In vitro anti-biofilm activity of bacteriocin from a marine Bacillus sp. strain Sh10 against Proteus mirabilis
,
Abstract
Background and Objectives: Biofilm formed by Proteus mirabilis strains is one of the most important medical problems especially in the case of device-related urinary tract infections. This study was conducted to evaluate the bacteriocin produced by a marine isolate of Bacillus sp. Sh10, for it's in vitro inhibitory activity against pre-formed biofilm and in interference with the biofilm-forming of two biofilm-producing bacteria (P. mirabilis UCa4 and P. mirabilis UCe1).
Materials and Methods: Sensitivity of two biofilm-producing bacteria (P. mirabilis UCa4 and P. mirabilis UCe1) to bacteriocin, was investigated in planktonic and biofilm states by cell viability and crystal violet assay, respectively. Scanning electron microscopy (SEM) was also performed to determine the effect of bacteriocin on the morphology of the cells associated with biofilm.
Results: It was found that bacteriocin possessed bactericidal activity to biofilm-forming isolates in the planktonic state. However, bacteriocin interferes with the formation of biofilms and disrupts established biofilms. Bacteriocin reduced biofilm formation in the isolates of P. mirabilis UCa4 and P. mirabilis UCe1 with SMIC50 of 32 and 128 μg/mL, desirable SMIC50 of bacteriocin for biofilm disruption were 128 and 256 μg/mL, respectively. The SEM results indicated that bacteriocin affected the cell morphology of biofilm-associated cells.
Conclusion: The present findings indicated that bacteriocin from Bacillus sp. Sh10 has bactericidal properties against biofilm-forming isolates of P. mirabilis UCa4 and P. mirabilis UCe1 and has the ability to inhibit the formation of biofilm and disrupt established biofilm.
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2. Jacobsen SM, Shirtliff ME. Proteus mirabilis biofilms and catheter-associated urinary tract infections. Virulence 2011; 2:460-465
3. Warren JW (1996). Clinical presentations and epidemiology of urinary tract infections. In: Urinary tract infections: molecular pathogenesis and clinical management. Ed, Mobley HL, Warren JW. Washington DC: ASM Press, pp. 245-269.
4. Jacobsen SM, Stickler DJ, Mobley HLT, Shirtliff ME. Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin Microbiol Rev 2008; 21:26-59.
5. Donlan R, Costerton J. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002; 15: 167-193
6. Eyoh AB, Toukam M, Atashili J, Fokunang C, Gonsu H, Lyonga EE, et al. Relationship between multiple drug resistance and biofilm formation in Staphylococcus aureus isolated from medical and nonmedical personnel in Yaounde, Cameroon. Pan Afr Med J 2014; 17: 186.
7. Rao RS, Karthika RU, Singh SP, Shashikala P, Kanungo R, Jayachandran S, et al. Correlation between biofilm production and multiple drug resistance in imipenem resistant clinical isolates of Acinetobacter baumannii. Indian J Med Microbiol 2008; 26: 333-337.
8. Kanayama A, Iyoda T, Matsuzaki K, Saika T, Ikeda F, Ishii Y, et al. Rapidly spreading CTX-M-type beta-lactamase-producing Proteus mirabilis in Japan. Int J Antimicrob Agents 2010; 36: 340-342.
9. Ho PL, Ho AY, Chow KH, Wong RC, Duan RS, Ho WL, et al. Occurrence and molecular analysis of extended-spectrum {beta}-lactamase-producing Proteus mirabilis in Hong Kong, 1999-2002. J
ntimicrob Chemother 2005; 55: 840-845
10. Saito R, Okugawa S, Kumita W, Sato K, Chida T, Okamura N, et al. Clinical epidemiology of ciprofloxacin-resistant Proteus mirabilis isolated from urine samples of hospitalised patients. Clin Microbiol Infect 2007; 13: 1204-1206
11. Hernandez JR, Martínez-Martínez L, Pascual A, Suárez AI, Perea EJ. Trends in the susceptibilities of Proteus mirabilis isolates to quinolones. J Antimicrob Chemother 2000; 45: 407-408.
