):1–15. https://doi.org/10.1371/journal.pone.0192368

    Article  CAS  Google Scholar 

  17. Niu KM, Kothari D, Cho SB, Han SG, Song IG, Kim SC, Kim SK (2019) Exploring the probiotic and compound feed fermentative applications of Lactobacillus plantarum SK1305 isolated from Korean green chili pickled pepper. Probiotics Antimicrob Proteins 11(3):801–812. https://doi.org/10.1007/s12602-018-9447-2

    Article  CAS  PubMed  Google Scholar 

  18. de Souza BMS, Borgonovi TF, Casarotti SN, Todorov SD, Penna ALB (2019) Lactobacillus casei and Lactobacillus fermentum strains isolated from mozzarella cheese: probiotic potential, safety, acidifying kinetic parameters and viability under gastrointestinal tract conditions. Probiotics Antimicrob Proteins 11(2):382–396. https://doi.org/10.1007/s12602-018-9406-y

    Article  CAS  PubMed  Google Scholar 

  19. Mohanty D, Panda S, Kumar S, Ray P (2019) In vitro evaluation of adherence and anti-infective property of probiotic Lactobacillus plantarum DM 69 against Salmonella enterica. Microb Pathog 126:212–217. https://doi.org/10.1016/j.micpath.2018.11.014

    Article  CAS  PubMed  Google Scholar 

  20. Sirichokchatchawan W, Pupa P, Praechansri P, Am-In N, Tanasupawat S, Sonthayanon P, Prapasarakul N (2018) Autochthonous lactic acid bacteria isolated from pig faeces in Thailand show probiotic properties and antibacterial activity against enteric pathogenic bacteria. Microb Pathog 119:208–215. https://doi.org/10.1016/j.micpath.2018.04.031

    Article  CAS  PubMed  Google Scholar 

  21. Zhang B, Wang YP, Tan ZF, Li ZW, Jiao Z, Huang QC (2016) Screening of probiotic activities of Lactobacilli strains isolated from traditional Tibetan Qula, a raw yak milk cheese. Asian Australas J Anim Sci 29(10):1490–1499. https://doi.org/10.5713/ajas.15.0849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Li YT, Xu H, Ye JZ, Wu WR, Shi D, Fang DQ, Liu Y, Li LJ (2019) Efficacy of Lactobacillus rhamnosus GG in treatment of acute pediatric diarrhea: a systematic review with meta-analysis. World J Gastroenterol 25(33):4999–5016. https://doi.org/10.3748/wjg.v25.i33.4999

    Article  PubMed  PubMed Central  Google Scholar 

  23. Bonyadian M, Barati S, Mahzounieh MR (2019) Phenotypic and genotypic characterization of antibiotic-resistant in Escherichia coli isolates from patients with diarrhea. Iran J Microbiol 11(3):220–224. https://doi.org/10.18502/ijm.v11i3.1323

    Article  PubMed  PubMed Central  Google Scholar 

  24. Wei Z, Xu X, Yan M, Chang H, Li Y, Kan B, Zeng M (2019) Salmonella Typhimurium and Salmonella enteritidis infections in sporadic diarrhea in children: source tracing and resistance to third-generation cephalosporins and ciprofloxacin. Foodborne Pathog Dis 16(4):244–255. https://doi.org/10.1089/fpd.2018.2557

    Article  CAS  PubMed  Google Scholar 

  25. Ouarabi L, Chait YA, Seddik HA, Drider D, Bendali F (2019) Newly isolated Lactobacilli strains from Algerian human vaginal microbiota: Lactobacillus fermentum strains relevant probiotic’s candidates. Probiotics Antimicrob Proteins 11(1):43–54. https://doi.org/10.1007/s12602-017-9360-0

    Article  CAS  PubMed  Google Scholar 

  26. Cui X, Shi Y, Gu S, Yan X, Chen H, Ge J (2018) Antibacterial and antibiofilm activity of lactic acid bacteria isolated from traditional artisanal milk cheese from Northeast China against enteropathogenic bacteria. Probiotics Antimicrob Proteins 10(4):601–610. https://doi.org/10.1007/s12602-017-9364-9

