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Potential Control of Listeria monocytogenes by Bacteriocinogenic Enterococcus hirae ST57ACC and Pediococcus pentosaceus ST65ACC Strains Isolated From Artisanal Cheese

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Abstract

Bacteriocinogenic Enterococcus hirae ST57ACC and Pediococcus pentosaceus ST65ACC strains, previously isolated from artisanal cheese, were evaluated for their safety with the aim to determine whether they could be used as beneficial strains, especially in the control of Listeria monocytogenes. Both isolates survived simulated gastrointestinal conditions and showed high levels of auto- and co-aggregation with L. monocytogenes, although the hydrophobicity of cells varied. Using the agar-spot test with 33 commercial drugs from different groups, only anti-inflammatory drugs and drugs containing loratadine and propranolol hydrochloride were able to affect the growth of the tested strains. Both strains were resistant to 3 out of 11 antibiotics tested by the disc diffusion method, and low frequencies of antibiotic resistance-encoding genes were observed by PCR analysis. Tested strains neither presented biogenic amine-related genes nor produced these substances. Aside from some antibiotic resistance characteristics, the tested strains were considered safe as they lack other virulence-related genes. E. hirae ST57ACC and P. pentosaceus ST65ACC both presented beneficial properties, particularly their ability to survive gastrointestinal conditions and to aggregate with L. monocytogenes, which can facilitate the elimination of this pathogen. Further studies should be conducted to better understand these interactions.

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References

  1. Donovan S (2015) Listeriosis: a rare but deadly disease. Clin Microbiol Newsl 37(17):135–140

    Article  Google Scholar 

  2. Grif K, Patscheider G, Dierich MP, Allerberger F (2003) Incidence of fecal carriage of Listeria monocytogenes in three healthy volunteers: a one-year prospective stool survey. Eur J Clin Microbiol Infect Dis 22(1):16–20

    CAS  PubMed  Google Scholar 

  3. Swaminathan B, Gerner-Smidt P (2007) The epidemiology of human listeriosis. Microbes Infect 9(10):1236–1243

    Article  PubMed  Google Scholar 

  4. Camargo AC, Woodward JJ, Call DR, Nero LA (2017) Listeria monocytogenes in food-processing facilities, food contamination, and human listeriosis: the Brazilian scenario. Foodborne Pathog Dis 14(11):623–636. https://doi.org/10.1089/fpd.2016.2274

    Article  PubMed  Google Scholar 

  5. Camargo AC, Dias MR, Cossi MVC, Lanna FGPA, Cavicchioli VQ, Vallim DC, Pinto PSA, Hofer E, Nero LA (2015) Serotypes and pulsotypes diversity of Listeria monocytogenes in a beef-processing environment. Foodborne Pathog Dis 12(4):323–326

    Article  PubMed  Google Scholar 

  6. Gandhi M, Chikindas ML (2007) Listeria: a foodborne pathogen that knows how to survive. Int J Food Microbiol 113(1):1–15

    Article  PubMed  Google Scholar 

  7. Alvarez-Sieiro P, Montalbán-López M, Mu D, Kuipers OP (2016) Bacteriocins of lactic acid bacteria: extending the family. Appl Microbiol Biotechnol 100(7):2939–2951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Drider D, Rebuffat S (2011) Prokaryotic antimicrobial peptides: from genes to applications. Springer

  9. Dobson A, Cotter PD, Ross RP, Hill C (2012) Bacteriocin production: a probiotic trait? Appl Environ Microbiol 78(1):1–6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Cotter PD, Hill C, Ross RP (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3(10):777–788

    Article  CAS  PubMed  Google Scholar 

  11. Martinez RCR, Staliano CD, Vieira ADS, Villarreal MLM, Todorov SD, Saad SMI, Franco BDGM (2015) Bacteriocin production and inhibition of Listeria monocytogenes by Lactobacillus sakei subsp. sakei 2a in a potentially symbiotic cheese spread. Food Microbiol 48:143–152. https://doi.org/10.1016/j.fm.2014.12.010

    Article  CAS  PubMed  Google Scholar 

  12. Settanni L, Guarcello R, Gaglio R, Francesca N, Aleo A, Felis GE, Moschetti G (2014) Production, stability, gene sequencing and in situ anti-Listeria activity of mundticin KS expressed by three Enterococcus mundtii strains. Food Control 35(1):311–322

