Lactic Acid Bacteria from Fermented Asparagus and Stinky Beans Inhibit Clinical Diarrheagenic Escherichia coli and Clinical Methicillin-Resistant Staphylococcus aureus
Article Sidebar
Main Article Content
Abstract
The probiotics exhibiting antagonistic activity against gastrointestinal pathogenic bacteria are essential for protecting the host from illnesses and regulating intestinal balance. In this study, we successfully isolated 7 lactic acid bacteria (LAB) from fermented asparagus and fermented stinky beans. They showed the sign of probiotic properties, especially 2 strains from fermented asparagus, PZ12 and PZ14, strongly tolerated to simulated gastric juice pH 3.0 supplemented with 0.3% pepsin. Additionally, these 2 LAB strains tolerated 0.5% bile salts for up to 3 hours. Antagonistic activity of 7 LAB strains against clinical Diarrheagenic Escherichia coli (DEC) and clinical MRSA in this study showed that all LAB strains were capable of inhibiting clinical DEC and clinical MRSA by providing an inhibition zone in the range between 22 and 39 mm. PZ12 and PZ14 also displayed relatively wide inhibition zones against these intestinal pathogens. Antimicrobial-resistant examination demonstrated that most LAB strains could be destroyed by most of the antimicrobial agents tested. LAB strains PZ12 and PZ14 were shown to be resistant to three antimicrobial agents. PZ12 could resist ciprofloxacin, fosfomycin, and streptomycin, and PZ14 was resistant to ciprofloxacin, cefoxitin, and streptomycin. Hence, pickles are a good source of beneficial probiotics for humans.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Armas F.; Camperio C.; Marianelli, C. In vitro assessment of the probiotic potential of Lactococcus lactis LMG 7930 against ruminant mastitis-causing pathogens. PLoS One. 2017, 12(1), Article e0169543. https://doi.org/10.1371/journal.pone.0169543
Bunnueang, N.; Kongpheng, S.; Yadrak P.; Rattanachuay, P.; Khianngam, S.; Sukhumungoon, P. Methicillin-resistant Staphylococcus aureus: 1-year collection and characterization from petients in two tertiary hospitals, southern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health. 2016, 47, 234-244.
Charteris, W. P.; Kelly, P. M.; Morelli, L.; Collins, J. K. Selective detection, enumeration and identification of potentially probiotic Lactobacillus and Bifidobacterium species in mixed bacterial populations. International Journal of Food Microbiology. 1997, 35, 1-27. https://doi.org/10.1016/S0168-1605(96)01222-6
Crago, B.; Ferrato, C.; Drews, S. J.; Svenson, L. W.; Tyrrell, G.; Louie, M. Prevalence of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in food samples associated with foodborne illness in Alberta, Canada from 2007 to 2010. Food Microbiol. 2012, 32(1), 202-5. https://doi.org/10.1016/j.fm.2012.04.012
Danielsen, M.; Wind, A. Susceptibility of Lactobacillus spp. to antimicrobial agents. International Journal of Food Microbiology. 2003, 82, 1-11. https://doi.org/10.1016/S0168-1605(02)00254-4
Duangjitcharoen, Y.; Kantachote, D.; Ongsakul, M.; Poosaran, N.; Chaiyasut, C. Potential use of probiotic Lactobacillus plantarum SS2 isolated from a fermented plant beverage: safety assessment and persistence in the murine gastrointestinal tract. World Journal of Microbiology and Biotechnology. 2009, 25, 315-321. https://doi.org/10.1007/s11274-008-9894-0
Dušková, M.; Karpíšková, R. Antimicrobial resistance of Lactobacilli isolated from food. Czech Journal of Food Sciences. 2013, 31, 27-32. https://doi.org/10.17221/110/2012-CJFS [8]Fluer, F. S. Staphylococcal toxin of toxic shock syndrome. Zh Mikrobiol Epidemiol Immunobiol. 2007; Sep-Oct (5), 106-14.
Gómez-Zavaglia, A.; Kociubinski, G.; Pérez, P.; DeAntoni, G. Effect of bile on the lipid composition and surface properties of bifidobacteria. Journal of Applied Microbiology. 2002, 93, 794-799. https://doi.org/10.1046/j.1365-2672.2002.01747.x
Hayisama-ae, W.; Kantachote, D.; Bhongsuwan, D.; Nokkaew, U.; Chaiyasut, C. A potential synbiotic beverage from fermented red seaweed (Gracilaria fisheri) using Lactobacillus plantarum DE12. International Food Research Journal. 2014, 21(5): 1789-1796.
