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:: Volume 9, Issue 1 (Jan-Mar 2022) ::
Nutr Food Sci Res 2022, 9(1): 31-40 Back to browse issues page
Lactic Acid Bacteria Antagonism of Acid-tolerant and Antibiotic-resistant Non-staphylococcal Pathogenic Species Isolated from a Fermented Cereal Beverage using Baird-Parker Agar
Stellah Byakika , Ivan Muzira Mukisa , Charles Muyanja
Department of Food Technology and Nutrition, Makerere University, Kampala, Uganda , ivanmukisa@gmail.com
Abstract:   (5698 Views)
Background and Objectives: Fermented foods may contain acid-tolerant and antibiotic-resistant pathogenic microorganisms. Pathogens can be antagonized by lactic acid bacteria, resulting in improved microbiological safety. This study assessed the antagonistic effects of selected lactic acid bacteria against pathogenic bacteria isolated from a cereal fermented food.
Materials and Methods: Eight presumptive staphylococci isolated from a commercially produced cereal fermented beverage on Baird-Parker agar supplemented with tellurite were identified using 16S rRNA sequencing. Acid resistance of the isolates was assessed using acidified media (brain heart infusion broth of pH 3.6 and 1.5% acidity) for 48 h followed by taking plate counts. Antibiotic resistance (19 antibiotics) was assessed using the disk diffusion assay. A spot-on-the-lawn method was used to assess antagonistic effects of Lactobacillus plantarum MNC 21, Lactococcus lactis MNC 24, Weissella confusa MNC 20 and Lactobacillus rhamnosus yoba 2012 against Lysinibacillus macroides, Bacillus subtilis, Enterococcus faecalis and Escherichia coli.
Results: Presumptive staphylococci were identified as Lysinibacillus macroides (n = 1), Bacillus subtilis (n = 2), Enterococcus faecalis (n = 4) and Escherichia coli (n = 1). These isolates were acid-tolerant (from 6.3 ±0.9 log cfu/mL at 0 h to 3.6 ±0.9 log cfu/mL at 48 h), antibiotic-resistant (multiple antibiotic resistance index of 0.1–0.5) and their growth was inhibited by the lactic acid bacteria (inhibition zone diameters of 14–24 mm).
Conclusions: The lactic acid bacteria cultures of MNC 20, MNC 21, MNC 24 and Lactobacillus rhamnosus yoba 2012 can be used in various food fermentations to inhibit growth of bacterial pathogens; thus, improving product safety.
Keywords: Antagonism, acid-tolerant, antibiotic-resistant, lactic acid bacteria, Baird-Parker Agar
Full-Text [PDF 704 kb]   (360 Downloads)    
Article type: Research | Subject: Food Science
Received: 2020/11/2 | Accepted: 2021/08/14 | Published: 2022/01/22
1. Steinkraus KH. Nutritional significance of fermented foods. Food Res Int 1994;27(3):259-67. [DOI:10.1016/0963-9969(94)90094-9]
2. Steinkraus KH. Handbook of indigenous fermented foods. rev. and expanded. Food Science and Technology (USA) no 73. 1996.
3. Rajaram G, Manivasagan P, Thilagavathi B, Saravanakumar A. Purification and characterization of a bacteriocin produced by Lactobacillus lactis isolated from marine environment. Adv J Food Sci Tech 2010;2(2):138-44.