    Article  CAS  PubMed  Google Scholar 

  27. Delgado S, Florez AB, Mayo B (2005) Antibiotic susceptibility of Lactobacillus and Bifidobacterium species from the human gastrointestinal tract. Curr Microbiol 50(4):202–207. https://doi.org/10.1007/s00284-004-4431-3

    Article  CAS  PubMed  Google Scholar 

  28. Zhou JS, Pillidge CJ, Gopal PK, Gill HS (2005) Antibiotic susceptibility profiles of new probiotic Lactobacillus and Bifidobacterium strains. Int J Food Microbiol 98(2):211–217. https://doi.org/10.1016/j.ijfoodmicro.2004.05.011

    Article  CAS  PubMed  Google Scholar 

  29. Teuber M, Meile L, Schwarz F (1999) Acquired antibiotic resistance in lactic acid bacteria from food. Antonie Van Leeuwenhoek 76:115–137. https://doi.org/10.1023/A:1002035622988

    Article  CAS  PubMed  Google Scholar 

  30. Franz CMAP, Stiles ME, Schleifer KH, Holzapfel WH (2003) Enterococci in foods - a conundrum for food safety. Int J Food Micrbiol 88(2–3):105–122. https://doi.org/10.1016/S0168-1605(03)00174-0

    Article  CAS  Google Scholar 

  31. Toomey N, Bolton D, Fanning S (2010) Characterisation and transferability of antibiotic resistance genes from lactic acid bacteria isolated from Irish pork and beef abattoirs. Res Microbiol 161(2):127–135. https://doi.org/10.1016/j.resmic.2009.12.010

    Article  CAS  PubMed  Google Scholar 

  32. Valenzuela AS, Ben Omar N, Abriouel H, Lopez RL, Veljovic K, Canamero MM, Topisirovic MKL, Galvez A (2009) Virulence factors, antibiotic resistance, and bacteriocins in Enterococci from artisan foods of animal origin. Food Control 20(4):381–385. https://doi.org/10.1016/j.foodcont.2008.06.004

    Article  CAS  Google Scholar 

  33. Wang J, Wei X, Fan M (2018) Assessment of antibiotic susceptibility within lactic acid bacteria and coagulase-negative Staphylococci isolated from Hunan smoked pork, a naturally fermented meat product in China. J Food Sci 83(6):1707–1715. https://doi.org/10.1111/1750-3841.14147

    Article  CAS  PubMed  Google Scholar 

  34. Saelim K, Jampaphaeng K, Maneerat S (2017) Functional properties of Lactobacillus plantarum S0/7 isolated fermented stinky bean (Sa Taw Dong) and its use as a starter culture. J Funct Foods 38:370–377. https://doi.org/10.1016/j.jff.2017.09.035

    Article  CAS  Google Scholar 

  35. Wang J, Wang J, Yang K, Liu M, Zhang J, Wei X, Fan M (2018) Screening for potential probiotic from spontaneously fermented non-dairy foods based on in vitro probiotic and safety properties. Ann Microbiol 68(12):803–813. https://doi.org/10.1007/s13213-018-1386-3

    Article  CAS  Google Scholar 

  36. Das JK, Mishra D, Ray P, Tripathy P, Beuria TK, Singh N, Suar M (2013) In vitro evaluation of anti-infective activity of a Lactobacillus plantarum strain against Salmonella enterica serovar enteritidis. Gut Pathog 5(1):11. https://doi.org/10.1186/1757-4749-5-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Riaz Rajoka MS, Mehwish HM, Siddiq M, Haobin Z, Zhu J, Yan L, Shao D, Xu X, Shi J (2017) Identification, characterization, and probiotic potential of Lactobacillus rhamnosus isolated from human milk. LWT - Food Sci Technol 84:271–280. https://doi.org/10.1016/j.lwt.2017.05.055

    Article  CAS  Google Scholar 

  38. Todorov SD, Furtado DN, Saad SM, Tome E, Franco BD (2011) Potential beneficial properties of bacteriocin-producing lactic acid bacteria isolated from smoked salmon. J Appl Microbiol 110(4):971–986. https://doi.org/10.1111/j.1365-2672.2011.04950.x

