Effect of low concentrations of lactic acid and temperature on the expression of adhesion, invasion, and toxin-encoding genes of Campylobacter jejuni from poultry
-
Aliakbar Jadidi
,
Abdolmajid Ghasemian
,
Abbas Abdollahi
,
Tannaz Abbasi-Dokht
,
Esmail Abdollahzadeh
,
Rasoul Baharlou
Abstract
Background and Objectives: The consumption of contaminated poultry meat is considered as a significant route of campylobacteriosis transmission. Lactic acid is a disinfectant agent with bactericidal effects on Campylobacter spp. The purpose of this study was to assess the low concentrations of lactic acid effect and different temperatures on the transcriptomic responses of Campylobacter jejuni (C. jejuni) adhesion and virulence-associated genes including peb4, ciaB, cdtA, cdtB, and cdtC.
Materials and Methods: The samples were incubated at 10°C and 22°C for 48 h upon exposure to 30% and 60% lactic acid. The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of lactic acid was also determined. Then, gene expression was assessed using real-time polymerase chain reaction (RT-PCR).
Results: Lactic acid had lower MIC and MBC levels at lower temperature. The utilization of both levels of lactic acid significantly reduced the expression of peb4, ciaB, cdtB, and cdtC genes over 48 h of incubation at 22°C. However, no significant difference was found in the expression of the cdtA gene between 10 and 22°C at 30% lactic acid.
Conclusion: These results highlight the potential of low-concentration lactic acid in the downregulation of adhesion and virulence-associated genes as well as reduction of C. jejuni pathogenicity.
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2. Wieczorek K, Wołkowicz T, Osek J. Antimicrobial resistance and virulence-associated traits of Campylobacter jejuni isolated from poultry food chain and humans with diarrhea. Front Microbiol 2018; 9: 1508.
3. Ashrafganjooyi Sb, Saedadlei N. Isolation and determine antibiotic susceptibility of Campylobacter jejuni in poultry feces in kerman. Iran J Med Microbiol 2016; 9: 95-98.
4. Sarabi Asiabar A, Asadzadeh Aghdaei H, Zamani S, Bokaie S, Zali MR, Feizabadi MM. Molecular detection of Campylobacter jejuni in patients with Crohn’s disease in Iran. Med J Islam Repub Iran 2019; 33: 76.
5. Koolman L, Whyte P, Burgess C, Bolton D. Virulence gene expression, adhesion and invasion of Campylobacter jejuni exposed to oxidative stress (H2O2). Int J Food Microbiol 2016; 220: 33-38.
6. Rahimifard N, Shoeibi SH, Mirsalehian A, Mehdizadeh M, Saadati SH, Noori Z, et al. Detection of Campylobacter jejuni in raw meat. Iran J Microbiol 2009; 1: 43-44.
7. Feizabadi MM, Dolatabadi S, Zali MR. Isolation and drug-resistant patterns of Campylobacter strains cultured from diarrheic children in Tehran. Jpn J Infect Dis 2007; 60: 217-219.
8. Skarp C, Hänninen M-L, Rautelin HIK. Campylobacteriosis: the role of poultry meat. Clin Microbiol Infect 2016; 22: 103-109.
9. El Baaboua A, El Maadoudi M, Bouyahya A, Kounnoun A, Bougtaib H, Belmehdi O, et al. Prevalence and antimicrobial profiling of Campylobacter spp. isolated from meats, animal, and human feces in Northern of Morocco. Int J Food Microbiol 2021; 349: 109202.
10. Walker LJ, Wallace RL, Smith JJ, Graham T, Saputra T, Symes S, et al. Prevalence of Campylobacter coli and Campylobacter jejuni in retail chicken, beef, lamb, and pork products in three Australian states. J Food Prot 2019; 82: 2126-2134.
11. Maktabi S, Ghorbanpoor M, Hossaini M, Motavalibashi A. Detection of multi-antibiotic resistant Campylobacter coli and Campylobacter jejuni in beef, mutton, chicken and water buffalo meat in Ahvaz, Iran. Vet Res Forum 2019; 10: 37-42.
