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Research article

Food Microbiology and Biotechnology(FMB)  |  Probiotics and Foodborne Microorganisms

Isolation and Characterization of Lactic Acid Bacteria from Fermented Goat Milk in Tajikistan

Gyu-Sung Cho 1, Claudia Cappello 2, Katrin Schrader 3, Olakunle Fagbemigum 4, Folarin A. Oguntoyinbo 4, 7, Claudia Csovcsics 5, Niels Rösch 1, Jan Kabisch 1, Horst Neve 1, Wilhelm Bockelmann 1, Karlis Briviba 5, Monica Modesto 2, Elisabetta Cilli 6, Paola Mattarelli 2 and Charles M.A.P. Franz 1*

1Max Rubner-Insititut, Federal Research Institute for Nutrition and Food, Department of Microbiology and Biotechnology, , 2Department of Agricultural Food Sciences, University of Bologna, Viale Fanin 42, I-40127 Bologna, Italy, 3Department of Safety and Quality of Milk and Fish Products, Hermann-Weigmann-Str. 1, D-24103 Kiel, Germany, 4Department of Microbiology, Faculty of Science, University of Lagos, Akoka, Lagos, Nigeria, 55Physiology and Biochemistry of Nutrition, Haid-und-Neu-Str. 9, D-76131 Karlsruhe, Germany, 6Department of Cultural Heritage, University of Bologna, Via degli Ariani 1, I-48121 Ravenna, Italy, 7A.R. Smith Department of Chemistry and Fermentation Sciences, Appalachian State University, Boone, NC 28608

Received: August 8, 2018; Accepted: October 16, 2018

J. Microbiol. Biotechnol. 2018; 28(11): 1834-1845

Published November 28, 2018 https://doi.org/10.4014/jmb.1807.08011

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

The lactobacilli associated with a fermented goat milk product from Tajikistan were isolated to characterize their technological properties and antibiotic resistances in order to assess their suitability for development as starter cultures. In this study, twenty three strains were identified by 16S rRNA sequencing as typical dairy-associated lactic acid bacterial strains, i.e. L. plantarum, L. pentosus, L. delbrueckii, L. helveticus and L. paracasei. These strains were generally susceptible to most antibiotics tested in this study and this allowed a selection of strains as safe starters. The draft genomes of four representative strains were sequenced and the number of contigs of the four assembled genomes ranged from 51 to 245 and the genome sizes ranged from 1.75 to 3.24 Mbp. These representative strains showed differences in their growth behavior and pH-reducing abilities in in vitro studies. The co-inoculation of these Lactobacillus spp. strains together with a yeast Kluyveromyces marxianus MBT-5698, or together with the yeast and an additional Streptococcus thermophilus MBT-2, led to a pH reduction to 3.4 after 48 h. Only in the case of fermentation inoculated with the co-culture, the viscosity of the milk increased noticeably. In contrast, fermentations with single strains did not lead to gelation of the milk or to a decrease in the pH after 24h. The results of this study provide a comprehensive understanding of the predominant lactobacilli related to Tajikistani fermented milk products.