4. Muyanja C, Narvhus J, Treimo J, Langsrud T. Isolation, characterisation and identification of lactic acid bacteria from bushera: a Ugandan traditional fermented beverage. Int J Food Microbiol 2003;80(3):201-10. [DOI:10.1016/S0168-1605(02)00148-4]
5. Mukisa IM, Porcellato D, Byaruhanga YB, Muyanja C, Rudi K, Langsrud T, et al. The dominant microbial community associated with fermentation of Obushera (sorghum and millet beverages) determined by culture-dependent and culture-independent methods. Int J Food Microbiol 2012;160(1):1-10. [DOI:10.1016/j.ijfoodmicro.2012.09.023]
6. Byakika S, Mukisa IM, Mugabi R, Muyanja C. Antimicrobial activity of lactic acid bacteria starters against acid tolerant, antibiotic resistant and potentially virulent E. coli Isolated from a fermented sorghum-millet beverage. Int J Microbiol 2019;2019. [DOI:10.1155/2019/2013539]
7. Byakika S, Mukisa IM, Byaruhanga YB, Male D, Muyanja C. Influence of food safety knowledge, attitudes and practices of processors on microbiological quality of commercially produced traditional fermented cereal beverages, a case of Obushera in Kampala. Food Control. 2019;100:212-9. [DOI:10.1016/j.foodcont.2019.01.024]
8. Izah SC, Kigigha LT, Okowa IP. Microbial quality assessment of fermented maize Ogi (a cereal product) and options for overcoming constraints in production. Biotechnol Res 2016;2(2):81-93.
9. Oyelana O, Coker A. Microbial contamination at different stages of production of Ogi in Mowe: A rural community, southwest, Nigeria. Bacteriol J 2012;2(1):1-11. [DOI:10.3923/bj.2012.1.11]
10. Byakika S, Mukisa IM, Byaruhanga YB, Muyanja C. Probiotic potential of lactic acid starter cultures isolated from a traditional fermented sorghum-millet beverage. Int J Microbiol 2020;2020. [DOI:10.1155/2020/7825943]
11. Byakika S, Mukisa IM, Wacoo AP, Kort R, Byaruhanga YB, Muyanja C. Potential application of lactic acid starters in the reduction of aflatoxin contamination in fermented sorghum-millet beverages. Int J Food Contam 2019;6(1):4. [DOI:10.1186/s40550-019-0074-9]
12. Mukisa IM. Sensory characteristics, microbial diversity and starter culture development for Obushera, a traditional cereal fermented beverage from Uganda 2012. PhD thesis. Aas, Norway: Norwegian University of Life Sciences.
13. Mukisa IM, Ntaate D, Byakika S. Application of starter cultures in the production of Enturire-a traditional sorghum‐based alcoholic beverage. Food Sci Nutr 2017;5(3):609-16. [DOI:10.1002/fsn3.438]
14. (CLSI) CaLSI. Performance standards for antimicrobial susceptibility testing; Twenty-Third Information Supplement 2013 [Available from: http://www.facm.ucl.ac.be/intranet/CLSI/CLSI-M100S23-susceptibility-testing-2013-no-protection.pdf.
15. Krumperman PH. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Applied Environ Microbiol 1983;46(1):165-70. [DOI:10.1128/aem.46.1.165-170.1983]
16. Byaruhanga Y, Bester B, Watson T. Growth and survival of Bacillus cereus in mageu, a sour maize beverage. World J Microbiol Biotechnol 1999;15(3):329-33. [DOI:10.1023/A:1008967117381]
17. Addinsoft. XLSTAT. 2010.5.02 ed. France2010.
18. Mathara JM, Schillinger U, Guigas C, Franz C, Kutima PM, Mbugua SK, et al. Functional characteristics of Lactobacillus spp. from traditional Maasai fermented milk products in Kenya. Int J Food Microbiol 2008;126(1-2):57-64. [DOI:10.1016/j.ijfoodmicro.2008.04.027]
19. Oxoid. Baird-Parker agar base 2020 [Available from: http://www.oxoid.com/uk/blue/prod_detail/prod_detail.asp?pr=CM0275&org=153&c=uk.