12. Andrzejewska M, Szczepańska B, Śpica D, Klawe JJ. Prevalence, virulence, and antimicrobial resistance of Campylobacter spp. in raw milk, beef, and pork meat in Northern Poland. Foods 2019; 8: 420.
13. Lee N-K, Jung BS, Na DS, Yu HH, Kim J-S, Paik H-D. The impact of antimicrobial effect of chestnut inner shell extracts against Campylobacter jejuni in chicken meat. LWT 2016; 65: 746-750.
14. Salaheen S, Nguyen C, Hewes D, Biswas D. Cheap extraction of antibacterial compounds of berry pomace and their mode of action against the pathogen Campylobacter jejuni. Food Control 2014; 46: 174-181.
15. Sima F, Stratakos AC, Ward P, Linton M, Kelly C, Pinkerton L, et al. A novel natural antimicrobial can reduce the in vitro and in vivo pathogenicity of T6SS positive Campylobacter jejuni and Campylobacter coli chicken isolates. Front Microbiol 2018; 9: 2139.
16. Wang G, Zhao Y, Tian F, Jin X, Chen H, Liu X, et al. Screening of adhesive lactobacilli with antagonistic activity against Campylobacter jejuni. Food Control 2014; 44: 49-57.
17. Gonzalez-Fandos E, Maya N, Martínez-Laorden A, Perez-Arnedo I. Efficacy of lactic acid and modified atmosphere packaging against Campylobacter jejuni on chicken during refrigerated storage. Foods 2020; 9: 109.
18. Wang Y, Wu J, Lv M, Shao Z, Hungwe M, Wang J, et al. Metabolism characteristics of lactic acid bacteria and the expanding applications in food industry. Front Bioeng Biotechnol 2021; 9: 612285.
19. Wang Y, Han J, Wang D, Gao F, Zhang K, Tian J, et al. Research update on the impact of lactic acid bacteria on the substance metabolism, flavor, and quality characteristics of fermented meat products. Foods 2022; 11: 2090.
20. Reddy S, Zishiri OT. Genetic characterisation of virulence genes associated with adherence, invasion and cytotoxicity in Campylobacter spp. isolated from commercial chickens and human clinical cases. Onderstepoort J Vet Res 2018; 85(1): e1-e9.
21. de Oliveira MG, Rizzi C, Galli V, Lopes GV, Haubert L, Dellagostin OA, et al. Presence of genes associated with adhesion, invasion, and toxin production in Campylobacter jejuni isolates and effect of temperature on their expression. Can J Microbiol 2019; 65: 253-260.
22. Talukder KA, Aslam M, Islam Z, Azmi IJ, Dutta DK, Hossain S, et al. Prevalence of virulence genes and cytolethal distending toxin production in Campylobacter jejuni isolates from diarrheal patients in Bangladesh. J Clin Microbiol 2008; 46: 1485-1488.
23. Asakura H, Yamasaki M, Yamamoto S, Igimi S. Deletion of peb4 gene impairs cell adhesion and biofilm formation in Campylobacter jejuni. FEMS Microbiol Lett 2007; 275: 278-285.
24. Bai Y, Ding X, Zhao Q, Sun H, Li T, Li Z, et al. Development of an organic acid compound disinfectant to control food-borne pathogens and its application in chicken slaughterhouses. Poult Sci 2022; 101: 101842.
25. Silveira VAI, Nishio EK, Freitas CA, Amador IR, Kobayashi RK, Caretta T, et al. Production and antimicrobial activity of sophorolipid against Clostridium perfringens and Campylobacter jejuni and their additive interaction with lactic acid. Biocatal Agric Biotechnol 2019; 21: 101287.
26. Byun K-H, Na KW, Ashrafudoulla M, Choi MW, Han SH, Kang I, et al. Combination treatment of peroxyacetic acid or lactic acid with UV-C to control Salmonella Enteritidis biofilms on food contact surface and chicken skin. Food Microbiol 2022; 102: 103906.
27. Kraemer MVDS, Fernandes AC, Chaddad MCC, Uggioni PL, Rodrigues VM, Bernardo GL, et al. Food additives in childhood: a review on consumption and health consequences. Rev Saude Publica 2022; 56: 32.
