Abstract
Probiotic is an alternative method to treat intestinal infection disease caused by antibiotic-resistant bacteria. In this study, Lactococcus lactis KA-FF 1-4 demonstrated to have the potential to inhibit the growth of Vancomycin-resistant enterococci (VRE) by producing anti-microbial substance. In co-culture, L. lactis KA-FF 1-4 (108 CFU/mL) inhibited the growth of VRE from 103–104 CFU/mL to zero after 6 h of exposure. However, in a gut model contained human gut microbiota, this anti-VRE activity of L. lactis KA-FF 1-4 was reduced to only 3.59–6.12%. The unexpected difference in efficacy between the experimental models could be explained by the fact that the growth of L. lactis KA-FF 1-4 was stable in the gut model. Leaving aside these limitations, we observed that adding L. lactis KA-FF 1-4 into the human gut model containing VRE was able to enhance microbial richness and diversity. Specifically, a higher abundance of beneficial microbes from the group of Bifidobacterium spp. and Bacteroides fragilis. L. lactis KA-FF 1-4 also enhanced the abundance of Parabacteroides, Lactococcus, and Fusobacterium and promoted the production of lactic acid in the gut model. However, these effects were not observed in the gut model without L. lactis KA-FF 1-4. Even though this study could not demonstrate a significant anti-VRE effect of the L. lactis KA-FF 1-4 in a gut model, our results still offer evidence that L. lactis KA-FF 1-4 could positively modulate the gut microbiota by promoting the growth of beneficial microbes and their metabolite. L. lactis KA-FF 1-4 has probiotic properties to fight against VRE infection, therefore further investigation in animal model is needed.
Similar content being viewed by others
References
Adamberg S, Tomson K, Vija H, Puurand M, Kabanova N, Visnapuu T, Jõgi E, Alamäe T, Adamberg K (2014) Degradation of fructans and production of propionic acid by bacteroides thetaiotaomicron are enhanced by the shortage of amino acids. Front Nutr 1:21
Alexander C, Swanson KS, Fahey GC Jr, Garleb KA (2019) Perspective: physiologic importance of short-chain fatty acids from nondigestible carbohydrate fermentation. Adv Nutr 10(4):576–589
Almohaya AM, Almutairy TS, Alqahtani A, Binkhamis K, Almajid FM (2020) Fusobacterium bloodstream infections: a literature review and hospital-based case series. Anaerobe 62:102165
Baothman OA, Zamzami MA, Taher I, Abubaker J, Abu-Farha M (2016) The role of gut microbiota in the development of obesity and diabetes. Lipids Health Dis 15(1):108
Bartosch S, Fite A, Macfarlane GT, McMurdo MET (2004) Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol 70(6):3575–3581
Belizario JE, Faintuch J, Garay-Malpartida M (2018) Gut microbiome dysbiosis and immunometabolism: new frontiers for treatment of metabolic diseases. Mediat Inflamm 2018:2037838
Blandino G, Inturri R, Lazzara F, Di Rosa M, Malaguarnera L (2016) Impact of gut microbiota on diabetes mellitus. Diabetes Metab 42(5):303–315
Doron S, Hibberd PL, Goldin B, Thorpe C, McDermott L, Snydman DR (2015) Effect of Lactobacillus rhamnosus GG administration on vancomycin-resistant enterococcus colonization in adults with comorbidities. Antimicrob Agents Chemother 59(8):4593–4599
Dou L, Meng D, Dong Y, Chen L, Han X, Fan D, Dong H (2020) Dosage regimen and toxicity risk assessment of linezolid in sepsis patients. Int J Infect Dis 96:105–111
Gill PA, van Zelm MC, Muir JG, Gibson PR (2018) Review article: short chain fatty acids as potential therapeutic agents in human gastrointestinal and inflammatory disorders. Aliment Pharmacol Ther 48(1):15–34