20. Neogen. Technical Specification Sheet - Baird-Parker Agar (NCM0024). 2019.
21. Golob M, Pate M, Kušar D, Dermota U, Avberšek J, Papić B, et al. Antimicrobial resistance and virulence genes in Enterococcus faecium and Enterococcus faecalis from humans and retail red meat. BioMed Res Int 2019;2019. [DOI:10.1155/2019/2815279]
22. Wenzler E, Kamboj K, Balada-Llasat J-M. Severe sepsis secondary to persistent Lysinibacillus sphaericus, Lysinibacillus fusiformis and Paenibacillus amylolyticus bacteremia. Int J Infect Dis 2015;35:93-5. [DOI:10.1016/j.ijid.2015.04.016]
23. Momtaz H, Karimian A, Madani M, Dehkordi FS, Ranjbar R, Sarshar M, et al. Uropathogenic Escherichia coli in Iran: serogroup distributions, virulence factors and antimicrobial resistance properties. Ann Clin Microbiol Antimicrob 2013;12(1):8. [DOI:10.1186/1476-0711-12-8]
24. Logan N. Bacillus and relatives in foodborne illness. J Appl Microbiol 2012;112(3):417-29. [DOI:10.1111/j.1365-2672.2011.05204.x]
25. Griffiths M, Schraft H. Bacillus cereus food poisoning. Foodborne diseases: Elsevier; 2017. p. 395-405. [DOI:10.1016/B978-0-12-385007-2.00020-6]
26. Gu H-J, Sun Q-L, Luo J-C, Zhang J, Sun L. A first study of the virulence potential of a Bacillus subtilis isolate from deep-sea hydrothermal vent. Front Cell Infect Microbiol 2019;9:183. [DOI:10.3389/fcimb.2019.00183]
27. Brett KN, Hornitzky MA, Bettelheim KA, Walker MJ, Djordjevic SP. Bovine non-O157 Shiga toxin 2-containing Escherichia coli isolates commonly possess stx2-EDL933 and/or stx2vhb subtypes. J Clin Microbiol 2003;41(6):2716-22. [DOI:10.1128/JCM.41.6.2716-2722.2003]
28. Ranjbar R, Dehkordi FS, Shahreza MHS, Rahimi E. Prevalence, identification of virulence factors, O-serogroups and antibiotic resistance properties of Shiga-toxin producing Escherichia coli strains isolated from raw milk and traditional dairy products. Antimicrob Resist Infect Control 2018;7(1):53. [DOI:10.1186/s13756-018-0345-x]
29. Tosun H, Seckin AK, Gönül ŞA. Acid adaptation effect on survival of Escherichia coli O157: H7 in fermented milk products. Turk J Vet Anim Sci 2007;31(1):61-6.
30. Inatsu Y, Bari M, Kawasaki S, Isshiki K. Survival of Escherichia coli O157: H7, Salmonella enteritidis, Staphylococcus aureus and Listeria monocytogenes in Kimchi. J Food Protect 2004;67(7):1497-500. [DOI:10.4315/0362-028X-67.7.1497]
31. Svanberg U, Sjögren E, Lorri W, Svennerholm A-M, Kaijser B. Inhibited growth of common enteropathogenic bacteria in lactic-fermented cereal gruels. World J Microbiol Biotechnol 1992;8(6):601-6. [DOI:10.1007/BF01238797]
32. Simango C, Rukure G. Survival of Campylobacter jejuni and pathogenic Escherichia coli in mahewu, a fermented cereal gruel. Trans R Soc Trop Med Hyg 1991;85(3):399-400. [DOI:10.1016/0035-9203(91)90305-I]
33. Cotter PD, Hill C. Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol Mol Biol Rev 2003;67(3):429-53. [DOI:10.1128/MMBR.67.3.429-453.2003]
34. Fillingame RH, Divall S, editors. Proton ATPases in bacteria: comparison to Escherichia coli F~ 1F~ 0 as the prototype. Novartis Foundation Symposium; 1999: Wiley Online Library.
