Native chicken-derived Lactobacillus spp. strains with high probiotic, cholesterol-assimilation and aflatoxin-degradation capabilities
,
Abstract
Background and Objectives: Probiotics are added into the food or feed systems and provide beneficial effects to the human or animal health. This study aimed to isolate the gastrointestinal native Lactobacillus strains with high probiotic, cholesterol-assimilation and aflatoxin-degradation capabilities from native chickens.
Materials and Methods: About 70 Lactobacillus isolates were isolated from ileum of the Fars province native chickens and were investigated for their probiotic properties.
Results: Of 70 Lactobacillus isolates, 10 showed high probiotic capabilities, including survival at acidic conditions (pH up to 2.5), tolerance of 0.5% bile and 6-10% NaCl salts, growth in a wide range of temperature from 15 to 45°C, antagonistic effects against different important bacterial pathogens (Pseudomonas aeruginosa, Escherichia coli, Streptococcus mutans, Clostridium defficile, Enterococcus hirae, Salmonella enterica and Staphylococcus aureus) and sensitivity to some important antibiotics. The selected strains had an aggregation time less than 120 min. The 16S-rDNA sequencing showed that the selected strains were highly related to Lactobacillus reuteri and L. casei. Finally, the selected strains in this study along with 10 other probiotic strains isolated and characterized in our pervious study were used to evaluate their cholesterol assimilation and aflatoxin B1 degradation capabilities. The potentials of cholesterol assimilation of the selected strains were significantly different (P<0.05) and ranged from 2.3% to 99%. The highest content of cholesterol assimilation was obtained in isolates M20 and M4 with more than 98% absorption. Moreover, four strains 43, OR7, M21 and OR9 were able to absorb AFB1 with 58.6%, 52.33%, 47% and 31.6% efficiency respectively.
Conclusion: It could be concluded that the strains 43, M21 and OR7 showed high probiotic potentials for application in the poultry industry.
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7. Choi EA, Chang HC. Cholesterol-lowering effects of a putative probiotic strain Lactobacillus plantarum EM isolated from kimchi. LWT-Food Sci Technol 2015; 62:210-217.8.
8. Heenan CN, Adams MC, Hosken RW, Fleet GH. Survival and sensory acceptability of probiotic microorganisms in a nonfermented frozen vegetarian dessert. LWT-Food Sci Technol 2004; 37:461-466.
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12. Lim SY, Son YE, Lee DH, Eom TJ, Kim MJ, Park HS. Function of crzA in fungal development and aflatoxin production in Aspergillus flavus. Toxins (Basel) 2019;11:567.
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15. Wu Q, Jezkova A, Yuan Z, Pavlikova L, Dohnal V, Kuca K. Biological degradation of aflatoxins. Drug Metab Rev 2009; 41:1-7.
16. Petchkongkaew A, Taillandier P, Gasaluck P, Lebrihi A. Isolation of Bacillus spp. from Thai fermented soybean (Thua‐nao): screening for aflatoxin B1 and ochratoxin A detoxification. J Appl Microbiol 2008; 104:1495-1502.
17. Sezer Ç, Güven A, Oral NB, Vatansever L. Detoxification of aflatoxin B1 by bacteriocins and bacteriocinogenic lactic acid bacteria. Turk J Vet Anim Sci 2013; 37: 594-601.
18. Biglu MH, Ghavami M, Biglu S. Cardiovascular diseases in the mirror of science. J Cardiovasc Thorac Res 2016; 8:158-163.
19. Đokić B, Đonović N, Tadić B, Nikolić D. Factors and estimation of risk for cardiovascular diseases among patients in primary health care in central Serbia. Cent Eur J Public Health 2015; 23:195-199.
20. Costabile A, Buttarazzi I, Kolida S, Quercia S, Baldini J, Swann JR, et al. An in vivo assessment of the cholesterol-lowering efficacy of Lactobacillus plantarum ECGC 13110402 in normal to mildly hypercholesterolaemic adults. PLoS One 2017; 12: (12): e0187964.
21. Aazami N, Salehi Jouzani G, Khodaei Z, Meimandipour A, Safari M, Goudarzvand M . Characterization of some potentially probiotic Lactobacillus strains isolated from Iranian native chickens. J Gen Appl Microbiol 2014; 60:215-221.
22. Aazami N, Kalantar E, Poormazaheri H, Vali Pour NS, Salehi Jouzani G. Selection and characterization of potential probiotic Lactobacilli spp isolated from chicken feces may be used as a potent antibacterial agent. Asian J Dairy Food Res 2016; 35:50-57.