    Article  CAS  Google Scholar 

  13. Richard C, Brillet A, Pilet MF, Prévost H, Drider D (2003) Evidence on inhibition of Listeria monocytogenes by divercin V41 action. Lett Appl Microbiol 36(5):288–292. https://doi.org/10.1046/j.1472-765X.2003.01310.x

    Article  CAS  PubMed  Google Scholar 

  14. Corr SC, Hill C, Gahan CGM (2009) Understanding the mechanisms by which probiotics inhibit gastrointestinal pathogens. Adv Food Nutr Res 56:1–15

    Article  CAS  PubMed  Google Scholar 

  15. Londoño-Zapata AF, Durango-Zuleta MM, Sepúlveda-Valencia JU, Herrera CXM (2017) Characterization of lactic acid bacterial communities associated with a traditional Colombian cheese: double cream cheese. LWT Food Sci Technol 82:39–48

    Article  CAS  Google Scholar 

  16. Portilla-Vázquez S, Rodríguez A, Ramírez-Lepe M, Mendoza-García PG, Martínez B (2016) Biodiversity of Bacteriocin-producing lactic acid Bacteria from Mexican regional cheeses and their contribution to milk fermentation. Food Biotechnol 30(3):155–172

    Article  CAS  Google Scholar 

  17. Aspri M, O'Connor PM, Field D, Cotter PD, Ross P, Hill C, Papademas P (2017) Application of bacteriocin-producing Enterococcus faecium isolated from donkey milk, in the bio-control of Listeria monocytogenes in fresh whey cheese. Int Dairy J 73:1–9

    Article  CAS  Google Scholar 

  18. Huang Y, Luo Y, Zhai Z, Zhang H, Yang C, Tian H, Li Z, Feng J, Liu H, Hao Y (2009) Characterization and application of an anti-Listeria bacteriocin produced by Pediococcus pentosaceus 05-10 isolated from Sichuan pickle, a traditionally fermented vegetable product from China. Food Control 20(11):1030–1035

    Article  CAS  Google Scholar 

  19. Cavicchioli VQ, Camargo AC, Todorov SD, Nero LA (2017) Novel bacteriocinogenic Enterococcus hirae and Pediococcus pentosaceus strains with antilisterial activity isolated from Brazilian artisanal cheese. J Dairy Sci 100(4):2526–2535. https://doi.org/10.3168/jds.2016-12049

    Article  CAS  PubMed  Google Scholar 

  20. Santos KMO, Vieira ADS, Buriti FCA, Nascimento JCF, Melo MES, Bruno LM, Borges MF, Rocha CRC, Lopes AC, Franco BDGM (2015) Artisanal Coalho cheeses as source of beneficial Lactobacillus plantarum and Lactobacillus rhamnosus strains. Dairy Sci Technol 95(2):209–230

    Article  CAS  Google Scholar 

  21. Santos KMO, Vieira ADS, Salles HO, Oliveira JS, Rocha CRC, Borges MF, Bruno LM, Franco BDGM, Todorov SD (2015) Safety, beneficial and technological properties of Enterococcus faecium isolated from Brazilian cheeses. Braz J Microbiol 46(1):237–249

    Article  PubMed  PubMed Central  Google Scholar 

  22. Todorov SD, Botes M, Guigas C, Schillinger U, Wiid I, Wachsman MB, Holzapfel WH, Dicks LMT (2008) Boza, a natural source of probiotic lactic acid bacteria. J Appl Microbiol 104(2):465–477

    CAS  PubMed  Google Scholar 

  23. Paula AT, Jeronymo-Ceneviva AB, Silva LF, Todorov SD, Franco BDGM, Penna ALB (2015) Leuconostoc mesenteroides SJRP55: a potential probiotic strain isolated from Brazilian water buffalo mozzarella cheese. Ann Microbiol 65(2):899–910

    Article  CAS  Google Scholar 

  24. CLSI (2016) M100-S26 - performance standards for antimicrobial susceptibility testing: twenty-sixth informational supplement. Clinical and laboratory standards institute, Wayne, PA

  25. Perin LM, Miranda RO, Todorov SD, Franco BDGM, Nero LA (2014) Virulence, antibiotic resistance and biogenic amines of bacteriocinogenic lactococci and enterococci isolated from goat milk. Int J Food Microbiol 185:121–126

    Article  CAS  PubMed  Google Scholar 

  26. Bover-Cid S, Holzapfel WH (1999) Improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol 53(1):33–41

    Article  CAS  PubMed  Google Scholar 

  27. Joosten HMLJ, Northolt MD (1989) Detection, growth, and amine-producing capacity of lactobacilli in cheese. Appl Environ Microbiol 55:2356–2359

