Microcultures of lactic acid bacteria: characterization and selection of strains, optimization of nutrients and gallic acid concentration

  • Oswaldo Guzmán-López
  • Octavio Loera
  • José Luis Parada
  • Alberto Castillo-Morales
  • Cándida Martínez-Ramírez
  • Christopher Augur
  • Isabelle Gaime-Perraud
  • Gerardo Saucedo-Castañeda
Original Paper

Abstract

Eighteen lactic acid bacteria (LAB) strains, isolated from coffee pulp silages were characterized according to both growth and gallic acid (GA) consumption. Prussian blue method was adapted to 96-well microplates to quantify GA in LAB microcultures. Normalized data of growth and GA consumption were used to characterize strains into four phenotypes. A number of 5 LAB strains showed more than 60% of tolerance to GA at 2 g/l; whereas at 10 g/l GA growth inhibition was detected to a different extent depending on each strain, although GA consumption was observed in seven studied strains (>60%). Lactobacillus plantarum L-08 was selected for further studies based on its capacity to degrade GA at 10 g/l (97%). MRS broth and GA concentrations were varied to study the effect on growth of LAB. Cell density and growth rate were optimized by response surface methodology and kinetic analysis. Maximum growth was attained after 7.5 h of cultivation, with a dilution factor of 1–1/2 and a GA concentration between 0.625 and 2.5 g/l. Results indicated that the main factor affecting LAB growth was GA concentration. The main contribution of this study was to propose a novel adaptation of a methodology to characterize and select LAB strains with detoxifying potential of simple phenolics based on GA consumption and tolerance. In addition, the methodology presented in this study integrated the well-known RSM with an experimental design based on successive dilutions.

Keywords

Lactic acid bacteria Gallic acid Microculture Prussian blue method Response surface methodology 

Abbreviations

GA

Gallic acid

HPLC

High performance liquid chromatography

LAB

Lactic acid bacteria

MRS

Man Rogosa and Sharpe

OD

Optical density

PC

Phenolic compounds

RSM

Response surface methodology

X1

Dilution factor

X2

Gallic acid concentration

X1

Coded dilution factor, −log2(X1)

X2

Coded GA, −log2(X2/10)

Notes

Acknowledgments

The present work was performed as a part of the CONACYT Project #24715. O. Guzmán-López was awarded a PhD scholarship (#188180) from CONACyT, Mexico.