23. Kharazian ZA, Salehi Jouzani G, Aghdasi M, Khorvash M, Zamani M, Mohammadzadeh H. Biocontrol potential of Lactobacillus strains isolated from corn silages against some plant pathogenic fungi. Biol Control 2017; 110: 33-43.
24. Atashpaz S, Khani S, Barzegari A, Barar J, Vahed SZ, Azarbaijani R, Omidi Y. A robust universal method for extraction of genomic DNA from bacterial species. Mikrobiologiia 2010; 79: 562-566.
25. Miller CS, Handley KM, Wrighton KC, Frischkorn KR, Thomas BC, Banfield JF. Short-read assembly of full-length 16S amplicons reveals bacterial diversity in subsurface sediments. PLoS One 2013; 8(2): e56018.
26. Reniero R, Cocconcelli P, Bottazzi V, Morelli L. High frequency of conjugation in Lactobacillus mediated by an aggregation-promoting factor. J Gen Microbiol 1992; 138:763-768.
27. Liasi SA, Azmi TI, Hassan MD, Shuhaimi M, Rosfarizan M, Ariff AB. Antimicrobial activity and antibiotic sensitivity of three isolates of lactic acid bacteria from fermented fish product, Budu. Malays J Microbiol 2009; 5:33-37.
28. Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E. Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J 2006; 16:189-199.
29. Anandharaj M, Sivasankari B, Santhanakaruppu R, Manimaran M, Rani RP, Sivakumar S. Determining the probiotic potential of cholesterol-reducing Lactobacillus and Weissella strains isolated from gherkins (fermented cucumber) and south Indian fermented koozh. Res Microbiol 2015; 166: 428-439.
30. Shetty PH, Hald B, Jespersen L .Surface binding of aflatoxin B1 by Saccharomyces cerevisiae strains with potential decontaminating abilities in indigenous fermented foods. Int J Food Microbiol 2007; 113:41-46.
31. Reuben RC, Roy PC, Sarkar SL, Alam RU, Jahid IK. Isolation, characterization, and assessment of lactic acid bacteria toward their selection as poultry probiotics. BMC Microbiol 2019; 19: 253.
32. Terpou A, Papadaki A, Lappa IK, Kachrimanidou V, Bosnea LA, Kopsahelis N. Probiotics in food systems: significance and emerging strategies towards improved viability and delivery of enhanced beneficial value. Nutrients 2019; 11:1591.
33. Sharma C, Singh BP, Thakur N, Gulati S, Gupta S, Mishra SK, Panwar H. Antibacterial effects of Lactobacillus isolates of curd and human milk origin against food-borne and human pathogens. 3 Biotech 2017; 7:31.
34. Karimi S, Azizi F, Nayeb-Aghaee M, Mahmoodnia L. The antimicrobial activity of probiotic bacteria Escherichia coli isolated from different natural sources against hemorrhagic E. coli O157: H7. Electron Physician 2018; 10:6548-6553.
35. Kizerwetter-Swida M, Binek M. Selection of potentially probiotic Lactobacillus strains towards their inhibitory activity against poultry enteropathogenic bacteria. Pol J Microbiol 2005; 54: 287-294.
36. Reuben RC, Roy PC, Sarkar SL, Alam RU, Jahid IK. Isolation, characterization, and assessment of lactic acid bacteria toward their selection as poultry probiotics. BMC Microbiol 2019; 19: 253.
37. Peltonen KD, El‐Nezami HS, Salminen SJ, Ahokas JT. Binding of aflatoxin B1 by probiotic bacteria. J Sci Food Agric 2000; 80:1942-1945.
38. Wang CY, Wu SC, Ng CC, Shyu YT . Effect of Lactobacillus-fermented adlay-based milk on lipid metabolism of hamsters fed cholesterol-enriched diet. Food Res Int 2010; 43:819-824.
39. Getachew T. A review on effects of probiotic supplementation in poultry performance and cholesterol levels of egg and meat. J World's Poult Res 2016; 6:31-36.
2. Isolauri E, Kirjavainen PV, Salminen S. Probiotics: a role in the treatment of intestinal infection and inflammation? Gut 2002; 50 Suppl 3(Suppl 3): III54-9.
3. Holzapfel WH, Haberer P, Geisen R, Björkroth J, Schillinger U. Taxonomy and important features of probiotic microorganisms in food and nutrition. Am J Clin Nutr 2001;73 (2 Suppl):365S-373S.