35. Quivey Jr RG, Faustoferri R, Monahan K, Marquis R. Shifts in membrane fatty acid profiles associated with acid adaptation of Streptococcus mutans. FEMS Microbiol Lett 2000;189(1):89-92. [DOI:10.1111/j.1574-6968.2000.tb09211.x]
36. Diaz-Torres ML, Russell RR. HtrA protease and processing of extracellular proteins of Streptococcus mutans. FEMS Microbiol Lett 2001;204(1):23-8. [DOI:10.1111/j.1574-6968.2001.tb10856.x]
37. Haberbeck LU, Wang X, Michiels C, Devlieghere F, Uyttendaele M, Geeraerd AH. Cross-protection between controlled acid-adaptation and thermal inactivation for 48 Escherichia coli strains. Int J Food Microbiol 2017;241:206-14. [DOI:10.1016/j.ijfoodmicro.2016.10.006]
38. EFSA, European Food Safety Authority. Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J 2012;10(6):2740. [DOI:10.2903/j.efsa.2012.2740]
39. Galimand M, Schmitt E, Panvert M, Desmolaize B, Douthwaite S, Mechulam Y, et al. Intrinsic resistance to aminoglycosides in Enterococcus faecium is conferred by the 16S rRNA m5C1404-specific methyltransferase EfmM. RNA. 2011;17(2):251-62. [DOI:10.1261/rna.2233511]
40. Arias CA, Contreras GA, Murray BE. Management of multidrug-resistant enterococcal infections. Clin Microbiol Infect 2010;16(6):555-62. [DOI:10.1111/j.1469-0691.2010.03214.x]
41. Eliopoulos GM, Gold H. Vancomycin-resistant enterococci: mechanisms and clinical observations. Clin Infect Dis 2001;33(2):210-9. [DOI:10.1086/321815]
42. Giraffa G. Enterococci from foods. FEMS Microbiol Rev 2002;26(2):163-71. [DOI:10.1111/j.1574-6976.2002.tb00608.x]
43. Donskey CJ, Chowdhry TK, Hecker MT, Hoyen CK, Hanrahan JA, Hujer AM, et al. Effect of antibiotic therapy on the density of vancomycin-resistant enterococci in the stool of colonized patients. N Eng J Med 2000;343(26):1925-32. [DOI:10.1056/NEJM200012283432604]
44. Nation RL, Li J. Colistin in the 21st century. Curr Opin Infect Dis 2009;22(6):535. [DOI:10.1097/QCO.0b013e328332e672]
45. Lopes MdFS, Ribeiro T, Abrantes M, Marques JJF, Tenreiro R, Crespo MTB. Antimicrobial resistance profiles of dairy and clinical isolates and type strains of enterococci. Int J Food Microbiol 2005;103(2):191-8. [DOI:10.1016/j.ijfoodmicro.2004.12.025]
46. Luo Y, Helmann JD. Analysis of the role of Bacillus subtilis σM in β‐lactam resistance reveals an essential role for c‐di‐AMP in peptidoglycan homeostasis. Mol Microbiol 2012;83(3):623-39. [DOI:10.1111/j.1365-2958.2011.07953.x]
47. Bozdogan B, Galopin S, Leclercq R. Characterization of a new erm-related macrolide resistance gene present in probiotic strains of Bacillus clausii. Appl Environ Microbiol 2004;70(1):280-4. [DOI:10.1128/AEM.70.1.280-284.2004]
48. Kim H-S, Choi E-C, Kim B-K. A macrolide-lincosamide-streptogramin B resistance determinant from Bacillus anthracis 590: cloning and expression of ermJ. Microbiol 1993;139(3):601-7. [DOI:10.1099/00221287-139-3-601]
49. Gryczan T, Israeli-Reches M, Del Bue M, Dubnau D. DNA sequence and regulation of ermD, a macrolide-lincosamide-streptogramin B resistance element from Bacillus licheniformis. Mol Gen Genet 1984;194(3):349-56. [DOI:10.1007/BF00425543]
50. Adimpong DB, Sørensen KI, Thorsen L, Stuer-Lauridsen B, Abdelgadir WS, Nielsen DS, et al. Antimicrobial susceptibility of Bacillus strains isolated from primary starters for African traditional bread production and characterization of the bacitracin operon and bacitracin biosynthesis. Appl Environ Microbiol 2012;78(22):7903-14. [DOI:10.1128/AEM.00730-12]
51. Barbosa TM, Serra CR, La Ragione RM, Woodward MJ, Henriques AO. Screening for Bacillus isolates in the broiler gastrointestinal tract. Appl Environ Microbiol 2005;71(2):968-78. [DOI:10.1128/AEM.71.2.968-978.2005]
