Role of lactic acid bacteria in fermented vegetables

  1. Bautista-Gallego, J. 1
  2. Medina, E. 1
  3. Sánchez, B. 2
  4. Benítez-Cabello, A. 1
  5. Arroyo-López, F. N. 1
  1. 1 Food Biotechnology Department. Instituto de la Grasa (CSIC), Spain
  2. 2 MicroHealth Group. IPLA (CSIC), Spain
Revista:
Grasas y aceites

ISSN: 0017-3495,  1988-4214

Año de publicación: 2020

Volumen: 71

Número: 2

Tipo: Artículo

DOI: 10.3989/GYA.0344191 DIALNET GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Grasas y aceites

Objetivos de desarrollo sostenible

Resumen

El consumo de vegetales fermenta­dos está muy extendido en el mundo y representa un componente importante de la dieta humana con un apoyo considerable a la cadena alimentaria para una población mundial en continuo crecimiento. Muchos de los vege­tales fermentados comparten un proceso general, que requiere una puesta en salmuera y acidificación. Entre los microorganismos responsables de la fermentación, las bacterias del ácido láctico son las más relevantes con una importante influencia sobre aspectos organolépticos, de calidad y seguridad del producto final. Esta revisión trata sobre la ecología microbiana de los vegetales fermentados, prestando especial atención a la biodiversidad de las bacterias del ácido láctico, las técnicas moleculares más importantes utilizadas para su identificación y genotipado, su importancia para la formación de biofilms y su uso como cultivos iniciadores multifuncionales para la obtención de productos vegetales de alta calidad y seguridad.

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Información de financiación

AB-C and JB-G thank the Spanish Ministry of Economy and Competitiveness for their FPI grant and JDC-Incorp. contracts, respectively.