Keywords

Lactic acid bacteria, fermentation, Lactobacillus, whole genome sequencing, milk

References

  1. Holzapfel WH. 2002. Appropriate starter culture technologies for small-scale fermentation in developing countries. Int. J. Food Microbiol. 75: 197-212.
    CrossRef
  2. Leroy F, De Vuyst L. 2004. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 15: 67-78.
    CrossRef
  3. Oguntoyinbo FA, Cho GS, Trierweiler B, Kabisch J , Rosch N, Neve H, et al. 2016. Fermentation of African kale (Brassica carinata) using L. plantarum BFE 5092 and L. fermentum BFE 6620 starter strains. Int. J. Food Microbiol. 238: 103-112.
    Pubmed CrossRef
  4. Tamang JP, Watanabe K, Holzapfel WH. 2016. Review:diversity of microorganisms in global fermented foods and beverages. Front Microbiol. 7: 377.
    Pubmed PMC CrossRef
  5. Blandino A, Al-Aseeri ME, Pandiella SS, Cantero D, Webb C. 2003. Cereal-based fermented foods and beverages. Food Res. Int. 36: 527-543.
    CrossRef
  6. Franz CMAP, Huch M, Mathara JM, Abriouel H, Benomar N, Reid G, et al. 2014. African fermented foods and probiotics. Int. J. Food Microbiol. 190: 84-96.
    Pubmed CrossRef
  7. Marsh AJ, O’Sullivan O, Hill C, Ross RP, Cotter PD. 2014. Sequence-based analysis of the bacterial and fungal compositions of multiple kombucha (tea fungus) samples. Food Microbiol. 38: 171-178.
    Pubmed CrossRef
  8. Qvirist LA, De Filippo C, Strati F, Stefanini I, Sordo M, Andlid T, et al. 2016. Isolation, identification and characterization of yeasts from fermented goat milk of the Yaghnob Valley in Tajikistan. Front Microbiol. 7: 1690.
    Pubmed PMC CrossRef
  9. Powers EM. 1995. Efficacy of the Ryu nonstaining KOH technique for rapidly determining gram reactions of foodborne and waterborne bacteria and yeasts. Appl. Environ. Microbiol. 61: 3756-3758.
    Pubmed PMC
  10. Mathara J M, Schillinger U , Kutima PM, Mbugua SK, Holzapfel WH. 2004. Isolation, identification and characterisation of the dominant microorganisms of kule naoto: the Maasai traditional fermented milk in Kenya. Int. J. Food Microbiol. 94: 269-278.
    Pubmed CrossRef
  11. Pitcher DG, Saunders NA, Owen RJ. 1989. Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett. Appl. Microbiol. 8: 151-156.
    CrossRef
  12. Bjorkroth J, Korkeala H. 1996. rRNA gene restriction patterns as a characterization tool for Lactobacillus sake strains producing ropy slime. Int. J. Food Microbiol. 30: 293-302.
    CrossRef
  13. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, et al. 2012. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62: 716-721.
    Pubmed CrossRef
  14. Yousif NM, Huch M, Schuster T, Cho G S, Dirar H A, Holzapfel WH, et al. 2010. Diversity of lactic acid bacteria from Hussuwa, a traditional African fermented sorghum food. Food Microbiol. 27: 757-768.
    Pubmed CrossRef
  15. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120.
    Pubmed PMC CrossRef
  16. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19: 455-477.
    Pubmed PMC CrossRef
  17. Gurevich A, Saveliev V, Vyahhi N, Tesler G. 2013. QUAST:quality assessment tool for genome assemblies. Bioinformatics 29: 1072-1075.
    Pubmed PMC CrossRef
  18. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genom. 9: 75.
    Pubmed PMC CrossRef
  19. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, et al. 2012. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67:2640-2644.
    Pubmed PMC CrossRef
  20. Carattoli A, Zankari E, Garcia-Fernandez A, Voldby Larsen M, Lund O, Villa L, et al. 2014. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58: 3895-3903.
    Pubmed PMC CrossRef
  21. Klare I , Konstabel C, Muller-Bertling S, Reissbrodt R, Huys G, Vancanneyt M, et al. 2005. Evaluation of new broth media for microdilution antibiotic susceptibility testing of Lactobacilli, Pediococci, Lactococci, and Bifidobacteria. Appl. Environ. Microbiol. 71: 8982-8986.
    CrossRef
  22. EFSA. 2012. Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J. 10: 1-10.
  23. Douillard FP, de Vos WM. 2014. Functional genomics of lactic acid bacteria: from food to health. Microb. Cell Fact. 13(Suppl 1): S8.
    Pubmed PMC CrossRef
  24. Dellaglio F, Felis GE, Castioni A, Torriani S, Germond JE. 2005. Lactobacillus delbrueckii subsp. indicus subsp. nov., isolated from Indian dairy products. Int. J. Syst. Evol. Microbiol. 55: 401-404.
    Pubmed CrossRef