References

  1. 1.
    Alberto MR, Farías ME, Manca de Nadra MC (2001) Effect of gallic acid and catechin on Lactobacillus hilgardii 5w growth and metabolism of organic compounds. J Agric Food Chem 49:4359–4363. doi: 10.1021/jf0101915 PubMedCrossRefGoogle Scholar
  2. 2.
    Belén A, Egervärn M, Danielsen M, Tosi L, Morelli L, Lindaren S et al (2006) Susceptibility of Lactobacillus plantarum strains to six antibiotics and definition of new susceptibility-resistance cutoff values. Microb Drug Resist 12:252–256. doi: 10.1089/mdr.2006.12.252 CrossRefGoogle Scholar
  3. 3.
    Campos FM, Couto JA, Hogg TA (2003) Influence of phenolic acids on growth and inactivation of Oenococcus oeni and Lactobacillus hilgardii. J Appl Microbiol 94:167–174. doi: 10.1046/j.1365-2672.2003.01801.x PubMedCrossRefGoogle Scholar
  4. 4.
    Cavin JF, Andioc V, Etievant PX, Divies C (1993) Ability of wine lactic acid bacteria to metabolize phenol carboxylic acids. Am J Enol Vitic 44:76–80Google Scholar
  5. 5.
    De Man JC, Rogosa M, Sharpe ME (1960) A medium for the cultivation of Lactobacilli. J Appl Bact 23:130–135Google Scholar
  6. 6.
    Delgado A, Brito D, Peres C, Noé-Arroyo F, Garrido-Fernández A (2005) Bacteriocin production by Lactobacillus pentosus B96 can be expressed as a function of temperature and NaCl concentration. Food Microbiol 22:521–528. doi: 10.1016/j.fm.2004.11.015 CrossRefGoogle Scholar
  7. 7.
    Ely LO, Sudweeks EM, Moon NJ (1981) Inoculation with Lactobacillus plantarum of alfalfa, corn, sorghum and wheat silages. J Dairy Sci 64:2378–2387CrossRefGoogle Scholar
  8. 8.
    Gaime-Perraud I, Saucedo-Castañeda G, Augur C, Roussos S (2000) Adding value to coffee solid by-products through biotechnology. In: Sera T, Soccol CR, Pandey A, Roussos S (eds) Coffee biotechnology and quality. Kluwer, Dordrecht, pp 437–446Google Scholar
  9. 9.
    Gilarova R, Voldrich M, Demnerova K, Cerovsky K, Dobias J (1994) Cellular fatty acids analysis in the identification of lactic acid bacteria. Int J Food Microbiol 24:315–319. doi: 10.1016/0168-1605(94)90129-5 PubMedCrossRefGoogle Scholar
  10. 10.
    Graham H (1992) Stabilization of the Prussian blue color in the determination of polyphenols. J Agric Food Chem 40:801–805. doi: 10.1021/jf00017a018 CrossRefGoogle Scholar
  11. 11.
    Groenewald WH, Van Reenen CA, Todorov SD, Toit MD, Witthuhn RC, Holzapfel WH et al (2006) Identification of lactic acid bacteria from vinegar flies based on phenotypic and genotypic characteristics. Am J Enol Vitic 57:519–525Google Scholar
  12. 12.
    Horáková H, Greifová M, Seemannova Z, Gondová B, Wyatt GM (2004) A comparison of the traditional method of counting viable cells and a quick microplate method for monitoring the growth characteristics of Listeria monocytogenes. Lett Appl Microbiol 38:181–184. doi: 10.1111/j.1472-765X.2004.01448.x PubMedCrossRefGoogle Scholar
  13. 13.
    Klare I, Konstabel C, Müller-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. doi: 10.1128/AEM.71.12.8982-8986.2005 PubMedCrossRefGoogle Scholar
  14. 14.
    Koneman EW, Allen SD, Janda WM, Schreckenberger PC, Winn WC (1999) Color atlas and textbook of diagnostic microbiology, 7th edn. ASM Press, WashingtonGoogle Scholar
  15. 15.
    Makkar H (2003) Effects and fate of tannins in ruminant animals, adaptation to tannins, and strategies to overcome detrimental effects of feeding tanning-rich feeds. Small Rumin Res 49:241–256. doi: 10.1016/S0921-4488(03)00142-1 CrossRefGoogle Scholar
  16. 16.
    McDonnell G, Russell AD (1999) Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12:147–179PubMedGoogle Scholar
  17. 17.
    Montgomery DC (1991) Design and analysis of experiments, 3rd edn. Wiley, New YorkGoogle Scholar
  18. 18.
    Naczk M, Shahidi F (2004) Extraction and analysis of phenolics in food. J Chromatogr A 1054:95–111PubMedGoogle Scholar
  19. 19.
    Nelson KE, Thonney ML, Woolston TK, Zinder SH, Pell AN (1998) Phenotypic and phylogenetic characterization of ruminal tannin-tolerant bacteria. Appl Environ Microbiol 64:3824–3830PubMedGoogle Scholar
  20. 20.
    Odenyo AA, Bishop R, Asefa G, Jamnadass R, Odongo Osuji P (2001) Characterization of tannin-tolerant bacterial isolates from east african ruminants. Anaerobe 7:5–15. doi: 10.1006/anae.2000.0367 CrossRefGoogle Scholar