Financiadores

Referencias bibliográficas

  • Abriouel H, Benomar N, Cobo A, Caballero N, Fernández-Fuentes MÁ, Pérez-Pulido R, Gálvez A. 2012. Characterization of lactic acid bacteria from naturally-fermented Manzanilla Aloreña green table olives. Food Microbiol. 32, 308–316.
  • Abriouel H, Benomar N, Lucas R, Gálvez A. 2011. Culture-independent study of the diversity of microbial populations in brines during fermentation of naturally-fermented Aloreña green table olives. Int. J. Food Microbiol. 144, 487–496.
  • Ampe F, ben Omar N, Moizan C, Wacher C, Guyot JP. 1999. Polyphasic study of the spatial distribution of microorganisms in Mexican pozol, a fermented maize dough, demonstrates the need for cultivation-independent methods to investigate traditional fermentations. Appl. Environ. Microbiol. 65, 5464–5473
  • Andersson RE, Daeschel MA, Eriksson CE. 1988. Controlled lactic acid fermentation of vegetables. In Proceedings: 8th International Biotechnology Symposium, Paris 1988/edited by G. Durand, L. Bobichon, J. Florent. [Paris, France]: Societe francaise de microbiologie, c1988.
  • Aponte M, Blaiotta G, Croce FL, Mazzaglia A, Farina, V, Settanni L, Moschetti G. 2012. Use of selected autochthonous lactic acid bacteria for Spanish-style table olive fermentation. Food Microbiol. 30, 8–16.
  • Argyri AA, Zoumpopoulou G, Karatzas KA, Tsakalidou E, Nychas GJ, Panagou EZ, Tassou CC. 2013. Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol. 33, 282–291.
  • Arroyo-López FN, Querol A, Bautista-Gallego J, Garrido-Fernández A. 2008. Role of yeasts in table olive production. Int. J. Food Microbiol. 128, 189–196.
  • Arroyo-López FN, Bautista-Gallego J, Domínguez-Manzano J, Romero-Gil V, Rodríguez-Gómez F, García-García P, Garrido-Fernández A, Jiménez-Díaz R. 2012a. Formation of lactic acid bacteria-yeasts communities on the olive surface during Spanish-style Manzanilla fermentations. Food Microbiol. 32, 295–301.
  • Arroyo-López FN, Romero-Gil V, Bautista-Gallego J, Rodríguez-Gómez F, Jiménez-Díaz R, García-García P, Querol A, Garrido-Fernández A. 2012b. Yeasts in table olive processing: desirable or spoilage microorganisms? Int. J. Food Microbiol. 160, 42–49.
  • Arroyo-López FN, Blanquet-Diot S, Denis S, Thévenot J, Chalancon S, Alric, M, Rodríguez-Gómez F, Romero-Gil V, Jiménez Díaz R, Garrido-Fernández A. 2014. Survival of pathogenic and lactobacilli species of fermented olives during simulated human digestion. Front. Microbiol. 5, 540.
  • Babuchowsk A, Laniewska-Moroz L, Warminska-Radyko I. 1999. Propionibacteria in fermented vegetables. Lait 79, 113–124.
  • Bautista-Gallego J, Arroyo-López FN, Rantsiou K, Jiménez-Díaz R, Garrido-Fernández A, Cocolin LS. 2013. Screening of lactic acid bacteria isolated from fermented table olives with probiotic potential. Food Res. Int. 50, 135–142.
  • Bellis P de, Valerio F, Sisto A, Lonigro SL, Lavermicocca P. 2010. Probiotic table olives: microbial populations adhering on olive surface in fermentation sets inoculated with the probiotic strain Lactobacillus paracasei IMPC2.1 in an industrial plant. Int. J. Food Microbiol. 140, 6–13.
  • Benítez-Cabello A, Bautista-Gallego J, Garrido-Fernández A, Rantsiou K, Cocolin L, Jiménez-Díaz R, Arroyo-López FN. 2016. RT-PCR–DGGE Analysis to Elucidate the Dominant Bacterial Species of Industrial Spanish-Style Green Table Olive Fermentations. Front Microbiol. 7, 1291.
  • Benítez-Cabello A, Calero-Delgado B, Rodríguez-Gómez F, Garrido-Fernández A, Jiménez-Díaz R, Arroyo-López FN. 2019. Biodiversity and multifunctional features of lactic acid bacteria isolated from table olive biofilms. Front. Microbiol. 10 (3), Art 836.
  • Botta C, Cocolin L. 2012. Microbial dynamics and biodiversity in table olive fermentation: culture-dependent and -independent approaches. Front Microbiol. 3, 245.
  • Botta C, Langerholc T, Cencič A, Cocolin L. 2014. In vitro selection and characterization of new probiotic candidates from table olive microbiota. Plos One. 9 (4).
  • Breidt F, Medina E, Wafa D, Pérez-Díaz I, Franco W, Huang, HY, Johanningsmeier SD, Kim JH. 2013a. Characterization of cucumber fermentation spoilage bacteria by enrichment culture and 16S rDNA cloning. J. Food Sci. 78, M470–476.