Houlihan HH, Stokes DP, Rybak MJ (2000) Pharmacodynamics of vancomycin and ampicillin alone and in combination with gentamicin once daily or thrice daily against Enterococcus faecalis in an in vitro infection model. J Antimicrob Chemother 46(1):79–86
Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D (2015) Role of the normal gut microbiota. World J Gastroenterol 21(29):8787–8803
La-Ongkham O, Nakphaichit M, Leelavatcharamas V, Keawsompong S, Nitisinprasert S (2015) Distinct gut microbiota of healthy children from two different geographic regions of Thailand. Arch Microbiol 197(4):561–573
Li L, Ma L, Fu P (2017) Gut microbiota-derived short-chain fatty acids and kidney diseases. Drug Des Dev Ther 11:3531–3542
Lund M, Bjerrum L, Pedersen K (2010) Quantification of Faecalibacterium prausnitzii- and Subdoligranulum variabile-like bacteria in the cecum of chickens by real-time PCR. Poult Sci 89(6):1217–1224
Marcos M, Iñurrieta A, Soriano A, Martínez JA, Almela M, Marco F, Mensa J (2008) Effect of antimicrobial therapy on mortality in 377 episodes of Enterobacter spp. bacteraemia. J Antimicrob Chemother 62(2):397–403
Martinis E, Alves V, Franco B (2002) Fundamentals and perspectives for the use of bacteriocins produced by lactic acid bacteria in meat products. Food Rev Int 18:191–208
Matsuki T, Watanabe K, Fujimoto J, Miyamoto Y, Takada T, Matsumoto K, Oyaizu H, Tanaka R (2002) Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol 68(11):5445–5451
Matsuki T, Watanabe K, Fujimoto J, Takada T, Tanaka R (2004) Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol 70(12):7220–7228
McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6(3):610–618
Millette M, Cornut G, Dupont C, Shareck F, Archambault D, Lacroix M (2008) Capacity of human nisin- and pediocin-producing lactic acid bacteria to reduce intestinal colonization by vancomycin-resistant enterococci. Appl Environ Microbiol 74(7):1997–2003
Moise PA, Sakoulas G, McKinnell JA, Lamp KC, DePestel DD, Yoon MJ, Reyes K, Zervos MJ (2015) Clinical outcomes of daptomycin for vancomycin-resistant enterococcus bacteremia. Clin Ther 37(7):1443–1453
Morrison DJ, Preston T (2016) Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7(3):189–200
Nakayama J (2010) Pyrosequence-based 16S rRNA profiling of gastrointestinal microbiota. Biosci Microflo 29(2):83–96
Onumpai C, Kolida S, Bonnin E, Rastall RA (2011) Microbial utilization and selectivity of pectin fractions with various structures. Appl Environ Microbiol 77(16):5747–5754
Phumisantiphong U, Siripanichgon K, Reamtong O, Diraphat P (2017) A novel bacteriocin from Enterococcus faecalis 478 exhibits a potent activity against vancomycin-resistant enterococci. PLoS ONE 12(10):e0186415
Phuttisarikorn T, Phumsombat P, Nitisinpraset S (2018) Optimization of bacteriocin lacnegacin production by Lactococcus lactis KA-FF 1-4. In: The 53th Kasetsart University annual conference book. KURDI Publisher, Bangkok, pp 1092–1099
Pokusaeva K, Fitzgerald GF, van Sinderen D (2011) Carbohydrate metabolism in bifidobacteria. Genes Nutr 6(3):285–306
Rinttilä T, Kassinen A, Malinen E, Krogius L, Palva A (2004) Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microb 97(6):1166–1177
Ríos-Covián D, Arboleya S, Hernandez-Barranco AM, Alvarez-Buylla JR, Ruas-Madiedo P, Gueimonde M, de los Reyes-Gavilan CG (2013) Interactions between Bifidobacterium and Bacteroides species in cofermentations are affected by carbon sources, including exopolysaccharides produced by bifidobacteria. Appl Environ Microbiol 79(23):7518–7524