  25. Adimpong DB, Nielsen DS, Sorensen KI, Vogensen FK, Sawadogo-Lingani H, Derkx PM, et al. 2013. Lactobacillus delbrueckii subsp. jakobsenii subsp. nov., isolated from dolo wort, an alcoholic fermented beverage in Burkina Faso. Int. J. Syst. Evol. Microbiol. 63: 3720-3726.
    Pubmed CrossRef
  26. Pot B, Felis GE, Bruyne KD, Tsakalidou E, Papadimitriou K, Leisner J, et al. 2014. The genus Lactobacillus, pp. 249-353. Lactic Acid Bacteria, Ed. John Wiley & Sons, Ltd,
  27. Torriani S, Felis GE, Dellaglio F. 2001. Differentiation of Lactobacillus plantarum, L. pentosus, and L. paraplantarum by recA gene sequence analysis and multiplex PCR assay with recA gene-derived primers. Appl. Environ. Microbiol. 67:3450-3454.
    Pubmed PMC CrossRef
  28. Kostinek M, Specht I, Edward VA, Schillinger U, Hertel C, Holzapfel WH, et al. 2005. Diversity and technological properties of predominant lactic acid bacteria from fermented cassava used for the preparation of Gari, a traditional African food. Syst. Appl. Microbiol. 28: 527-540.
    Pubmed CrossRef
  29. Bringel F, Curk MC, Hubert JC. 1996. Characterization of lactobacilli by Southern-type hybridization with a Lactobacillus plantarum pyrDFE probe. Int. J. Syst. Bacteriol. 46: 588-594.
    Pubmed CrossRef
  30. Naser SM, Hagen KE, Vancanneyt M, Cleenwerck I, Swings J, Tompkins TA. 2006. Lactobacillus suntoryeus Cachat and Priest 2005 is a later synonym of Lactobacillus helveticus (Orla-Jensen 1919) Bergey et al. 1925 (Approved Lists 1980). Int. J. Syst. Evol. Microbiol. 56: 355-360.
    Pubmed CrossRef
  31. Giraffa G. 2014. Lactobacillus helveticus: importance in food and health. Front Microbiol. 5: 338.
    Pubmed PMC CrossRef
  32. Sesena S, Sanchez I, Palop L. 2004. Genetic diversity (RAPDPCR) of lactobacilli isolated from “Almagro” eggplant fermentations from two seasons. FEMS Microbiol. Lett. 238:159-165.
    Pubmed CrossRef
  33. Griffiths MW, Tellez AM. 2013. Lactobacillus helveticus: the proteolytic system. Front Microbiol. 4: 30.
    Pubmed PMC CrossRef
  34. Slattery L, O’Callaghan J, Fitzgerald GF, Beresford T, Ross RP. 2010. Invited review: Lactobacillus helveticus--a thermophilic dairy starter related to gut bacteria. J. Dairy Sci. 93: 44354454.
    Pubmed CrossRef
  35. Settachaimongkon S, Nout MJ, Antunes Fernandes EC, Hettinga KA, Vervoort JM, van Hooijdonk TC, et al. 2014. Influence of different proteolytic strains of Streptococcus thermophilus in co-culture with Lactobacillus delbrueckii subsp. bulgaricus on the metabolite profile of set-yoghurt. Int. J. Food Microbiol. 177: 29-36.
    Pubmed CrossRef
  36. Plessas S, Bosnea L, Psarianos C, Koutinas AA, Marchant R, Banat IM. 2008. Lactic acid production by mixed cultures of Kluyveromyces marxianus, Lactobacillus delbrueckii ssp. bulgaricus and Lactobacillus helveticus. Bioresour. Technol. 99: 5951-5955.
    Pubmed CrossRef
  37. Devirgiliis C, Zinno P, Perozzi G. 2013. Update on antibiotic resistance in foodborne Lactobacillus and Lactococcus species. Front Microbiol. 4: 301.
    Pubmed PMC CrossRef
  38. Lin C F, Fung ZF, Wu CL, Chung T C. 1996. M olecular characterization of a plasmid-borne (pTC82) chloramphenicol resistance determinant (cat-TC) from Lactobacillus reuteri G4. Plasmid 36: 116-124.
    Pubmed CrossRef
  39. Cataloluk O, Gogebakan B. 2004. Presence of drug resistance in intestinal lactobacilli of dairy and human origin in Turkey. FEMS Microbiol. Lett. 236: 7-12.
    Pubmed CrossRef
  40. Huys G, D'Haene K, Collard JM, Swings J. 2004. P revalence and molecular characterization of tetracycline resistance in Enterococcus isolates from food. Appl. Environ. Microbiol. 70:1555-1562.
    Pubmed PMC CrossRef
  41. Huys G, D’Haene K, Swings J. 2006. Genetic basis of tetracycline and minocycline resistance in potentially probiotic Lactobacillus plantarum strain CCUG 43738. Antimicrob. Agents Chemother. 50: 1550-1551.
    Pubmed PMC CrossRef
  42. Temmerman R, Pot B, Huys G, Swings J. 2003. Identification and antibiotic susceptibility of bacterial isolates from probiotic products. Int. J. Food Microbiol. 81: 1-10.
    CrossRef
  43. Ammor MS, Florez AB, Mayo B. 2007. Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol. 24: 559-570.
    Pubmed CrossRef
  44. Hugenholtz J. 1993. Citrate metabolism in lactic acid bacteria. FEMS Microbiol. Rev. 12: 165-178.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2018; 28(11): 1834-1845