12. Okuda K, Zendo T, Sugimoto S, Iwase T, Tajima A, Yamada S, et al. Effects of bacteriocins on methicillin-resistant Staphylococcus aureus biofilm. Antimicrob Agents Chemother 2013; 57: 5572-5579.
13. Jack RW, Tagg JR, Ray B. Bacteriocins of gram-positive bacteria. Microbiol Rev 1995; 59: 171-200.
14. Batoni G, Maisetta G, Brancatisano FL, Esin S, Campa M. Use of antimicrobial peptides against microbial biofilms: advantages and limits. Curr Med Chem 2011;18: 256-279.
15. Riley MA, Wertz JE. Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie 2002; 84: 357-364.
16. Shayesteh F, Ahmad A, Usup G. Bacteriocin production by a marine strain of Bacillus sp. Sh10: Isolation, screening and optimization of culture condition. Biotechnol 2014; 13: 273-281.
17. Shayesteh F, Ahmad A, Usup G. Partial characterization of an anti-Candida albicans bacteriocin produced by a marine strain of Bacillus sp., Sh10. Adv J Food Sci Technol 2015; 9: 664-671.
18. Ahmad A, Hamid R, Usup G. Activities of bacteriocin from Pseudomonas putida strain FStm2 against biofilm-forming bacteria isolated from urinary catheter. Mal J Microbiol 2014; 10: 7-14.
19. Djordjevic D, Wiedmann M, McLandsborough LA. Microtiter plate assayfor assessment of
Listeria monocytogenes biofilm formation. Appl Environ Microbiol 2002;68: 2950-2958.
20. Pridham TG, Gottlieb D. The utilization of carbon compounds by some actinomycetales as an aid for species determination. J Bacteriol 1948; 56: 107-114.
21. Rajaram G, Manivasagan P, Thilagavathi B, Saravanakumar A. Purification and characterization of a bacteriocin produced by Lactobacillus lactis isolated from marine environment. J Food Sci Technol 2010; 2: 138-144.
22. Seuk-Hyun K, Cheol A. Bacteriocin production by Lactococcus lactis KCA 2386 isolated from.
23. Clinical and Laboratory Institute (2003). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically. 6th ed. CLSI Document M7-A6: Wayne.
24. Hufnagel M, Koch S, Creti R, Balda SL, Huebner JA. Putative sugar binding transcriptional regulator in a novel gene locus in Enterococcus faecalis contributes to production of biofilm and prolonged bacteremia in mice. J Infect Dis 2004; 189: 420-430.
25. Olszewska MA, Kocot AM, Stanowicka A, Łaniewska-Trokenheim Ł. Biofilm formation by Pseudomonas aeruginosa and disinfectant susceptibility of planktonic and biofilm cells. Czech J Food Sci 2016; 34: 204-210.
26. Chylkova T, Cadena M, Ferreiro A, Pitesky M. Susceptibility of Salmonella biofilm and panktonic bacteria to common disinfectant agents used in poultry processing. J Food Prot 2017; 80: 1072-1079.
27. Mah TF, O’Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 2001;9: 34-39.
28. Brown MR, Allison DG, Gilbert P. Resistance of bacterial biofilms to antibiotics: a growth-rate related effect? J Antimicrob Chemother 1988; 22: 777-780.
29. Keren I, Shah D, Spoering A, Kaldalu N, Lewis K. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol 2004; 186: 8172-8180.
30. Overhage J, Campisano A, Bains M, Torfs EC, Rehm BH, Hancock RE. Human host defence peptide LL-37 prevents bacterial biofilm formation. Infect Immun 2008; 76: 4176-4182.
31. Park SC, Park Y, Hahm KS. The role of antimicrobial peptides in preventing multidrug-resistant bacterial infections and biofilm formation. Int J Mol Sci 2011; 12: 5971-5992.