52. Sun H, Bjerketorp J, Levenfors JJ, Schnürer A. Isolation of antibiotic-resistant bacteria in biogas digestate and their susceptibility to antibiotics. Environ Pollut 2020:115265. [DOI:10.1016/j.envpol.2020.115265]
53. Nicholson WL, Maughan H. The spectrum of spontaneous rifampin resistance mutations in the rpoB gene of Bacillus subtilis 168 spores differs from that of vegetative cells and resembles that of Mycobacterium tuberculosis. J Bacteriol 2002;184(17):4936-40. [DOI:10.1128/JB.184.17.4936-4940.2002]
54. Bisicchia P, Bui NK, Aldridge C, Vollmer W, Devine KM. Acquisition of VanB‐type vancomycin resistance by Bacillus subtilis: the impact on gene expression, cell wall composition and morphology. Mol Microbiol 2011;81(1):157-78. [DOI:10.1111/j.1365-2958.2011.07684.x]
55. Fiedler G, Schneider C, Igbinosa EO, Kabisch J, Brinks E, Becker B, et al. Antibiotics resistance and toxin profiles of Bacillus cereus-group isolates from fresh vegetables from German retail markets. BMC Microbiol 2019;19(1):250. [DOI:10.1186/s12866-019-1632-2]
56. Eliopoulos GM, Huovinen P. Resistance to trimethoprim-sulfamethoxazole. Clin Infect Dis 2001;32(11):1608-14. [DOI:10.1086/320532]
57. Dhand A, Snydman DR. Mechanism of resistance in metronidazole. Antimicrobial drug resistance: Springer; 2009. p. 223-7. [DOI:10.1007/978-1-59745-180-2_19]
58. Johura F-T, Tasnim J, Barman I, Biswas SR, Jubyda FT, Sultana M, et al. Colistin-resistant Escherichia coli carrying mcr-1 in food, water, hand rinse and healthy human gut in Bangladesh. Gut Pathog 2020;12(1):5. [DOI:10.1186/s13099-020-0345-2]
59. Tamae C, Liu A, Kim K, Sitz D, Hong J, Becket E, et al. Determination of antibiotic hypersensitivity among 4,000 single-gene-knockout mutants of Escherichia coli. J Bacteriol 2008;190(17):5981-8. [DOI:10.1128/JB.01982-07]
60. Jackson D, Salem A, Coombs G. The in-vitro activity of metronidazole against strains of Escherichia coli with impaired DNA repair systems. Journal of Antimicrob Chemother 1984;13(3):227-36. [DOI:10.1093/jac/13.3.227]
61. Paul S, Bezbaruah RL, Roy MK, Ghosh AC. Multiple antibiotic resistance (MAR) index and its reversion in Pseudomonas aeruginosa. Lett Appl Microbiol 1997;24(3):169-71. [DOI:10.1046/j.1472-765X.1997.00364.x]
62. Chorianopoulos N, Giaouris E, Grigoraki I, Skandamis P, Nychas G-J. Effect of acid tolerance response (ATR) on attachment of Listeria monocytogenes Scott A to stainless steel under extended exposure to acid or/and salt stress and resistance of sessile cells to subsequent strong acid challenge. Int J Food Microbiol 2011;145(2-3):400-6. [DOI:10.1016/j.ijfoodmicro.2011.01.001]
63. Jin J, Zhang B, Guo H, Cui J, Jiang L, Song S, et al. Mechanism analysis of acid tolerance response of Bifidobacterium longum subsp. longum BBMN 68 by gene expression profile using RNA-sequencing. PLoS One 2012;7(12):e50777. [DOI:10.1371/journal.pone.0050777]
64. Neal-McKinney JM, Lu X, Duong T, Larson CL, Call DR, Shah DH, et al. Production of organic acids by probiotic lactobacilli can be used to decrease pathogen load in poultry. PloS One 2012;7(9):e43928. [DOI:10.1371/journal.pone.0043928]
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Byakika S, Mukisa I M, Muyanja C. Lactic Acid Bacteria Antagonism of Acid-tolerant and Antibiotic-resistant Non-staphylococcal Pathogenic Species Isolated from a Fermented Cereal Beverage using Baird-Parker Agar. Nutr Food Sci Res 2022; 9 (1) :31-40
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