Published online November 28, 2018 https://doi.org/10.4014/jmb.1807.08011

Copyright © The Korean Society for Microbiology and Biotechnology.

Isolation and Characterization of Lactic Acid Bacteria from Fermented Goat Milk in Tajikistan

Gyu-Sung Cho 1, Claudia Cappello 2, Katrin Schrader 3, Olakunle Fagbemigum 4, Folarin A. Oguntoyinbo 4, 7, Claudia Csovcsics 5, Niels Rösch 1, Jan Kabisch 1, Horst Neve 1, Wilhelm Bockelmann 1, Karlis Briviba 5, Monica Modesto 2, Elisabetta Cilli 6, Paola Mattarelli 2 and Charles M.A.P. Franz 1*

1Max Rubner-Insititut, Federal Research Institute for Nutrition and Food, Department of Microbiology and Biotechnology, , 2Department of Agricultural Food Sciences, University of Bologna, Viale Fanin 42, I-40127 Bologna, Italy, 3Department of Safety and Quality of Milk and Fish Products, Hermann-Weigmann-Str. 1, D-24103 Kiel, Germany, 4Department of Microbiology, Faculty of Science, University of Lagos, Akoka, Lagos, Nigeria, 55Physiology and Biochemistry of Nutrition, Haid-und-Neu-Str. 9, D-76131 Karlsruhe, Germany, 6Department of Cultural Heritage, University of Bologna, Via degli Ariani 1, I-48121 Ravenna, Italy, 7A.R. Smith Department of Chemistry and Fermentation Sciences, Appalachian State University, Boone, NC 28608