4. Florou-Paneri P, Christaki E, Bonos E (2013). Lactic acid bacteria as source of functional ingredients. In: Lactic acid bacteria-R & D for food, health and livestock purposes. Ed, M Kongo. IntechOpen publishing, 1st ed. Rijeka, Croatia, pp. 589-614.
5. Kechagia M, Basoulis D, Konstantopoulou S, Dimitriadi D, Gyftopoulou K, Skarmoutsou N, et al. Health benefits of probiotics: a review. ISRN Nutr 2013; 2013: 481651.
6. Asahara T, Shimizu K, Nomoto K, Hamabata T, Ozawa A, Takeda Y. Probiotic bifidobacteria protect mice from lethal infection with Shiga toxin-producing Escherichia coli O157: H7. Infect Immun 2004; 72:2240-2247.
7. Choi EA, Chang HC. Cholesterol-lowering effects of a putative probiotic strain Lactobacillus plantarum EM isolated from kimchi. LWT-Food Sci Technol 2015; 62:210-217.8.
8. Heenan CN, Adams MC, Hosken RW, Fleet GH. Survival and sensory acceptability of probiotic microorganisms in a nonfermented frozen vegetarian dessert. LWT-Food Sci Technol 2004; 37:461-466.
9. Bermudez-Brito M, Plaza-Díaz J, Munoz-Quezada S, Gomez-Llorente C, Gil A. Probiotic mechanisms of action. Ann Nutr Metab 2012; 61:160-174.
10. Eslami M, Bahar A, Keikha M, Karbalaei M, Kobyliak NM, Yousefi B. Probiotics function and modulation of the immune system in allergic diseases. Allergol Immunopathol (Madr) 2020; 48: 771-788.
11. Topcu A, Bulat T, Wishah R, Boyacı IH. Detoxification of aflatoxin B1 and patulin by Enterococcus faecium strains. Int J Food Microbiol 2010; 139:202-205.
12. Lim SY, Son YE, Lee DH, Eom TJ, Kim MJ, Park HS. Function of crzA in fungal development and aflatoxin production in Aspergillus flavus. Toxins (Basel) 2019;11:567.
13. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. IARC Monogr Eval Carcinog Risks Hum 2002; 82:1-556.
14. Marchese S, Polo A, Ariano A, Velotto S, Costantini S, Severino L. Aflatoxin B1 and M1: Biological properties and their involvement in cancer development. Toxins (Basel) 2018; 10: 214.
15. Wu Q, Jezkova A, Yuan Z, Pavlikova L, Dohnal V, Kuca K. Biological degradation of aflatoxins. Drug Metab Rev 2009; 41:1-7.
16. Petchkongkaew A, Taillandier P, Gasaluck P, Lebrihi A. Isolation of Bacillus spp. from Thai fermented soybean (Thua‐nao): screening for aflatoxin B1 and ochratoxin A detoxification. J Appl Microbiol 2008; 104:1495-1502.
17. Sezer Ç, Güven A, Oral NB, Vatansever L. Detoxification of aflatoxin B1 by bacteriocins and bacteriocinogenic lactic acid bacteria. Turk J Vet Anim Sci 2013; 37: 594-601.
18. Biglu MH, Ghavami M, Biglu S. Cardiovascular diseases in the mirror of science. J Cardiovasc Thorac Res 2016; 8:158-163.
19. Đokić B, Đonović N, Tadić B, Nikolić D. Factors and estimation of risk for cardiovascular diseases among patients in primary health care in central Serbia. Cent Eur J Public Health 2015; 23:195-199.
20. Costabile A, Buttarazzi I, Kolida S, Quercia S, Baldini J, Swann JR, et al. An in vivo assessment of the cholesterol-lowering efficacy of Lactobacillus plantarum ECGC 13110402 in normal to mildly hypercholesterolaemic adults. PLoS One 2017; 12: (12): e0187964.
21. Aazami N, Salehi Jouzani G, Khodaei Z, Meimandipour A, Safari M, Goudarzvand M . Characterization of some potentially probiotic Lactobacillus strains isolated from Iranian native chickens. J Gen Appl Microbiol 2014; 60:215-221.
22. Aazami N, Kalantar E, Poormazaheri H, Vali Pour NS, Salehi Jouzani G. Selection and characterization of potential probiotic Lactobacilli spp isolated from chicken feces may be used as a potent antibacterial agent. Asian J Dairy Food Res 2016; 35:50-57.