28. Hosseini S, Abdollahzadeh E, Ranaei V, Mahmoudzadeh M, Pilevar Z. Effect of Zataria multiflora Boiss. essential oil, time, and temperature on the expression of Listeria monocytogenes virulence genes in broth and minced rainbow trout. Food Sci Nutr 2021; 9: 2290-2298.
29. de Souza EL, de Barros JC, da Conceição ML, Neto NJ, da Costa AC. Combined application of Origanum vulgare L. essential oil and acetic acid for controlling the growth of Staphylococcus aureus in foods. Braz J Microbiol 2009; 40: 387-393.
30. Abdollahzadeh E, Rezaei M, Hosseini H. Antibacterial activity of plant essential oils and extracts: The role of thyme essential oil, nisin, and their combination to control Listeria monocytogenes inoculated in minced fish meat. Food Control 2014; 35: 177-183.
31. Dasti JI, Tareen AM, Lugert R, Zautner AE, Groß U. Campylobacter jejuni: a brief overview on pathogenicity-associated factors and disease-mediating mechanisms. Int J Med Microbiol 2010; 300: 205-211.
32. Shyaka A, Kusumoto A, Chaisowwong W, Okouchi Y, Fukumoto S, Yoshimura A, et al. Virulence characterization of Campylobacter jejuni isolated from resident wild birds in Tokachi area, Japan. J Vet Med Sci 2015; 77: 967-972.
33. Klančnik A, Vučković D, Jamnik P, Abram M, Možina SS. Stress response and virulence of heat-stressed Campylobacter jejuni. Microbes Environ 2014; 29: 338-345.
34. Blevins RE, Kim SA, Park SH, Rivera R, Ricke SC (2018). Historical, current, and future prospects for food safety in poultry product processing systems. Food and feed safety systems and analysis: Elsevier. p. 323-345.
35. Kovács JK, Cox A, Schweitzer B, Maróti G, Kovács T, Fenyvesi H, et al. Virulence traits of inpatient Campylobacter jejuni isolates, and a transcriptomic approach to identify potential genes maintaining intracellular survival. Microorganisms 2020; 8: 531.
36. Kovács JK, Felső P, Makszin L, Pápai Z, Horváth G, Ábrahám H, et al. Antimicrobial and virulence-modulating effects of clove essential oil on the foodborne pathogen Campylobacter jejuni. Appl Environ Microbiol 2016; 82: 6158-6166.
37. Duodu S, Holst-Jensen A, Skjerdal T, Cappelier J-M, Pilet M-F, Loncarevic S. Influence of storage temperature on gene expression and virulence potential of Listeria monocytogenes strains grown in a salmon matrix. Food Microbiol 2010; 27: 795-801.
38. Habib I, Uyttendaele M, De Zutter L. Survival of poultry-derived Campylobacter jejuni of multilocus sequence type clonal complexes 21 and 45 under freeze, chill, oxidative, acid and heat stresses. Food Microbiol 2010; 27: 829-834.
39. Tiganitas A, Zeaki N, Gounadaki AS, Drosinos EH, Skandamis PN. Study of the effect of lethal and sublethal pH and aw stresses on the inactivation or growth of Listeria monocytogenes and Salmonella Typhimurium. Int J Food Microbiol 2009; 134: 104-112.
40. Hosseini S, Abdollahzadeh E, Ranaei V, Mahmoudzadeh M, Pilevar Z. Effect of Zataria multiflora Boiss. essential oil, NaCl, acid, time, and temperature on the growth of Listeria monocytogenes strains in broth and minced rainbow trout. Food Sci Nutr 2021; 9: 2290-2298.
41. Efimochkina NR, Bykova IB, Markova YM, Korotkevich YV, Sheveleva SA. The study of influence of stresses on virulence genes expression in foodborne pathogens Campylobacter jejuni. Vopr Pitan 2016; 85: 66-74.
42. Khalid MI, Tang JY, Baharuddin NH, Rahman NS, Rahimi NF, Radu S. Prevalence, antibiogram, and cdt genes of toxigenic Campylobacter jejuni in salad style vegetables (ulam) at farms and retail outlets in Terengganu. J Food Prot 2015; 78: 65-71.