Received: August 8, 2018; Accepted: October 16, 2018

Abstract

The lactobacilli associated with a fermented goat milk product from Tajikistan were isolated to
characterize their technological properties and antibiotic resistances in order to assess their
suitability for development as starter cultures. In this study, twenty three strains were
identified by 16S rRNA sequencing as typical dairy-associated lactic acid bacterial strains, i.e.
L. plantarum, L. pentosus, L. delbrueckii, L. helveticus and L. paracasei. These strains were
generally susceptible to most antibiotics tested in this study and this allowed a selection of
strains as safe starters. The draft genomes of four representative strains were sequenced and
the number of contigs of the four assembled genomes ranged from 51 to 245 and the genome
sizes ranged from 1.75 to 3.24 Mbp. These representative strains showed differences in their
growth behavior and pH-reducing abilities in in vitro studies. The co-inoculation of these
Lactobacillus spp. strains together with a yeast Kluyveromyces marxianus MBT-5698, or together
with the yeast and an additional Streptococcus thermophilus MBT-2, led to a pH reduction to 3.4
after 48 h. Only in the case of fermentation inoculated with the co-culture, the viscosity of the
milk increased noticeably. In contrast, fermentations with single strains did not lead to
gelation of the milk or to a decrease in the pH after 24h. The results of this study provide a
comprehensive understanding of the predominant lactobacilli related to Tajikistani fermented
milk products.

Keywords: Lactic acid bacteria, fermentation, Lactobacillus, whole genome sequencing, milk