23. Kharazian ZA, Salehi Jouzani G, Aghdasi M, Khorvash M, Zamani M, Mohammadzadeh H. Biocontrol potential of Lactobacillus strains isolated from corn silages against some plant pathogenic fungi. Biol Control 2017; 110: 33-43.
24. Atashpaz S, Khani S, Barzegari A, Barar J, Vahed SZ, Azarbaijani R, Omidi Y. A robust universal method for extraction of genomic DNA from bacterial species. Mikrobiologiia 2010; 79: 562-566.
25. Miller CS, Handley KM, Wrighton KC, Frischkorn KR, Thomas BC, Banfield JF. Short-read assembly of full-length 16S amplicons reveals bacterial diversity in subsurface sediments. PLoS One 2013; 8(2): e56018.
26. Reniero R, Cocconcelli P, Bottazzi V, Morelli L. High frequency of conjugation in Lactobacillus mediated by an aggregation-promoting factor. J Gen Microbiol 1992; 138:763-768.
27. Liasi SA, Azmi TI, Hassan MD, Shuhaimi M, Rosfarizan M, Ariff AB. Antimicrobial activity and antibiotic sensitivity of three isolates of lactic acid bacteria from fermented fish product, Budu. Malays J Microbiol 2009; 5:33-37.
28. Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E. Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J 2006; 16:189-199.
29. Anandharaj M, Sivasankari B, Santhanakaruppu R, Manimaran M, Rani RP, Sivakumar S. Determining the probiotic potential of cholesterol-reducing Lactobacillus and Weissella strains isolated from gherkins (fermented cucumber) and south Indian fermented koozh. Res Microbiol 2015; 166: 428-439.
30. Shetty PH, Hald B, Jespersen L .Surface binding of aflatoxin B1 by Saccharomyces cerevisiae strains with potential decontaminating abilities in indigenous fermented foods. Int J Food Microbiol 2007; 113:41-46.
31. Reuben RC, Roy PC, Sarkar SL, Alam RU, Jahid IK. Isolation, characterization, and assessment of lactic acid bacteria toward their selection as poultry probiotics. BMC Microbiol 2019; 19: 253.
32. Terpou A, Papadaki A, Lappa IK, Kachrimanidou V, Bosnea LA, Kopsahelis N. Probiotics in food systems: significance and emerging strategies towards improved viability and delivery of enhanced beneficial value. Nutrients 2019; 11:1591.
33. Sharma C, Singh BP, Thakur N, Gulati S, Gupta S, Mishra SK, Panwar H. Antibacterial effects of Lactobacillus isolates of curd and human milk origin against food-borne and human pathogens. 3 Biotech 2017; 7:31.
34. Karimi S, Azizi F, Nayeb-Aghaee M, Mahmoodnia L. The antimicrobial activity of probiotic bacteria Escherichia coli isolated from different natural sources against hemorrhagic E. coli O157: H7. Electron Physician 2018; 10:6548-6553.
35. Kizerwetter-Swida M, Binek M. Selection of potentially probiotic Lactobacillus strains towards their inhibitory activity against poultry enteropathogenic bacteria. Pol J Microbiol 2005; 54: 287-294.
36. Reuben RC, Roy PC, Sarkar SL, Alam RU, Jahid IK. Isolation, characterization, and assessment of lactic acid bacteria toward their selection as poultry probiotics. BMC Microbiol 2019; 19: 253.
37. Peltonen KD, El‐Nezami HS, Salminen SJ, Ahokas JT. Binding of aflatoxin B1 by probiotic bacteria. J Sci Food Agric 2000; 80:1942-1945.
38. Wang CY, Wu SC, Ng CC, Shyu YT . Effect of Lactobacillus-fermented adlay-based milk on lipid metabolism of hamsters fed cholesterol-enriched diet. Food Res Int 2010; 43:819-824.
39. Getachew T. A review on effects of probiotic supplementation in poultry performance and cholesterol levels of egg and meat. J World's Poult Res 2016; 6:31-36.
| Files | ||
| Issue | Vol 14 No 2 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i2.9192 | |
| Keywords | ||
| Probiotics; Aflatoxin B1; Cholesterol; Lactobacillus reuteri; Lactobacillus casei; Poultry | ||
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How to Cite
1.
Amir Ebrahimi N, Salehi Jouzani G, Ebrahimi MA. Native chicken-derived Lactobacillus spp. strains with high probiotic, cholesterol-assimilation and aflatoxin-degradation capabilities. Iran J Microbiol. 2022;14(2):227-237.