43. Poli VF, Thorsen L, Olesen I, Wik MT, Jespersen L. Differentiation of the virulence potential of Campylobacter jejuni strains by use of gene transcription analysis and a Caco-2 assay. Int J Food Microbiol 2012; 155: 60-68.
44. Carrillo CD, Taboada E, Nash JH, Lanthier P, Kelly J, Lau PC, et al. Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA. J Biol Chem 2004; 279: 20327-20338.
2. Wieczorek K, Wołkowicz T, Osek J. Antimicrobial resistance and virulence-associated traits of Campylobacter jejuni isolated from poultry food chain and humans with diarrhea. Front Microbiol 2018; 9: 1508.
3. Ashrafganjooyi Sb, Saedadlei N. Isolation and determine antibiotic susceptibility of Campylobacter jejuni in poultry feces in kerman. Iran J Med Microbiol 2016; 9: 95-98.
4. Sarabi Asiabar A, Asadzadeh Aghdaei H, Zamani S, Bokaie S, Zali MR, Feizabadi MM. Molecular detection of Campylobacter jejuni in patients with Crohn’s disease in Iran. Med J Islam Repub Iran 2019; 33: 76.
5. Koolman L, Whyte P, Burgess C, Bolton D. Virulence gene expression, adhesion and invasion of Campylobacter jejuni exposed to oxidative stress (H2O2). Int J Food Microbiol 2016; 220: 33-38.
6. Rahimifard N, Shoeibi SH, Mirsalehian A, Mehdizadeh M, Saadati SH, Noori Z, et al. Detection of Campylobacter jejuni in raw meat. Iran J Microbiol 2009; 1: 43-44.
7. Feizabadi MM, Dolatabadi S, Zali MR. Isolation and drug-resistant patterns of Campylobacter strains cultured from diarrheic children in Tehran. Jpn J Infect Dis 2007; 60: 217-219.
8. Skarp C, Hänninen M-L, Rautelin HIK. Campylobacteriosis: the role of poultry meat. Clin Microbiol Infect 2016; 22: 103-109.
9. El Baaboua A, El Maadoudi M, Bouyahya A, Kounnoun A, Bougtaib H, Belmehdi O, et al. Prevalence and antimicrobial profiling of Campylobacter spp. isolated from meats, animal, and human feces in Northern of Morocco. Int J Food Microbiol 2021; 349: 109202.
10. Walker LJ, Wallace RL, Smith JJ, Graham T, Saputra T, Symes S, et al. Prevalence of Campylobacter coli and Campylobacter jejuni in retail chicken, beef, lamb, and pork products in three Australian states. J Food Prot 2019; 82: 2126-2134.
11. Maktabi S, Ghorbanpoor M, Hossaini M, Motavalibashi A. Detection of multi-antibiotic resistant Campylobacter coli and Campylobacter jejuni in beef, mutton, chicken and water buffalo meat in Ahvaz, Iran. Vet Res Forum 2019; 10: 37-42.
12. Andrzejewska M, Szczepańska B, Śpica D, Klawe JJ. Prevalence, virulence, and antimicrobial resistance of Campylobacter spp. in raw milk, beef, and pork meat in Northern Poland. Foods 2019; 8: 420.
13. Lee N-K, Jung BS, Na DS, Yu HH, Kim J-S, Paik H-D. The impact of antimicrobial effect of chestnut inner shell extracts against Campylobacter jejuni in chicken meat. LWT 2016; 65: 746-750.
14. Salaheen S, Nguyen C, Hewes D, Biswas D. Cheap extraction of antibacterial compounds of berry pomace and their mode of action against the pathogen Campylobacter jejuni. Food Control 2014; 46: 174-181.
15. Sima F, Stratakos AC, Ward P, Linton M, Kelly C, Pinkerton L, et al. A novel natural antimicrobial can reduce the in vitro and in vivo pathogenicity of T6SS positive Campylobacter jejuni and Campylobacter coli chicken isolates. Front Microbiol 2018; 9: 2139.