Ríos-Covián D, Ruas-Madiedo P, Margolles A, Gueimonde M, de Los Reyes-Gavilán CG, Salazar N (2016) Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol 7:185–185
Rowland I, Gibson G, Heinken A, Scott K, Swann J, Thiele I, Tuohy K (2018) Gut microbiota functions: metabolism of nutrients and other food components. Eur J Nutr 57(1):1–24
Saelim K, Sohsomboon N, Kaewsuwan S, Maneerat S (2012) Probiotic properties of Enterococcus faecium CE5-1 producing a bacteriocin-like substance and its antagonistic effect against antibiotic-resistant enterococci in vitro. Czech J Anim Sci 57:529–539
Shetty SA, Smidt H, de Vos WM (2019) Reconstructing functional networks in the human intestinal tract using synthetic microbiomes. COBIOT 58:146–154
Shokri D, Zaghian S, Khodabakhsh F, Fazeli H, Mobasherizadeh S, Ataei B (2014) Antimicrobial activity of a UV-stable bacteriocin-like inhibitory substance (BLIS) produced by Enterococcus faecium strain DSH20 against vancomycin-resistant enterococcus (VRE) strains. J Microbiol Immunol Infect 47(5):371–376
Stefanaki C, Bacopoulou F, Michos A (2018) The impact of probiotics' administration on glycemic control, body composition, gut microbiome, mitochondria, and other hormonal signals in adolescents with prediabetes—a randomized, controlled trial study protocol. Contemp Clin Trials Commun 11:55–62
Sun Y, Cui X, Duan M, Ai C, Song S, Chen X (2019) In vitro fermentation of κ-carrageenan oligosaccharides by human gut microbiota and its inflammatory effect on HT29 cells. J Funct Foods 59:80–91
Ventola CL (2015) The antibiotic resistance crisis: part 1: causes and threats. P T 40(4):277–283
Verbeke KA, Boobis AR, Chiodini A, Edwards CA, Franck A, Kleerebezem M, Nauta A, Raes J, van Tol EAF, Tuohy KM (2015) Towards microbial fermentation metabolites as markers for health benefits of prebiotics. Nutr Res Rev 28(1):42–66
Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammers WP (2001) Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol 67(6):2578–2585
Xiang N, Lyu Y, Zhu X, Bhunia AK, Narsimhan G (2016) Methodology for identification of pore forming antimicrobial peptides from soy protein subunits β-conglycinin and glycinin. Peptides 85:27–40
Yang T, Santisteban Monica M, Rodriguez V, Li E, Ahmari N, Carvajal Jessica M, Zadeh M, Gong M, Qi Y, Zubcevic J, Sahay B, Pepine Carl J, Raizada Mohan K, Mohamadzadeh M (2015) Gut dysbiosis is linked to hypertension. Hypertension 65(6):1331–1340
Yasir M, Angelakis E, Bibi F, Azhar EI, Bachar D, Lagier JC, Gaborit B, Hassan AM, Jiman-Fatani AA, Alshali KZ, Robert C, Dutour A, Raoult D (2015) Comparison of the gut microbiota of people in France and Saudi Arabia. Nutr Diabetes 5:e153
Zeppa G, Conterno L, Gerbi V (2001) Determination of organic acids, sugars, diacetyl, and acetoin in cheese by high-performance liquid chromatography. J Agric Food Chem 49(6):2722–2726
Acknowledgements
This research was supported by Research and Researcher for Industries (RRI) Scholarship M.S. program (MSD58I0008). Scholarship: The Thailand Research Fund (TRF), MAG, CDIP (Thailand) Co., Ltd. We are grateful to Dr. Gabrila Martínes-Chacón for careful review that greatly improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Rights and permissions
About this article
Cite this article
Plupjeen, Sn., Chawjiraphan, W., Charoensiddhi, S. et al. Lactococcus lactis KA-FF 1-4 reduces vancomycin-resistant enterococci and impacts the human gut microbiome. 3 Biotech 10, 295 (2020). https://doi.org/10.1007/s13205-020-02282-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-020-02282-6