32. Yeaman MR, Yount NY. Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 2003; 55: 27-55.
33. Chen X, Zhang M, Zhou C, Kallenbach NR, Ren D. Control of bacterial persister cells by Trp/Arg-containing antimicrobial peptides. Appl Environ Microbiol 2011; 77: 4878-4885.
34. Li L, Shi Y, Cheserek MJ, Su G, Le G. Antibacterial activity and dual mechanisms of peptide analogue derived from cell-penetrating peptide against Salmonella typhimurium and Streptococcus pyogenes. Appl Microbiol Biotechnol 2013; 97: 1711-1723.
2. Jacobsen SM, Shirtliff ME. Proteus mirabilis biofilms and catheter-associated urinary tract infections. Virulence 2011; 2:460-465
3. Warren JW (1996). Clinical presentations and epidemiology of urinary tract infections. In: Urinary tract infections: molecular pathogenesis and clinical management. Ed, Mobley HL, Warren JW. Washington DC: ASM Press, pp. 245-269.
4. Jacobsen SM, Stickler DJ, Mobley HLT, Shirtliff ME. Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin Microbiol Rev 2008; 21:26-59.
5. Donlan R, Costerton J. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002; 15: 167-193
6. Eyoh AB, Toukam M, Atashili J, Fokunang C, Gonsu H, Lyonga EE, et al. Relationship between multiple drug resistance and biofilm formation in Staphylococcus aureus isolated from medical and nonmedical personnel in Yaounde, Cameroon. Pan Afr Med J 2014; 17: 186.
7. Rao RS, Karthika RU, Singh SP, Shashikala P, Kanungo R, Jayachandran S, et al. Correlation between biofilm production and multiple drug resistance in imipenem resistant clinical isolates of Acinetobacter baumannii. Indian J Med Microbiol 2008; 26: 333-337.
8. Kanayama A, Iyoda T, Matsuzaki K, Saika T, Ikeda F, Ishii Y, et al. Rapidly spreading CTX-M-type beta-lactamase-producing Proteus mirabilis in Japan. Int J Antimicrob Agents 2010; 36: 340-342.
9. Ho PL, Ho AY, Chow KH, Wong RC, Duan RS, Ho WL, et al. Occurrence and molecular analysis of extended-spectrum {beta}-lactamase-producing Proteus mirabilis in Hong Kong, 1999-2002. J
ntimicrob Chemother 2005; 55: 840-845
10. Saito R, Okugawa S, Kumita W, Sato K, Chida T, Okamura N, et al. Clinical epidemiology of ciprofloxacin-resistant Proteus mirabilis isolated from urine samples of hospitalised patients. Clin Microbiol Infect 2007; 13: 1204-1206
11. Hernandez JR, Martínez-Martínez L, Pascual A, Suárez AI, Perea EJ. Trends in the susceptibilities of Proteus mirabilis isolates to quinolones. J Antimicrob Chemother 2000; 45: 407-408.
12. Okuda K, Zendo T, Sugimoto S, Iwase T, Tajima A, Yamada S, et al. Effects of bacteriocins on methicillin-resistant Staphylococcus aureus biofilm. Antimicrob Agents Chemother 2013; 57: 5572-5579.
13. Jack RW, Tagg JR, Ray B. Bacteriocins of gram-positive bacteria. Microbiol Rev 1995; 59: 171-200.
14. Batoni G, Maisetta G, Brancatisano FL, Esin S, Campa M. Use of antimicrobial peptides against microbial biofilms: advantages and limits. Curr Med Chem 2011;18: 256-279.
15. Riley MA, Wertz JE. Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie 2002; 84: 357-364.
16. Shayesteh F, Ahmad A, Usup G. Bacteriocin production by a marine strain of Bacillus sp. Sh10: Isolation, screening and optimization of culture condition. Biotechnol 2014; 13: 273-281.