16. Wang G, Zhao Y, Tian F, Jin X, Chen H, Liu X, et al. Screening of adhesive lactobacilli with antagonistic activity against Campylobacter jejuni. Food Control 2014; 44: 49-57.
17. Gonzalez-Fandos E, Maya N, Martínez-Laorden A, Perez-Arnedo I. Efficacy of lactic acid and modified atmosphere packaging against Campylobacter jejuni on chicken during refrigerated storage. Foods 2020; 9: 109.
18. Wang Y, Wu J, Lv M, Shao Z, Hungwe M, Wang J, et al. Metabolism characteristics of lactic acid bacteria and the expanding applications in food industry. Front Bioeng Biotechnol 2021; 9: 612285.
19. Wang Y, Han J, Wang D, Gao F, Zhang K, Tian J, et al. Research update on the impact of lactic acid bacteria on the substance metabolism, flavor, and quality characteristics of fermented meat products. Foods 2022; 11: 2090.
20. Reddy S, Zishiri OT. Genetic characterisation of virulence genes associated with adherence, invasion and cytotoxicity in Campylobacter spp. isolated from commercial chickens and human clinical cases. Onderstepoort J Vet Res 2018; 85(1): e1-e9.
21. de Oliveira MG, Rizzi C, Galli V, Lopes GV, Haubert L, Dellagostin OA, et al. Presence of genes associated with adhesion, invasion, and toxin production in Campylobacter jejuni isolates and effect of temperature on their expression. Can J Microbiol 2019; 65: 253-260.
22. Talukder KA, Aslam M, Islam Z, Azmi IJ, Dutta DK, Hossain S, et al. Prevalence of virulence genes and cytolethal distending toxin production in Campylobacter jejuni isolates from diarrheal patients in Bangladesh. J Clin Microbiol 2008; 46: 1485-1488.
23. Asakura H, Yamasaki M, Yamamoto S, Igimi S. Deletion of peb4 gene impairs cell adhesion and biofilm formation in Campylobacter jejuni. FEMS Microbiol Lett 2007; 275: 278-285.
24. Bai Y, Ding X, Zhao Q, Sun H, Li T, Li Z, et al. Development of an organic acid compound disinfectant to control food-borne pathogens and its application in chicken slaughterhouses. Poult Sci 2022; 101: 101842.
25. Silveira VAI, Nishio EK, Freitas CA, Amador IR, Kobayashi RK, Caretta T, et al. Production and antimicrobial activity of sophorolipid against Clostridium perfringens and Campylobacter jejuni and their additive interaction with lactic acid. Biocatal Agric Biotechnol 2019; 21: 101287.
26. Byun K-H, Na KW, Ashrafudoulla M, Choi MW, Han SH, Kang I, et al. Combination treatment of peroxyacetic acid or lactic acid with UV-C to control Salmonella Enteritidis biofilms on food contact surface and chicken skin. Food Microbiol 2022; 102: 103906.
27. Kraemer MVDS, Fernandes AC, Chaddad MCC, Uggioni PL, Rodrigues VM, Bernardo GL, et al. Food additives in childhood: a review on consumption and health consequences. Rev Saude Publica 2022; 56: 32.
28. Hosseini S, Abdollahzadeh E, Ranaei V, Mahmoudzadeh M, Pilevar Z. Effect of Zataria multiflora Boiss. essential oil, time, and temperature on the expression of Listeria monocytogenes virulence genes in broth and minced rainbow trout. Food Sci Nutr 2021; 9: 2290-2298.
29. de Souza EL, de Barros JC, da Conceição ML, Neto NJ, da Costa AC. Combined application of Origanum vulgare L. essential oil and acetic acid for controlling the growth of Staphylococcus aureus in foods. Braz J Microbiol 2009; 40: 387-393.
30. Abdollahzadeh E, Rezaei M, Hosseini H. Antibacterial activity of plant essential oils and extracts: The role of thyme essential oil, nisin, and their combination to control Listeria monocytogenes inoculated in minced fish meat. Food Control 2014; 35: 177-183.
31. Dasti JI, Tareen AM, Lugert R, Zautner AE, Groß U. Campylobacter jejuni: a brief overview on pathogenicity-associated factors and disease-mediating mechanisms. Int J Med Microbiol 2010; 300: 205-211.