References

  1. Holzapfel WH. 2002. Appropriate starter culture technologies for small-scale fermentation in developing countries. Int. J. Food Microbiol. 75: 197-212.
    CrossRef
  2. Leroy F, De Vuyst L. 2004. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 15: 67-78.
    CrossRef
  3. Oguntoyinbo FA, Cho GS, Trierweiler B, Kabisch J , Rosch N, Neve H, et al. 2016. Fermentation of African kale (Brassica carinata) using L. plantarum BFE 5092 and L. fermentum BFE 6620 starter strains. Int. J. Food Microbiol. 238: 103-112.
    Pubmed CrossRef
  4. Tamang JP, Watanabe K, Holzapfel WH. 2016. Review:diversity of microorganisms in global fermented foods and beverages. Front Microbiol. 7: 377.
    Pubmed KoreaMed CrossRef
  5. Blandino A, Al-Aseeri ME, Pandiella SS, Cantero D, Webb C. 2003. Cereal-based fermented foods and beverages. Food Res. Int. 36: 527-543.
    CrossRef
  6. Franz CMAP, Huch M, Mathara JM, Abriouel H, Benomar N, Reid G, et al. 2014. African fermented foods and probiotics. Int. J. Food Microbiol. 190: 84-96.
    Pubmed CrossRef
  7. Marsh AJ, O’Sullivan O, Hill C, Ross RP, Cotter PD. 2014. Sequence-based analysis of the bacterial and fungal compositions of multiple kombucha (tea fungus) samples. Food Microbiol. 38: 171-178.
    Pubmed CrossRef
  8. Qvirist LA, De Filippo C, Strati F, Stefanini I, Sordo M, Andlid T, et al. 2016. Isolation, identification and characterization of yeasts from fermented goat milk of the Yaghnob Valley in Tajikistan. Front Microbiol. 7: 1690.
    Pubmed KoreaMed CrossRef
  9. Powers EM. 1995. Efficacy of the Ryu nonstaining KOH technique for rapidly determining gram reactions of foodborne and waterborne bacteria and yeasts. Appl. Environ. Microbiol. 61: 3756-3758.
    Pubmed KoreaMed
  10. Mathara J M, Schillinger U , Kutima PM, Mbugua SK, Holzapfel WH. 2004. Isolation, identification and characterisation of the dominant microorganisms of kule naoto: the Maasai traditional fermented milk in Kenya. Int. J. Food Microbiol. 94: 269-278.
    Pubmed CrossRef
  11. Pitcher DG, Saunders NA, Owen RJ. 1989. Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett. Appl. Microbiol. 8: 151-156.
    CrossRef
  12. Bjorkroth J, Korkeala H. 1996. rRNA gene restriction patterns as a characterization tool for Lactobacillus sake strains producing ropy slime. Int. J. Food Microbiol. 30: 293-302.
    CrossRef
  13. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, et al. 2012. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62: 716-721.
    Pubmed CrossRef
  14. Yousif NM, Huch M, Schuster T, Cho G S, Dirar H A, Holzapfel WH, et al. 2010. Diversity of lactic acid bacteria from Hussuwa, a traditional African fermented sorghum food. Food Microbiol. 27: 757-768.
    Pubmed CrossRef
  15. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120.
    Pubmed KoreaMed CrossRef
  16. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19: 455-477.
    Pubmed KoreaMed CrossRef
  17. Gurevich A, Saveliev V, Vyahhi N, Tesler G. 2013. QUAST:quality assessment tool for genome assemblies. Bioinformatics 29: 1072-1075.
    Pubmed KoreaMed CrossRef
  18. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genom. 9: 75.
    Pubmed KoreaMed CrossRef
  19. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, et al. 2012. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67:2640-2644.
    Pubmed KoreaMed CrossRef
  20. Carattoli A, Zankari E, Garcia-Fernandez A, Voldby Larsen M, Lund O, Villa L, et al. 2014. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58: 3895-3903.
    Pubmed KoreaMed CrossRef
  21. Klare I , Konstabel C, Muller-Bertling S, Reissbrodt R, Huys G, Vancanneyt M, et al. 2005. Evaluation of new broth media for microdilution antibiotic susceptibility testing of Lactobacilli, Pediococci, Lactococci, and Bifidobacteria. Appl. Environ. Microbiol. 71: 8982-8986.
    CrossRef
  22. EFSA. 2012. Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J. 10: 1-10.
  23. Douillard FP, de Vos WM. 2014. Functional genomics of lactic acid bacteria: from food to health. Microb. Cell Fact. 13(Suppl 1): S8.
    Pubmed KoreaMed CrossRef
  24. Dellaglio F, Felis GE, Castioni A, Torriani S, Germond JE. 2005. Lactobacillus delbrueckii subsp. indicus subsp. nov., isolated from Indian dairy products. Int. J. Syst. Evol. Microbiol. 55: 401-404.
    Pubmed CrossRef