Hermanns, G.; Funck, G. D.; Schmidt, J. T.; Pereira, J. Q.; Brandelli, A.; Richards, N. S. P. D. S. Evaluation of probiotic characteristics of lactic acid bacteria isolated from artisan cheese. Journal of Food Safety. 2014. 34, 380-387. https://doi.org/10.1111/jfs.12138
Hickson, M.; Souza, A. L. D.; Muthu, N.; Rogers, T. R.; Want, S.; Rajkumar, C.; Builpitt, C. J. Use of probiotic Lactobacillus preparation to prevent diarrhea associated with antibiotics: randomized double blind placebo controlled trial. British Medical Journal. 2007, 335 (7610), 80-83. https://doi.org/10.1136/bmj.39231.599815.55
Hwang, S. Y.; Kim, S. H.; Jang, E. J.; Kwon, N.H.; Park, Y. K.; Koo, H. C.; Jung, W. K.; Kim, J. M.; Park, Y. H. Novel multiplex PCR for the detection of the Staphylococcus aureus superantigen and its application to raw meat isolates in Korea. International Journal of Food Microbiology. 2007, 117(1), 99-105. https://doi.org/10.1016/j.ijfoodmicro.2007.02.013
Hussain, A.; Robinson, G.; Malkin, J.; Duthie, M.; Kearns, A.; Perera, N. Purpura fulminans in a child secondary to Panton-Valentine leukocidin-producing Staphylococcus aureus. Journal of Medical Microbiology. 2007, 56 (10), 1407-1409. https://doi.org/10.1099/jmm.0.47374-0
Jiang, W.; Hou, Y.; Inouye, M. CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. Journal of Biological Chemistry. 1997, 272(1), 196-202. https://doi.org/10.1074/jbc.272.1.196
Jitpakdee, J.; Kantachote, D.; Kanzaki, H.; Nitoda, T. Selected probiotic lactic acid bacteria isolated from fermented foods for functional milk production: Lower cholesterol with more beneficial compounds. LWT - Food Science and Technology. 2021, 135, 110061. https://doi.org/10.1016/j.lwt.2020.110061
Karapetkov, N.; Georgieva, R.; Rumyan, N.; Karaivanova, E. Antibiotic susceptibility of different lactic acid bacteria strains. Beneficial Microbes. 2011, 2, 335-339. https://doi.org/10.3920/BM2011.0016
Kumar, R. S.; Brannigan, J. A.; Prabhune, A. A.; Pundle, A. V.; Dodson, G. G.; Dodson, E. J.; Suresh, C. G. Structural and functional analysis of a conjugated bile salt hydrolase from Bifidobacterium longum reveals an evolutionary relationship with penicillin V acylase. Journal of Biological Chemistry. 2006, 281, 32516-32525. https://doi.org/10.1074/jbc.M604172200
Makras, L.; Triantafyllou, V.; Fayal-Messaoudi, D.; Adriany, T.; Zoumpopoulou, G.; Tsakalidou, E.; Servin, A; De Vuyst, L. Kinetic analysis of the antibacterial activity of probiotic lactobacilli towards Salmonella enterica serovar Typhimurium reveals a role for lactic acid and other inhibitory compounds. Research in Microbiology. 2005, 157, 241-247. https://doi.org/10.1016/j.resmic.2005.09.002
Marrack, P.; Kappler, J. The staphylococcal enterotoxins and their relatives. Science. 1990, 248, 705-711. https://doi.org/10.1126/science.2185544
Nataro, J. P.; Kaper, J. B. Diarrheagenic Escherichia coli. Clinical Microbiology Reviews. 1998, 11, 142-201. https://doi.org/10.1128/CMR.11.1.142
Nawaz, M.; Wang, J.; Zhou, A.; Ma, C.; Wu, X.; Moore, J. E.; Millar, B. C.; Xu, J. Characterization and transfer of antibiotic resistance in lactic acid bacteria from fermented food products. Current Microbiology. 2011, 62, 1081-1089. https://doi.org/10.1007/s00284-010-9856-2
Pfeiler, E. A.; Klaenhammer, T. R. Role of transporter proteins in bile tolerance of Lactobacillus acidophilus. Applied and Environmental Microbiology. 2009, 75, 6013-6016. https://doi.org/10.1128/AEM.00495-09