32. Shyaka A, Kusumoto A, Chaisowwong W, Okouchi Y, Fukumoto S, Yoshimura A, et al. Virulence characterization of Campylobacter jejuni isolated from resident wild birds in Tokachi area, Japan. J Vet Med Sci 2015; 77: 967-972.
33. Klančnik A, Vučković D, Jamnik P, Abram M, Možina SS. Stress response and virulence of heat-stressed Campylobacter jejuni. Microbes Environ 2014; 29: 338-345.
34. Blevins RE, Kim SA, Park SH, Rivera R, Ricke SC (2018). Historical, current, and future prospects for food safety in poultry product processing systems. Food and feed safety systems and analysis: Elsevier. p. 323-345.
35. Kovács JK, Cox A, Schweitzer B, Maróti G, Kovács T, Fenyvesi H, et al. Virulence traits of inpatient Campylobacter jejuni isolates, and a transcriptomic approach to identify potential genes maintaining intracellular survival. Microorganisms 2020; 8: 531.
36. Kovács JK, Felső P, Makszin L, Pápai Z, Horváth G, Ábrahám H, et al. Antimicrobial and virulence-modulating effects of clove essential oil on the foodborne pathogen Campylobacter jejuni. Appl Environ Microbiol 2016; 82: 6158-6166.
37. Duodu S, Holst-Jensen A, Skjerdal T, Cappelier J-M, Pilet M-F, Loncarevic S. Influence of storage temperature on gene expression and virulence potential of Listeria monocytogenes strains grown in a salmon matrix. Food Microbiol 2010; 27: 795-801.
38. Habib I, Uyttendaele M, De Zutter L. Survival of poultry-derived Campylobacter jejuni of multilocus sequence type clonal complexes 21 and 45 under freeze, chill, oxidative, acid and heat stresses. Food Microbiol 2010; 27: 829-834.
39. Tiganitas A, Zeaki N, Gounadaki AS, Drosinos EH, Skandamis PN. Study of the effect of lethal and sublethal pH and aw stresses on the inactivation or growth of Listeria monocytogenes and Salmonella Typhimurium. Int J Food Microbiol 2009; 134: 104-112.
40. Hosseini S, Abdollahzadeh E, Ranaei V, Mahmoudzadeh M, Pilevar Z. Effect of Zataria multiflora Boiss. essential oil, NaCl, acid, time, and temperature on the growth of Listeria monocytogenes strains in broth and minced rainbow trout. Food Sci Nutr 2021; 9: 2290-2298.
41. Efimochkina NR, Bykova IB, Markova YM, Korotkevich YV, Sheveleva SA. The study of influence of stresses on virulence genes expression in foodborne pathogens Campylobacter jejuni. Vopr Pitan 2016; 85: 66-74.
42. Khalid MI, Tang JY, Baharuddin NH, Rahman NS, Rahimi NF, Radu S. Prevalence, antibiogram, and cdt genes of toxigenic Campylobacter jejuni in salad style vegetables (ulam) at farms and retail outlets in Terengganu. J Food Prot 2015; 78: 65-71.
43. Poli VF, Thorsen L, Olesen I, Wik MT, Jespersen L. Differentiation of the virulence potential of Campylobacter jejuni strains by use of gene transcription analysis and a Caco-2 assay. Int J Food Microbiol 2012; 155: 60-68.
44. Carrillo CD, Taboada E, Nash JH, Lanthier P, Kelly J, Lau PC, et al. Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA. J Biol Chem 2004; 279: 20327-20338.
| Files | ||
| Issue | Vol 16 No 4 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i4.16313 | |
| Keywords | ||
| Campylobacter jejuni; Colonization; Gene expression; Virulence factors | ||
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How to Cite
1.
Jadidi A, Ghasemian A, Abdollahi A, Abbasi-Dokht T, Abdollahzadeh E, Baharlou R. Effect of low concentrations of lactic acid and temperature on the expression of adhesion, invasion, and toxin-encoding genes of Campylobacter jejuni from poultry. Iran J Microbiol. 2024;16(4):536-544.