  • Breidt F, McFeeters RF, Perez-Diaz I, Lee C. 2013b. Fermented vegetables. Ch. 33 in Doyle and Buchanan, Food Microbiology: Fundamentals and Frontiers, ASM Press.
  • Cagno R di, Coda R, De Angelis M, Gobbetti M. 2013. Exploitation of vegetables and fruits through lactic acid fermentation. Food Microbiol. 33, 1–10.
  • Castro A de, Rejano L, Sánchez AH, Montaño A. 1995. Fermentation of lye-treated carrots by Lactobacillus plantarum. J. Food Sci. 60, 316–319.
  • Castro A de, Sánchez AH, López-López A, Cortés-Delgado A, Medina E, Montaño A. 2018. Microbiota and Metabolite Profiling of Spoiled Spanish-Style Green Table Olives. Metabolites 8, 73.
  • Cocolin L, Ercolini D. 2007. Molecular techniques in the microbial ecology of fermented foods, Springer Science & Business Media.
  • Corsetti A, Perpetuini G, Schirone M, Tofalo R, Suzzi G. 2012. Application of starter cultures to table olive fermentation: an overview on the experimental studies. Front Microbiol. 3.
  • Costilow RN, Gates K, Lacy ML. 1980. Molds in brined cucumbers: cause of softening during air-purging of fermentations. Appl. Environ. Microbiol. 40, 417–422.
  • Domínguez-Manzano J, Olmo-Ruiz C, Bautista-Gallego J, Arroyo-López FN, Garrido-Fernández, A, Jiménez-Díaz R. 2012. Biofilm formation on abiotic and biotic surfaces during Spanish style green table olive fermentation. Int. J. Food Microbiol. 157, 230–238.
  • Elmacı SB, Tokatlı M, Dursun D, Özçelik F, Şanlıbaba P. 2015. Phenotypic and genotypic identification of lactic acid bacteria isolated from traditional pickles of the Çubuk region in Turkey. Folia Microbiol. 60, 241–251.
  • Etchells JL, Bell TA. 1950. Classification of yeasts from the fermentation of commercially brined cucumbers. Farlowia 4, 87–112.
  • Etchells JL, Jones ID. 1943. Bacteriological changes in cucumber fermentation. Food Industries 15, 54–56.
  • Ferrocino I, Cocolin L. 2017. Current perspectives in food-based studies exploiting multi-omics approaches. Curr. Opin. Food Sci. 13, 10–15.
  • Fleming HP, Etchells JL, Thompson RL, Bell TA. 1975. Purging of Co2 from Cucumber Brines to Reduce Bloater Damage. J. Food.Sci. 40, 1304–1310.
  • Franco W, Pérez-Díaz IM. 2013. Microbial interactions associated with secondary cucumber fermentation. J. Appl. Microbiol. 114, 161–172.
  • Franco W, Pérez-Díaz IM, Johanningsmeier SD, McFeeters RF. 2012. Characteristics of Spoilage-Associated Secondary Cucumber Fermentation. Appl. Environ Microbiol. 78, 1273–1284.
  • Franzetti L, Scarpellini M, Vecchio A, Planeta D. 2011. Microbiological and safety evaluation of green table olives marketed in Italy. Ann. Microbiol. 61, 843–851.
  • Garrido-Fernández A, Adams MR, Fernández-Díez MJ. 1997. Table olives: production and processing, Springer Science & Business Media.
  • Gebbers JO. 2007. Atherosclerosis, cholesterol, nutrition, and statins–a critical review. GMS Ger. Med. Sci. 5, 4.
  • Gililland JR, Vaughn RH. 1943. Characteristics of butyric acid bacteria from olives. J. Bacteriol. 46, 315.
  • González-Cancho F, Rejano-Navarro L, Rodríguez de la Borbolla, Alcalá JM. 1980. Formation of propionic acid during the conservation of table green olives, 3: Responsible microorganisms. Grasas Aceites 31, 245–250.
  • González-Ortiz G, Pérez JF, Gustavo-Hermes R, Molist F, Jiménez-Díaz R, Martín-Orue S. 2013. Screening the ability of natural feed ingredients to interfere with the adherence of enterotoxigenic Escherichia coli (ETEC) K88 to the porcine intestinal mucus. British J. Nutr. 111, 633–642.
  • Granato D, Branco GF, Nazzaro F, Cruz AG, Faria JA. 2010. Functional foods and nondairy probiotic food development: trends, concepts, and products. Compr. Rev. Food Sci. Food Saf. 9 (3), 292–302.
  • Hernández A, Martín A, Aranda E, Pérez-Nevado F, Córdoba MG. 2007. Identification and characterization of yeast isolated from the elaboration of seasoned green table olives. Food Microbiol. 24, 346–351.
  • Hong Y, Li J, Qin P, Lee SY, Kim HY. 2015. Predominant lactic acid bacteria in mukeunji, a long-term-aged kimchi, for different aging periods. Food Sci. Biotechnol. 24, 545–550.
