Comparison of the prevalence of bacteriocin encoding genes in Lactobacillus spp. isolated from fecal samples of healthy volunteers, IBD-patient and IBD-recovered
-
Seyedeh Tina Miri
,
Fattah Sotoodehnejadnematalahi
,
Mohammad Mehdi Amiri
,
Mohammad Reza Pourshafie
,
Mahdi Rohani
Abstract
Background and Objectives: Bacteriocins are antimicrobial peptides produced by many genera of bacteria especially Lactobacillus spp. against many pathogens, adapt bacterial composition in the gut and inhibit dysbiosis that can lead to inflammation disorders like inflammatory bowel disease (IBD). The aim of this study was to compare the prevalence of bacteriocin genes in health, IBD disease and recovery conditions.
Materials and Methods: In this survey 115 Lactobacillus spp. from 58 fecal samples of three different groups were evaluated. Comparison of the presence of bacteriocin genes in different groups were assayed by purified samples and PCR method, followed by statistical analysis to identify the effect of inflammation in the proportion of Lactobacillus spp. and presence of their bacteriocin genomes.
Results: Of 115 Lactobacillus spp. 60% of samples had positive bacteriocin-encoding genes which included: gassericin-A 29.56%, acidocin 15.65%, plantaricin-NC8 18.26%, plantaricin-S 13.04%, lactacin-F 9.5%, sakacin-P 6.08% and gassericin-T 6.08%. Results indicated that the percentage of positive bacteriocin genes were much more in healthy volunteer and IBD-recovered in comparison to IBD-patients which showed the effect of inflammation in the presence of bacteriocin genes.
Conclusion: The results obtained in this study demonstrated that the presence of bacteriocin genes can be related to health and disease states and inflammatory disease affected the prevalence of bacteriocin-encoding genes. This approach can help to identify bacterial functions that can be targeted in future concepts of IBD therapy.
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9. Liu G, Wang Y, Li X, Hao X, Xu D, Zhou Y, et al.. Genetic and biochemical evidence that Enterococcus faecalis Gr17 produces a novel and sec-dependent bacteriocin, enterocin Gr17. Front Microbiol 2019; 10: 1806.
10. Collins FWJ, O’Connor PM, O’Sullivan O, Gómez-Sala B, Rea MC, Hill C, et al. Bacteriocin gene-trait matching across the complete Lactobacillus pan-genome. Sci Rep 2017; 7: 3481.
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12. Saniabadi AR, Tanaka T, Ohmori T, Sawada K, Yamamoto T, Hanai H. Treating inflammatory bowel disease by adsorptive leucocytapheresis: a desire to treat without drugs. World J Gastroenterol 2014; 20: 9699-9715.
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15. Pereira DI, Gibson GR. Cholesterol assimilation by lactic acid bacteria and bifidobacteria isolated from the human gut. Appl Environ Microbiol 2002; 68: 4689-4693.
16. Başyiğit G, Kuleaşan H, Karahan AG. Viability of human-derived probiotic lactobacilli in ice cream produced with sucrose and aspartame. J Ind Microbiol Biotechnol 2006; 33: 796-800.
17. Barbosa MS, Todorov SD, Belguesmia Y, Choiset Y, Rabesona H, Ivanova IV, et al. Purification and characterization of the bacteriocin produced by Lactobacillus sakei MBSa1 isolated from Brazilian salami. J Appl Microbiol 2014; 116: 1195-1208.
18. Stoyancheva G, Marzotto M, Dellaglio F, Torriani S. Bacteriocin production and gene sequencing analysis from vaginal Lactobacillus strains. Arch Microbiol 2014; 196: 645-653.
19. Tai HF, Foo HL, Rahim RA, Loh TC, Abdullah MP, Yoshinobu K. Molecular characterisation of new organisation of plnEF and plw loci of bacteriocin genes harbour concomitantly in Lactobacillus plantarum I-UL4. Microb Cell Fact 2015; 14: 89.
20. Maldonado A, Ruiz-Barba JL, Jiménez-Díaz R. Purification and genetic characterization of plantaricin NC8, a novel coculture-inducible two-peptide bacteriocin from Lactobacillus plantarum NC8. Appl Environ Microbiol 2003; 69: 383-389.
21. Macwana SJ, Muriana PM. A ‘bacteriocin PCR array’for identification of bacteriocin-related structural genes in lactic acid bacteria. J Microbiol Methods 2012; 88: 197-204.
22. Kappelman MD, Bousvaros A, Hyams J, Markowitz J, Pfefferkorn M, Kugathasan S, et al. Intercenter variation in initial management of children with Crohn's disease. Inflamm Bowel Dis 2007; 13: 890-895.