    Article  CAS  PubMed  Google Scholar 

  39. Vizoso Pinto MG, Schuster T, Briviba K, Watzl B, Holzapfel WH, Franz CM (2007) Adhesive and chemokine stimulatory properties of potentially probiotic Lactobacillus strains. J Food Prot 70(1):125–134. https://doi.org/10.4315/0362-028x-70.1.125

    Article  PubMed  Google Scholar 

  40. Kotzamanidis C, Kourelis A, Litopoulou-Tzanetaki E, Tzanetakis N, Yiangou M (2010) Evaluation of adhesion capacity, cell surface traits and immunomodulatory activity of presumptive probiotic Lactobacillus strains. Int J Food Microbiol 140(2–3):154–163. https://doi.org/10.1016/j.ijfoodmicro.2010.04.004

    Article  CAS  PubMed  Google Scholar 

  41. Ramos CL, Thorsen L, Schwan RF, Jespersen L (2013) Strain-specific probiotics properties of Lactobacillus fermentum, Lactobacillus plantarum and Lactobacillus brevis isolates from Brazilian food products. Food Microbiol 36(1):22–29. https://doi.org/10.1016/j.fm.2013.03.010

    Article  CAS  PubMed  Google Scholar 

  42. Ferrari Ida S, de Souza JV, Ramos CL, da Costa MM, Schwan RF, Dias FS (2016) Selection of autochthonous lactic acid bacteria from goat dairies and their addition to evaluate the inhibition of Salmonella typhi in artisanal cheese. Food Microbiol 60:29–38. https://doi.org/10.1016/j.fm.2016.06.014

    Article  CAS  PubMed  Google Scholar 

  43. Kaewnopparat S, Dangmanee N, Kaewnopparat N, Srichana T, Chulasiri M, Settharaksa S (2013) In vitro probiotic properties of Lactobacillus fermentum SK5 isolated from vagina of a healthy woman. Anaerobe 22:6–13. https://doi.org/10.1016/j.anaerobe.2013.04.009

    Article  CAS  PubMed  Google Scholar 

  44. Lee KW, Park JY, Sa HD, Jeong JH, Jin DE, Heo HJ, Kim JH (2014) Probiotic properties of Pediococcus strains isolated from jeotgals, salted and fermented Korean sea-food. Anaerobe 28:199–206. https://doi.org/10.1016/j.anaerobe.2014.06.013

    Article  CAS  PubMed  Google Scholar 

  45. 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  PubMed  PubMed Central  Google Scholar 

  46. Saavedra L, Minahk C, Holgado APD, Sesma F (2004) Enhancement of the enterocin CRL35 activity by a synthetic peptide derived from the NH2-terminal sequence. Antimicrob Agents Chemother 48(7):2778–2781. https://doi.org/10.1128/AAC.48.7.2778-2781.2004

Download references

Funding

This work was supported by the Qinghai Province Key R&D and Transformation Plan of China (No. 2020-NK 127) and Foundation of Key Technology Research Project of Henan Province (Grant No. 192102110082 and Grant No. 182102110090).

Author information

Authors and Affiliations

  1. Henan Key Laboratory of Ion-Beam Bioengineering, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, China

    Xing Wang, Hua Zhang, Yuan Liu, Miao Zhang, Yanping Wang & Zhongfang Tan

  2. The Third Affiliated Hospital Xinxiang Medical University, Xinxiang, China

    Weidong Wang

  3. School of Food Science and Technology, Henan University of Technology, Zhengzhou, China

    Haoxin Lv

  4. School of Food and Biological Engineering, Henan University of Animal Husbandry and Economy, Zhengzhou, China

    Hua Zhang

Authors
  1. Xing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weidong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haoxin Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Miao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yanping Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhongfang Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhongfang Tan.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Wang, W., Lv, H. et al. Probiotic Potential and Wide-spectrum Antimicrobial Activity of Lactic Acid Bacteria Isolated from Infant Feces. Probiotics & Antimicro. Prot. 13, 90–101 (2021). https://doi.org/10.1007/s12602-020-09658-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-020-09658-3

Keywords

Search

Navigation