  • Hurtado A, Reguant C, Bordons A, Rozès N. 2012. Lactic acid bacteria from fermented table olives. Food Microbiol. 31, 1–8.
  • Jang S, Lee J, Jung U, Choi HS, Suh HJ. 2014. Identification of an anti-listerial domain from Pediococcus pentosaceus T1 derived from Kimchi, a traditional fermented vegetable. Food Control 43, 42–48.
  • Ji K, Jang NY, Kim YT. 2015. Isolation of Lactic Acid Bacteria Showing Antioxidative and Probiotic Activities from Kimchi and Infant Feces. J. Microbiol. Biotechnol. 25, 1568–1577.
  • Johanningsmeier S, McFeeters RF, Fleming HP, Thompson RL. 2007. Effects of Leuconostoc mesenteroides starter culture on fermentation of cabbage with reduced salt concentrations. J. Food Sci. 72, M166–172.
  • Johanningsmeier SD, McFeeters RF. 2013. Metabolism of lactic acid in fermented cucumbers by Lactobacillus buchneri and related species, potential spoilage organisms in reduced salt fermentations. Food Microbiol. 35, 129–135.
  • Jung JY, Lee SH, Jin HM, Hahn Y, Madsen EL, Jeon CO. 2013. Metatranscriptomic analysis of lactic acid bacterial gene expression during kimchi fermentation. Int. J. Food Microbiol. 163, 171–179.
  • Kawatomari T, Vaughn RH. 1956. Species of Clostridium associated with zapatera spoilages. J. Food Sci. 21, 481–490.
  • Kim E, Cho Y, Lee Y, Han SK, Kim CG, Choo DW, Kim YR, Kim HY. 2017. A proteomic approach for rapid identification of Weissella species isolated from Korean fermented foods on MALDI-TOF MS supplemented with an in-house database. Int. J. Food Microbiol. 243, 9–15.
  • Kyung KH, Medina E, Kim SG, Lee YJ, Kim KH, Choi JJ, Cho JH, Chung CH, Barrangou R, Breidt F. 2015. Microbial Ecology of Watery Kimchi. Food Control 80, M1031–8.
  • Lavermicocca P, Valerio F, Lonigro SL, Angelis MD, Morelli L, Callegari ML, Rizzello CG, Visconti A. 2005. Study of Adhesion and Survival of Lactobacilli and Bifidobacteria on Table Olives with the Aim of Formulating a New Probiotic Food. Appl. Environ. Microbiol. 71, 4233–4240.
  • Lee JS, Heo GY, Lee JW, Oh YJ, Park JA Park YH, Pyun YR, Ahn JS. 2005. Analysis of kimchi microflora using denaturing gradient gel electrophoresis. Int. J. Food Microbiol. 102, 143–150.
  • Lee ME, Jang JY, Lee JH, Park HW, Choi HJ, Kim TW. 2015. Starter cultures for kimchi fermentation. J. Microbiol. Biotechnol. 25, 559–568.
  • León-Romero Á, Domínguez-Manzano J, Garrido-Fernández A, Arroyo-López FN, Jiménez-Díaz R. 2016. Formation of in vitro mixed-species biofilms by Lactobacillus pentosus and yeasts isolated from Spanish-style green table olive Fermentations. Appl. Environ. Microbiol. 82, 689–695.
  • Lucena-Padrós H, Caballero-Guerrero B, Maldonado-Barragán A, Ruiz Barba JL. 2014. Microbial diversity and dynamics of Spanish-style green table-olive fermentations in large manufacturing companies through culture-dependent Techniques. Food Microbiol. 42, 154–165.
  • Lucena-Padrós H, Jiménez E, Maldonado-Barragán M, Rodriguez JM, Ruiz-Barba JL. 2015. PCR-DGGE assessment of the bacterial diversity in Spanish-style green table olive fermentations. Int. J. Food Microbiol. 205, 47–53.
  • Luke FK. 1996. Lactic acid bacteria involved in food fermentations and their present and future uses in food industry. Lactic Acid Bacteria: Current Advances in Metabolism, Genetics and Applications. Vol. H98. Ed. Faruk Bozoglu and Bibek Ray. Springer-Verlag Berlin Heidelberg.
  • Mattos FR, Fasina OO, Reina LD, Fleming HP, Breidt F, Damasceno GS, Passos FV. 2005. Heat Transfer and Microbial Kinetics Modeling to Determine the Location of Microorganisms within Cucumber Fruit. J. Food Sci. 70, E324–E330.
  • Medina E, Arroyo-López FN. 2015. Presence of toxic microbial metabolites in table olives. Front. Microbiol. 6.
  • Medina E, Pérez Díaz IM, Breidt F, Hayes J, Franco W, Butz N, Azcarate Peril MA. 2016. Bacterial Ecology of Fermented Cucumber Rising pH Spoilage as Determined by Nonculture-Based Methods. J. Food Sci. 81, M121–M129.