23. Frank DN, Amand ALS, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 2007; 104: 13780-13785.
24. Ewaschuk JB, Dieleman LA. Probiotics and prebiotics in chronic inflammatory bowel diseases. World J
Gastroenterol 2006; 12: 5941-5950.
25. Ng SC, Hart AL, Kamm MA, Stagg AJ, Knight SC. Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis 2009; 15: 300-310.
26. Durchschein F, Petritsch W, Hammer HF. Diet therapy for inflammatory bowel diseases: The established and the new. World J Gastroenterol 2016; 22: 2179-2194.
27. Messaoudi S, Manai M, Kergourlay G, Prévost H, Connil N, Chobert JM, et al. Lactobacillus salivarius: bacteriocin and probiotic activity. Food Microbiol 2013; 36: 296-304.
28. Majhenič AC, Venema K, Allison GE, Matijašić BB, Rogelj I, Klaenhammer TR. DNA analysis of the genes encoding acidocin LF221 A and acidocin LF221 B, two bacteriocins produced by Lactobacillus gasseri LF221. Appl Microbiol Biotechnol 2004; 63: 705-714.
29. Bibalan MH, Eshaghi M, Rohani M, Pourshafie MR, Talebi M. Determination of bacteriocin genes and antibacterial activity of Lactobacillus strains isolated from fecal of healthy individuals. Int J Mol Cell Med 2017; 6: 50-55.
30. Turroni F, Ventura M, Buttó LF, Duranti S, O’Toole PW, Motherway MO, et al. Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell Mol Life Sci 2014; 71: 183-203.
31. Yin X, Heeney D, Srisengfa Y, Golomb B, Griffey S, Marco M. Bacteriocin biosynthesis contributes to the anti-inflammatory capacities of probiotic Lactobacillus plantarum. Benef Microbes 2018; 9: 333-344.
2. Zhang Y, Zhao X, Zhu Y, Ma J, Ma H, Zhang H. Probiotic mixture protects dextran sulfate sodium-induced colitis by altering tight junction protein expressions and increasing tregs. Mediators Inflamm 2018; 2018: 9416391.
3. Sairenji T, Collins KL, Evans DV. An update on inflammatory bowel disease. Prim Care 2017; 44: 673-692.
4. Kim H, Jung BJ, Jung JH, Kim JY, Chung SK, Chung DK. Lactobacillus plantarum lipoteichoic acid alleviates TNF-α-induced inflammation in the HT-29 intestinal epithelial cell line. Mol Cells 2012; 33: 479-486.
5. Le B, Yang SH. Efficacy of Lactobacillus plantarum in prevention of inflammatory bowel disease. Toxicol Rep 2018; 5: 314-317.
6. Vila AV, Imhann F, Collij V, Jankipersadsing SA, Gurry T, Mujagic Z, et al. Gut microbiota composition and functional changes in inflammatory bowel disease and irritable bowel syndrome. Sci Transl Med 2018; 10(472): eaap8914.
7. Loh G, Blaut M. Role of commensal gut bacteria in inflammatory bowel diseases. Gut Microbes 2012; 3: 544-555.
8. Kasuga G, Tanaka M, Harada Y, Nagashima H, Yamato T, Wakimoto A, et al. Homologous expression and characterization of gassericin T and gassericin S, a novel class IIb bacteriocin produced by Lactobacillus gasseri LA327. Appl Environ Microbiol 2019; 85(6): e02815-18.
9. Liu G, Wang Y, Li X, Hao X, Xu D, Zhou Y, et al.. Genetic and biochemical evidence that Enterococcus faecalis Gr17 produces a novel and sec-dependent bacteriocin, enterocin Gr17. Front Microbiol 2019; 10: 1806.
10. Collins FWJ, O’Connor PM, O’Sullivan O, Gómez-Sala B, Rea MC, Hill C, et al. Bacteriocin gene-trait matching across the complete Lactobacillus pan-genome. Sci Rep 2017; 7: 3481.
11. Ahmad V, Jamal QMS, Siddiqui MU, Shukla AK, Alzohairy MA, Al Karaawi MA, et al. Methods of screening-purification and antimicrobial potentialities of bacteriocin in health care. Curr Drug Metab 2017; 18: 814-830.
12. Saniabadi AR, Tanaka T, Ohmori T, Sawada K, Yamamoto T, Hanai H. Treating inflammatory bowel disease by adsorptive leucocytapheresis: a desire to treat without drugs. World J Gastroenterol 2014; 20: 9699-9715.