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Taheur FB, Fedhila K, Chaieb K, Kouidhi B, Bakhrouf A, Abrunhosa L (2017) Adsorption of aflatoxin B1, zearalenone and ochratoxin a by microorganisms isolated from kefir grains. Int J Food Microbiol 251:1–7. https://doi.org/10.1016/j.ijfoodmicro.2017.03.021

    Article  CAS  PubMed  Google Scholar 

  29. Rojas M, Ascencio F, Conway PL (2002) Purification and characterization of a surface protein from Lactobacillus fermentum 104R that binds to porcine small intestinal mucus and gastric mucin. Appl Environ Microbiol 68(5):2330–2336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Aslim B, Onal D, Beyatli Y (2007) Factors influencing autoaggregation and aggregation of Lactobacillus delbrueckii subsp. bulgaricus isolated from handmade yogurt. J Food Prot 70(1):223–227

    Article  PubMed  Google Scholar 

  31. Chen X, Xu J, Shuai J, Chen J, Zhang Z, Fang W (2007) The S-layer proteins of Lactobacillus crispatus strain ZJ001 is responsible for competitive exclusion against Escherichia coli O157: H7 and Salmonella typhimurium. Int J Food Microbiol 115(3):307–312

    Article  CAS  PubMed  Google Scholar 

  32. Furtado DN, Todorov SD, Landgraf M, Destro MT, Franco BDGM (2014) Bacteriocinogenic Lactococcus lactis subsp. lactis DF04Mi isolated from goat milk: evaluation of the probiotic potential. Braz J Microbiol 45(3):1047–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Carvalho KG, Kruger MF, Furtado DN, Todorov SD, Franco BDGM (2009) Evaluation of the role of environmental factors in the human gastrointestinal tract on the behaviour of probiotic cultures of Lactobacillus casei Shirota and Lactobacillus casei LC01 by the use of a semi-dynamicin vitro model. Ann Microbiol 59(3):439–445

    Article  Google Scholar 

  34. Jeronymo-Ceneviva AB, Paula AT, Silva LF, Todorov SD, Franco BDGM, Penna ALB (2014) Probiotic properties of lactic acid bacteria isolated from water-buffalo mozzarella cheese. Probiotics Antimicrob Proteins 6(3–4):141–156

    Article  CAS  PubMed  Google Scholar 

  35. Valenzuela AS, Omar N, Abriouel H, López RL, Veljovic K, Cañamero MM, Topisirovic MKL, Gálvez A (2009) Virulence factors, antibiotic resistance, and bacteriocins in enterococci from artisan foods of animal origin. Food Control 20(4):381–385. https://doi.org/10.1016/j.foodcont.2008.06.004

    Article  CAS  Google Scholar 

  36. Franz CMAP, Endo A, Abriouel H, Reenen CAV, Gálvez A, Dicks LMT (2014) The genus Pediococcus. In: Lactic acid Bacteria: biodiversity and taxonomy. pp 359–376

  37. Danielsen M, Simpson PJ, O'Connor EB, Ross RP, Stanton C (2007) Susceptibility of Pediococcus spp. to antimicrobial agents. J Appl Microbiol 102(2):384–389

    Article  CAS  PubMed  Google Scholar 

  38. Mathur S, Singh R (2005) Antibiotic resistance in food lactic acid bacteria—a review. Int J Food Microbiol 105(3):281–295

    Article  CAS  PubMed  Google Scholar 

  39. Martín-Platero AM, Valdivia E, Maqueda M, Martínez-Bueno M (2009) Characterization and safety evaluation of enterococci isolated from Spanish goats' milk cheeses. Int J Food Microbiol 132(1):24–32

    Article  CAS  PubMed  Google Scholar 

  40. Lopes MFS, Simões AP, Tenreiro R, Marques JJF, Crespo MTB (2006) Activity and expression of a virulence factor, gelatinase, in dairy enterococci. Int J Food Microbiol 112(3):208–214. https://doi.org/10.1016/j.ijfoodmicro.2006.09.004

    Article  CAS  Google Scholar 

  41. Qin X, Singh KV, Weinstock GM, Murray BE (2001) Characterization of fsr, a regulator controlling expression of gelatinase and serine protease in Enterococcus faecalis OG1RF. J Bacteriol 183(11):3372–3382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Dunny GM (2013) Enterococcal sex pheromones: signaling, social behavior, and evolution. Annu Rev Genet 47:457–482