  25. Adimpong DB, Nielsen DS, Sorensen KI, Vogensen FK, Sawadogo-Lingani H, Derkx PM, et al. 2013. Lactobacillus delbrueckii subsp. jakobsenii subsp. nov., isolated from dolo wort, an alcoholic fermented beverage in Burkina Faso. Int. J. Syst. Evol. Microbiol. 63: 3720-3726.
    Pubmed CrossRef
  26. Pot B, Felis GE, Bruyne KD, Tsakalidou E, Papadimitriou K, Leisner J, et al. 2014. The genus Lactobacillus, pp. 249-353. Lactic Acid Bacteria, Ed. John Wiley & Sons, Ltd,
  27. Torriani S, Felis GE, Dellaglio F. 2001. Differentiation of Lactobacillus plantarum, L. pentosus, and L. paraplantarum by recA gene sequence analysis and multiplex PCR assay with recA gene-derived primers. Appl. Environ. Microbiol. 67:3450-3454.
    Pubmed KoreaMed CrossRef
  28. Kostinek M, Specht I, Edward VA, Schillinger U, Hertel C, Holzapfel WH, et al. 2005. Diversity and technological properties of predominant lactic acid bacteria from fermented cassava used for the preparation of Gari, a traditional African food. Syst. Appl. Microbiol. 28: 527-540.
    Pubmed CrossRef
  29. Bringel F, Curk MC, Hubert JC. 1996. Characterization of lactobacilli by Southern-type hybridization with a Lactobacillus plantarum pyrDFE probe. Int. J. Syst. Bacteriol. 46: 588-594.
    Pubmed CrossRef
  30. Naser SM, Hagen KE, Vancanneyt M, Cleenwerck I, Swings J, Tompkins TA. 2006. Lactobacillus suntoryeus Cachat and Priest 2005 is a later synonym of Lactobacillus helveticus (Orla-Jensen 1919) Bergey et al. 1925 (Approved Lists 1980). Int. J. Syst. Evol. Microbiol. 56: 355-360.
    Pubmed CrossRef
  31. Giraffa G. 2014. Lactobacillus helveticus: importance in food and health. Front Microbiol. 5: 338.
    Pubmed KoreaMed CrossRef
  32. Sesena S, Sanchez I, Palop L. 2004. Genetic diversity (RAPDPCR) of lactobacilli isolated from “Almagro” eggplant fermentations from two seasons. FEMS Microbiol. Lett. 238:159-165.
    Pubmed CrossRef
  33. Griffiths MW, Tellez AM. 2013. Lactobacillus helveticus: the proteolytic system. Front Microbiol. 4: 30.
    Pubmed KoreaMed CrossRef
  34. Slattery L, O’Callaghan J, Fitzgerald GF, Beresford T, Ross RP. 2010. Invited review: Lactobacillus helveticus--a thermophilic dairy starter related to gut bacteria. J. Dairy Sci. 93: 44354454.
    Pubmed CrossRef
  35. Settachaimongkon S, Nout MJ, Antunes Fernandes EC, Hettinga KA, Vervoort JM, van Hooijdonk TC, et al. 2014. Influence of different proteolytic strains of Streptococcus thermophilus in co-culture with Lactobacillus delbrueckii subsp. bulgaricus on the metabolite profile of set-yoghurt. Int. J. Food Microbiol. 177: 29-36.
    Pubmed CrossRef
  36. Plessas S, Bosnea L, Psarianos C, Koutinas AA, Marchant R, Banat IM. 2008. Lactic acid production by mixed cultures of Kluyveromyces marxianus, Lactobacillus delbrueckii ssp. bulgaricus and Lactobacillus helveticus. Bioresour. Technol. 99: 5951-5955.
    Pubmed CrossRef
  37. Devirgiliis C, Zinno P, Perozzi G. 2013. Update on antibiotic resistance in foodborne Lactobacillus and Lactococcus species. Front Microbiol. 4: 301.
    Pubmed KoreaMed CrossRef
  38. Lin C F, Fung ZF, Wu CL, Chung T C. 1996. M olecular characterization of a plasmid-borne (pTC82) chloramphenicol resistance determinant (cat-TC) from Lactobacillus reuteri G4. Plasmid 36: 116-124.
    Pubmed CrossRef
  39. Cataloluk O, Gogebakan B. 2004. Presence of drug resistance in intestinal lactobacilli of dairy and human origin in Turkey. FEMS Microbiol. Lett. 236: 7-12.
    Pubmed CrossRef
  40. Huys G, D'Haene K, Collard JM, Swings J. 2004. P revalence and molecular characterization of tetracycline resistance in Enterococcus isolates from food. Appl. Environ. Microbiol. 70:1555-1562.
    Pubmed KoreaMed CrossRef
  41. Huys G, D’Haene K, Swings J. 2006. Genetic basis of tetracycline and minocycline resistance in potentially probiotic Lactobacillus plantarum strain CCUG 43738. Antimicrob. Agents Chemother. 50: 1550-1551.
    Pubmed KoreaMed CrossRef
  42. Temmerman R, Pot B, Huys G, Swings J. 2003. Identification and antibiotic susceptibility of bacterial isolates from probiotic products. Int. J. Food Microbiol. 81: 1-10.
    CrossRef
  43. Ammor MS, Florez AB, Mayo B. 2007. Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol. 24: 559-570.
    Pubmed CrossRef
  44. Hugenholtz J. 1993. Citrate metabolism in lactic acid bacteria. FEMS Microbiol. Rev. 12: 165-178.
    CrossRef