13. Kelsey JL, Whittemore AS, Evans AS, Thompson WD (1996). Methods in observational epidemiology. 2nd ed. Oxford University Press. New York.
14. Fleiss JL, Levin B, Paik MC (2013). Statistical methods for rates and proportions. 3rd ed. John Wiley & Sons. New York. USA.
15. Pereira DI, Gibson GR. Cholesterol assimilation by lactic acid bacteria and bifidobacteria isolated from the human gut. Appl Environ Microbiol 2002; 68: 4689-4693.
16. Başyiğit G, Kuleaşan H, Karahan AG. Viability of human-derived probiotic lactobacilli in ice cream produced with sucrose and aspartame. J Ind Microbiol Biotechnol 2006; 33: 796-800.
17. Barbosa MS, Todorov SD, Belguesmia Y, Choiset Y, Rabesona H, Ivanova IV, et al. Purification and characterization of the bacteriocin produced by Lactobacillus sakei MBSa1 isolated from Brazilian salami. J Appl Microbiol 2014; 116: 1195-1208.
18. Stoyancheva G, Marzotto M, Dellaglio F, Torriani S. Bacteriocin production and gene sequencing analysis from vaginal Lactobacillus strains. Arch Microbiol 2014; 196: 645-653.
19. Tai HF, Foo HL, Rahim RA, Loh TC, Abdullah MP, Yoshinobu K. Molecular characterisation of new organisation of plnEF and plw loci of bacteriocin genes harbour concomitantly in Lactobacillus plantarum I-UL4. Microb Cell Fact 2015; 14: 89.
20. Maldonado A, Ruiz-Barba JL, Jiménez-Díaz R. Purification and genetic characterization of plantaricin NC8, a novel coculture-inducible two-peptide bacteriocin from Lactobacillus plantarum NC8. Appl Environ Microbiol 2003; 69: 383-389.
21. Macwana SJ, Muriana PM. A ‘bacteriocin PCR array’for identification of bacteriocin-related structural genes in lactic acid bacteria. J Microbiol Methods 2012; 88: 197-204.
22. Kappelman MD, Bousvaros A, Hyams J, Markowitz J, Pfefferkorn M, Kugathasan S, et al. Intercenter variation in initial management of children with Crohn's disease. Inflamm Bowel Dis 2007; 13: 890-895.
23. Frank DN, Amand ALS, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 2007; 104: 13780-13785.
24. Ewaschuk JB, Dieleman LA. Probiotics and prebiotics in chronic inflammatory bowel diseases. World J
Gastroenterol 2006; 12: 5941-5950.
25. Ng SC, Hart AL, Kamm MA, Stagg AJ, Knight SC. Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis 2009; 15: 300-310.
26. Durchschein F, Petritsch W, Hammer HF. Diet therapy for inflammatory bowel diseases: The established and the new. World J Gastroenterol 2016; 22: 2179-2194.
27. Messaoudi S, Manai M, Kergourlay G, Prévost H, Connil N, Chobert JM, et al. Lactobacillus salivarius: bacteriocin and probiotic activity. Food Microbiol 2013; 36: 296-304.
28. Majhenič AC, Venema K, Allison GE, Matijašić BB, Rogelj I, Klaenhammer TR. DNA analysis of the genes encoding acidocin LF221 A and acidocin LF221 B, two bacteriocins produced by Lactobacillus gasseri LF221. Appl Microbiol Biotechnol 2004; 63: 705-714.
29. Bibalan MH, Eshaghi M, Rohani M, Pourshafie MR, Talebi M. Determination of bacteriocin genes and antibacterial activity of Lactobacillus strains isolated from fecal of healthy individuals. Int J Mol Cell Med 2017; 6: 50-55.
30. Turroni F, Ventura M, Buttó LF, Duranti S, O’Toole PW, Motherway MO, et al. Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell Mol Life Sci 2014; 71: 183-203.
31. Yin X, Heeney D, Srisengfa Y, Golomb B, Griffey S, Marco M. Bacteriocin biosynthesis contributes to the anti-inflammatory capacities of probiotic Lactobacillus plantarum. Benef Microbes 2018; 9: 333-344.
| Files | ||
| Issue | Vol 14 No 2 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i2.9191 | |
| Keywords | ||
| Lactobacillus; Antimicrobial peptides; Dysbiosis; Bacteriocins; Inflammatory bowel disease | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Miri ST, Sotoodehnejadnematalahi F, Amiri MM, Pourshafie MR, Rohani M. Comparison of the prevalence of bacteriocin encoding genes in Lactobacillus spp. isolated from fecal samples of healthy volunteers, IBD-patient and IBD-recovered. Iran J Microbiol. 2022;14(2):219-226.