17. Shayesteh F, Ahmad A, Usup G. Partial characterization of an anti-Candida albicans bacteriocin produced by a marine strain of Bacillus sp., Sh10. Adv J Food Sci Technol 2015; 9: 664-671.
18. Ahmad A, Hamid R, Usup G. Activities of bacteriocin from Pseudomonas putida strain FStm2 against biofilm-forming bacteria isolated from urinary catheter. Mal J Microbiol 2014; 10: 7-14.
19. Djordjevic D, Wiedmann M, McLandsborough LA. Microtiter plate assayfor assessment of
Listeria monocytogenes biofilm formation. Appl Environ Microbiol 2002;68: 2950-2958.
20. Pridham TG, Gottlieb D. The utilization of carbon compounds by some actinomycetales as an aid for species determination. J Bacteriol 1948; 56: 107-114.
21. Rajaram G, Manivasagan P, Thilagavathi B, Saravanakumar A. Purification and characterization of a bacteriocin produced by Lactobacillus lactis isolated from marine environment. J Food Sci Technol 2010; 2: 138-144.
22. Seuk-Hyun K, Cheol A. Bacteriocin production by Lactococcus lactis KCA 2386 isolated from.
23. Clinical and Laboratory Institute (2003). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically. 6th ed. CLSI Document M7-A6: Wayne.
24. Hufnagel M, Koch S, Creti R, Balda SL, Huebner JA. Putative sugar binding transcriptional regulator in a novel gene locus in Enterococcus faecalis contributes to production of biofilm and prolonged bacteremia in mice. J Infect Dis 2004; 189: 420-430.
25. Olszewska MA, Kocot AM, Stanowicka A, Łaniewska-Trokenheim Ł. Biofilm formation by Pseudomonas aeruginosa and disinfectant susceptibility of planktonic and biofilm cells. Czech J Food Sci 2016; 34: 204-210.
26. Chylkova T, Cadena M, Ferreiro A, Pitesky M. Susceptibility of Salmonella biofilm and panktonic bacteria to common disinfectant agents used in poultry processing. J Food Prot 2017; 80: 1072-1079.
27. Mah TF, O’Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 2001;9: 34-39.
28. Brown MR, Allison DG, Gilbert P. Resistance of bacterial biofilms to antibiotics: a growth-rate related effect? J Antimicrob Chemother 1988; 22: 777-780.
29. Keren I, Shah D, Spoering A, Kaldalu N, Lewis K. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol 2004; 186: 8172-8180.
30. Overhage J, Campisano A, Bains M, Torfs EC, Rehm BH, Hancock RE. Human host defence peptide LL-37 prevents bacterial biofilm formation. Infect Immun 2008; 76: 4176-4182.
31. Park SC, Park Y, Hahm KS. The role of antimicrobial peptides in preventing multidrug-resistant bacterial infections and biofilm formation. Int J Mol Sci 2011; 12: 5971-5992.
32. Yeaman MR, Yount NY. Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 2003; 55: 27-55.
33. Chen X, Zhang M, Zhou C, Kallenbach NR, Ren D. Control of bacterial persister cells by Trp/Arg-containing antimicrobial peptides. Appl Environ Microbiol 2011; 77: 4878-4885.
34. Li L, Shi Y, Cheserek MJ, Su G, Le G. Antibacterial activity and dual mechanisms of peptide analogue derived from cell-penetrating peptide against Salmonella typhimurium and Streptococcus pyogenes. Appl Microbiol Biotechnol 2013; 97: 1711-1723.
| Files | ||
| Issue | Vol 12 No 1 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i1.2518 | |
| Keywords | ||
| Marine bacteria Bacterioci Bacillus sp sp Proteus mirabili Anti-biofilm activity | ||
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How to Cite
1.
Shayesteh F, Ahmad A, Usup G. In vitro anti-biofilm activity of bacteriocin from a marine Bacillus sp. strain Sh10 against Proteus mirabilis. Iran J Microbiol. 2020;12(1):52-61.