Reid, S. D.; Betting, D. J.; Whittam, T. S. Molecular detection and identification of intimin alleles in pathogenic Escherichia coli by multiplex PCR. Journal of Clinical Microbiology. 1999, 37, 2719-2722. https://doi.org/10.1128/JCM.37.8.2719-2722.1999
Riley, L.W.; Remis, R. S.; Helgerson, S. D.; McGee, H.B.; Wells, J. G.; Davis, B. R.; Hebert, R. J.; Olcott, E. S.; Johnson, L. M.; Hargrett, N. T.; Blake, P. A.; Cohen, M. L. Hemorrhagic colitis associated with a rare Escherichia coli serotype. New England Journal of Medicine. 1983, 308, 681-5. https://doi.org/10.1056/NEJM198303243081203
Ruiz, L.; Margolles, A.; Sanchez, B. Bile resistant mechanisms in Lactobacillus and Bifidobacterium. Frontier in Microbiology. 2013, 369(4), 1-8. https://doi.org/10.3389/fmicb.2013.00396. https://doi.org/10.3389/fmicb.2013.00396
Sirikaew, S.; Patungkaro, W.; Rattanachuay, P.; Sukkua, K.; Sukhumungoon, P. Enterotoxigenic Escherichia coli O169:HUT from a diarrheal patient: Phylogenetic group and antimicrobial susceptibility. Southeast Asian Journal of Tropical Medicine and Public Health. 2014, 45, 1376-1384.
Sukkua, K.; Patungkaro, W.; Sukhumungoon, P. Detection and molecular characterization of enteroaggregative Escherichia coli from diarrheal patients in tertiary hospitals, Southern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health. 2015, 46, 901-910.
Sukhumungoon, P., & Nakaguchi, Y. Shiga toxin 2-converting bacteriophages occupy sbcB gene as a primary integration site in bovine-origined Escherichia coli O157:H7 and non-O157 from Thailand. Life Science Journal. 2013, 10, 2334-2340.
Sukhumungoon, P.; Hayeebilan, F.; Yadrak, P.; Kanobthammakul, S.; Nakaguchi, Y.; Saengsuwan, P.; Singkhamanan, K. Molecular characterization and relationship of methicillin-resistant Staphylococcus aureus among strains from healthy carriers and University hospital patients, southern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health. 2014, 45, 402-412.
Tulini, F.L.; Winkelströter, L. K.; De Martinis, E. C. Identification and evaluation of the probiotic potential of Lactobacillus paraplantarum FT259, a bacteriocinogenic strain isolated from Brazilian semi-hard artisanal cheese. Anaerobe. 2013, 22, 57-63. https://doi.org/10.1016/j.anaerobe.2013.06.006
Urdaneta, V.; Casadesús, J. Interactions between bacteria and bile salts in the gastrointestinal and hepatobiliary tracts. Frontiers in Medicine (Lausanne). 2017, 4, 163. https://doi.org/10.3389/fmed.2017.00163
Wang, S.; Li, Y.; Xiong, H.; Cao, J. A broad-spectrum inhibitory peptide against staphylococcal enterotoxin superantigen SEA, SEB and SEC. Immunology Letters. 2008, 121, 167-72. https://doi.org/10.1016/j.imlet.2008.10.007
Wang, C.Y.; Lin, P.R.; Ng, C.C.; Shyu, Y. T. Probiotic properties of Lactobacillus strains isolated from the feces of breast-fed infants and Taiwanese pickled cabbage. Anaerobe. 2010, 16, 578-85. https://doi.org/10.1016/j.anaerobe.2010.10.003
Wang, C.; Cui, Y.; Qu, X. Mechanism and improvement of acid resistance in lactic acid bacteria. Archives of Microbiology. 2018. 200, 195-201. https://doi.org/10.1007/s00203-017-1446-2. https://doi.org/10.1007/s00203-017-1446-2
Witte, W.; Pasemann, B.; Cuny, C. Detection of low-level oxacillin resistance in mecA-positive Staphylococcus aureus. Clinical Microbiology and Infection. 2007, 13, 408-412. https://doi.org/10.1111/j.1469-0691.2006.01671.x