    Article  CAS  PubMed  Google Scholar 

  43. Ladero V, Martín MC, Redruello B, Mayo B, Flórez AB, Fernández M, Alvarez MA (2015) Genetic and functional analysis of biogenic amine production capacity among starter and non-starter lactic acid bacteria isolated from artisanal cheeses. Eur Food Res Technol 241(3):377–383

    Article  CAS  Google Scholar 

  44. Ladero V, Fernández M, Calles-Enríquez M, Sánchez-Llana E, Cañedo E, Martín MC, Alvarez MA (2012) Is the production of the biogenic amines tyramine and putrescine a species-level trait in enterococci? Food Microbiol 30(1):132–138

    Article  CAS  PubMed  Google Scholar 

  45. Aarestrup FM, Agerso Y, Gerner–Smidt P, Madsen M, Jensen LB (2000) Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers, and pigs in Denmark. Diagn Microbiol Infect Dis 37(2):127–137

    Article  CAS  PubMed  Google Scholar 

  46. Eaton TJ, Gasson MJ (2001) Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol 67(4):1628–1635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Fortina MG, Ricci G, Borgo F, Manachini PL, Arends K, Schiwon K, Abajy MY, Grohmann E (2008) A survey on biotechnological potential and safety of the novel Enterococcus species of dairy origin, E. italicus. Int J Food Microbiol 123(3):204–211. https://doi.org/10.1016/j.ijfoodmicro.2008.01.014

    Article  CAS  PubMed  Google Scholar 

  48. Matos R, Pinto VV, Ruivo M, Lopes MFS (2009) Study on the dissemination of the cluster in spp. reveals that the BcrAB transporter is sufficient to confer high-level bacitracin resistance. Int J Antimicrob Agents 34(2):142–147

    Article  CAS  PubMed  Google Scholar 

  49. Nakayama J, Kariyama R, Kumon H (2002) Description of a 23.9-kilobase chromosomal deletion containing a region encoding fsr genes which mainly determines the gelatinase-negative phenotype of clinical isolates of Enterococcus faecalis in urine. Appl Environ Microbiol 68(6):3152–3155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Radhouani H, Igrejas G, Pinto L, Gonçalves A, Coelho C, Rodrigues J, Poeta P (2011) Molecular characterization of antibiotic resistance in enterococci recovered from seagulls (Larus cachinnans) representing an environmental health problem. J Environ Monit 13(8):2227–2233

    Article  CAS  PubMed  Google Scholar 

  51. Rivas P, Alonso J, Moya J, de Górgolas M, Martinell J, Guerrero MLF (2005) The impact of hospital-acquired infections on the microbial etiology and prognosis of late-onset prosthetic valve endocarditis. CHEST J 128(2):764–771

    Article  Google Scholar 

  52. Sutcliffe J, Grebe T, Tait-Kamradt A, Wondrack L (1996) Detection of erythromycin-resistant determinants by PCR. Antimicrob Agents Chemother 40(11):2562–2566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Vankerckhoven V, Huys G, Vancanneyt M, Vael C, Klare I, Romond M, Entenza JM, Moreillon P, Wind RD, Knol J (2008) Biosafety assessment of probiotics used for human consumption: recommendations from the EU-PROSAFE project. Trends Food Sci Technol 19(2):102–114

    Article  CAS  Google Scholar 

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Funding

This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG).

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Authors and Affiliations

  1. Departamento de Veterinária, Campus UFV, Universidade Federal de Viçosa, Viçosa, MG, 36570-900, Brazil

    Valéria Quintana Cavicchioli, Anderson Carlos Camargo, Svetoslav Dimitrov Todorov & Luís Augusto Nero

  2. Faculdade de Ciências Farmacêuticas, Universidade de São Paulo, Av. Prof. Lineu Prestes 580, São Paulo, SP, 05508-000, Brazil

    Svetoslav Dimitrov Todorov

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  1. Valéria Quintana Cavicchioli
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  2. Anderson Carlos Camargo
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  3. Svetoslav Dimitrov Todorov
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  4. Luís Augusto Nero
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Correspondence to Luís Augusto Nero.

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None animal was used in any of the described experiments.

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Cavicchioli, V.Q., Camargo, A.C., Todorov, S.D. et al. Potential Control of Listeria monocytogenes by Bacteriocinogenic Enterococcus hirae ST57ACC and Pediococcus pentosaceus ST65ACC Strains Isolated From Artisanal Cheese. Probiotics & Antimicro. Prot. 11, 696–704 (2019). https://doi.org/10.1007/s12602-018-9449-0

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