  21. 21.
    Osawa R, Kuroiso K, Goto Shimizu A (2000) Isolation of tannin-degrading Lactobacilli from humans and fermented foods. Appl Environ Microbiol 66:3093–3097. doi: 10.1128/AEM.66.7.3093-3097.2000 PubMedCrossRefGoogle Scholar
  22. 22.
    Osuga IM, Abdulrazak SA, Ichinohe T, Ondiek JO, Fujihara T (2006) Degradation characteristics and tannin bioassay of some browse forage from Kenya harvested during the dry season. Anim Sci J 77:414–421. doi: 10.1111/j.1740-0929.2006.00367.x CrossRefGoogle Scholar
  23. 23.
    Price ML, Butler LG (1977) Rapid visual estimation and spectrophotometric determination of the tannin content of sorghum grain. J Agric Food Chem 25:1269–1273. doi: 10.1021/jf60214a034 CrossRefGoogle Scholar
  24. 24.
    Reguant C, Bordons A, Arola L, Rozès N (2000) Influence of phenolic compounds Oenococcus oeni from wine. J Appl Microbiol 88:1065–1071. doi: 10.1046/j.1365-2672.2000.01075.x PubMedCrossRefGoogle Scholar
  25. 25.
    Rodrigues L, Teixeira J, Oliveira R, van der Mei HC (2006) Response surface optimization of the medium components for the production of biosurfactants by probiotic bacteria. Process Biochem 41:1–10. doi: 10.1016/j.procbio.2005.01.030 CrossRefGoogle Scholar
  26. 26.
    Roy A, Raychaudhury C, Nandy A (1998) Novel techniques of graphical representation and analysis of DNA sequences—a review. J Biosci 23:55–71. doi: 10.1007/BF02728525 CrossRefGoogle Scholar
  27. 27.
    Sabu A, Augur C, Swati C, Pandey A (2006) Tannase production by Lactobacillus sp. ASR-S1 under solid-state fermentation. Process Biochem 41:575–580. doi: 10.1016/j.procbio.2005.05.011 CrossRefGoogle Scholar
  28. 28.
    Saucedo-Castañeda G, Gómez J (1989) The effect of glucose and ammonium sulfate on kinetic acidification by heterogeneous mixed culture. Biotechnol Lett 2:121–124. doi: 10.1007/BF01192187 CrossRefGoogle Scholar
  29. 29.
    Schubert PF, Finn RK (1981) Alcohol precipitation of proteins: the relationship of denaturation and precipitation for catalase. Biotechnol Bioeng 23:2569–2590. doi: 10.1002/bit.260231114 CrossRefGoogle Scholar
  30. 30.
    Singleton V, Osthofer R, Lamuela-Raventos R (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagents. Methods Enzymol 299:152–178. doi: 10.1016/S0076-6879(99)99017-1 CrossRefGoogle Scholar
  31. 31.
    Stead D (1993) The effect of hydroxycinnamic acids on the growth of wine-spoilage lactic acid bacteria. J Appl Microbiol 75:135–141. doi: 10.1111/j.1365-2672.1993.tb02758.x CrossRefGoogle Scholar
  32. 32.
    Tor ER, Francis TM, Holstege DM, Galey FD (1996) GC/MS determination of pyrogallol and gallic acid in biological matrices as diagnostic indicators of oak exposure. J Agric Food Chem 44:1275–1279. doi: 10.1021/jf950238k CrossRefGoogle Scholar
  33. 33.
    Vaquero I, Marcobal Á, Muñoz R (2004) Tannase activity by lactic acid bacteria isolated from grape must and wine. Int J Food Microbiol 96:199–204. doi: 10.1016/j.ijfoodmicro.2004.04.004 PubMedCrossRefGoogle Scholar
  34. 34.
    Vivas N, Lonvaud-Funel A, Glories Y (1997) Effect of phenolic acids and anthocyanins on growth, viability and malolactic activity of a lactic acid bacterium. Food Microbiol 14:291–300. doi: 10.1006/fmic.1996.0086 CrossRefGoogle Scholar
  35. 35.
    Weinberg ZG, Muco RE, Weimer PJ, Chen Y, Gamburg M (2004) Lactic acid bacteria used in inoculants for silage as probiotics for ruminants. Appl Biochem Biotechnol 118:1–10. doi: 10.1385/ABAB:118:1-3:001 PubMedCrossRefGoogle Scholar

Copyright information

© Society for Industrial Microbiology 2008

Authors and Affiliations

  • Oswaldo Guzmán-López
    • 1
  • Octavio Loera
    • 1
  • José Luis Parada
    • 1
  • Alberto Castillo-Morales
    • 2
  • Cándida Martínez-Ramírez
    • 1
  • Christopher Augur
    • 3
  • Isabelle Gaime-Perraud
    • 3
  • Gerardo Saucedo-Castañeda
    • 1
  1. 1.Department of BiotechnologyMetropolitan Autonomous University (UAM), Campus IztapalapaMexico D.F.Mexico
  2. 2.Department of MathematicsMetropolitan Autonomous University (UAM), Campus IztapalapaMexico D.F.Mexico
  3. 3.IRD-Unité BioTransIMEP UMR IRD 193, Boîte 441, Faculty of Science and Technology St. Jérôme, Université Paul CézanneMarseille Cedex 20France

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