  • Medina E, Ruiz-Bellido MA, Romero-Gil V, Rodríguez-Gómez F, Montes-Borrego M, Landa BB, Arroyo-López FN. 2016. Assessment of the bacterial community in directly brined Aloreña de Málaga table olive fermentations by metagenetic analysis. Int. J. Food Microbiol. 236, 47–55.
  • Medina E, Brenes M, García P, Romero C. 2018. Microbial ecology along the processing of Spanish olives darkened by oxidation. Food Control 86, 35–41.
  • Montet D, Ray RC, Zakhia-Rozis N. 2014. Lactic Acid Fermentation of Vegetables and Fruits. Microorganisms and Fermentation of Traditional Foods Chapter 4, 108–140.
  • Moon SH, Chang M, Kim HY, Chang HC. 2014. Pichia kudriavzevii is the major yeast involved in film-formation, off-odor production, and texture-softening in over-ripened Kimchi. Food Sci. Biotechnol. 23, 489–497.
  • Pederson CS, Albury MN. 1969. The sauerkraut fermentation, bulletin 824. Geneva, NY: New York State Agricultural Experiment Station.
  • Peres CM, Peres C, Hernández-Mendoza A, Malcata FX. 2012. Review on fermented plant materials as carriers and sources of potentially probiotic lactic acid bacteria – With an emphasis on table olives. Trends Food Sci. Technol. 26, 31–42.
  • Peréz-Díaz IM, Breidt F, Buescher RW, Arroyo-López FN, Jiménez Dıaz R, Garrido-Fernández, A, Bautista-Gallego J, Yoon SS, Johanningsmeire, SD. (2013). Fermented and acidified vegetables. Compendium of methods for the microbiological examination of foods, 4th edn. American Public Health Association, Washington, DC, 521–532.
  • Plastourgos S, Vaughn RH. 1957. Species of Propionibacterium associated with zapatera spoilage of olives. Applied Microbiology 5 (4), 267.
  • Plengvidhya V, Breidt F, Lu Z, Fleming HP. 2007. DNA Fingerprinting of Lactic Acid Bacteria in Sauerkraut Fermentations. Appl. Environ. Microbiol. 73, 7697–7702.
  • Rabie MA, Siliha H, el-Saidy S, el-Badawy AA, Malcata FX. 2011. Reduced biogenic amine contents in sauerkraut via addition of selected lactic acid bacteria. Food Chem. 129, 1778–1782.
  • Randazzo CL, Restuccia C, Romano AD, Caggia C. 2004. Lactobacillus casei, dominant species in naturally fermented Sicilian green olives. Int. J. Food Microbiol. 90, 9–14.
  • Rejano L, Sánchez AH, de Castro A, Montaño A. 1997. Chemical characteristics and storage stability of pickled garlic prepared using different processes. J. Food Sci. 62, 1120–1123.
  • Reina LD, Pérez-Díaz IM, Breidt F, Azcarate-Peril MA, Medina E, Butz N. 2015. Characterization of the microbial diversity in yacon spontaneous fermentation at 20 °C. Int. J. Food Microbiol. 203, 35–40.
  • Rodríguez-Gómez F, Arroyo-López FN, López-López A, Bautista-Gallego J, Garrido-Fernández A. 2010. Lipolytic activity of the yeast species associated with the fermentation/storage phase of ripe olive processing. Food Microbiol. 27, 604–612.
  • Rodríguez-Gómez F, Romero-Gil V, García-García P, Garrido-Fernández A, Arroyo-López FN. 2014. Fortification of table olive packing with the potential probiotic bacteria Lactobacillus pentosus TOMC-LAB2. Front. Microbiol. 5.
  • Romero-Gil V, Rodríguez-Gómez F, Garrido-Fernández A, García-García P, Arroyo-López FN. 2016. Lactobacillus pentosus is the dominant species in spoilt packaged Aloreña de Málaga table olives. LWT-Food Sci. Technol. 70, 252–260.
  • Ruiz-Barba JL, Brenes-Balbuena M, Jiménez-Díaz R, García-García P, Garrido-Fernández A. 1993. Inhibition of Lactobacillus plantarum by polyphenols extracted from two different kinds of olive brine. J. Appl. Bacteriol. 74 (1), 15–19.
  • Samish Z, Etinger-Tulczynska R, Bick M. 1963. The Microflora Within the Tissue of Fruits and Vegetables. J. Food Sci. 28, 259–266.
  • Sánchez AH, de Castro A, Rejano L. 1992. Controlled fermentation of caperberries. J. Food Sci. 57, 675–678.
  • Tamminen M, Joutsjoki T, Sjöblom M, Joutsen M, Palva A, Ryhänen EL, Joutsjoki V. 2004. Screening of lactic acid bacteria from fermented vegetables by carbohydrate profiling and PCR–ELISA. Lett. Appl. Microbiol. 39, 439–444.
  • Tofalo R, Perpetuini G, Schirone M, Ciarrocchi A, Fasoli G, Suzzi G, Corsetti A. 2014. Lactobacillus pentosus dominates spontaneous fermentation of Italian table olives. LWT - Food Sci. Technol. 57, 710–717.
  • Vaughn RH, Stevenson KE, Davé BA, Park HC. 1972. Fermenting yeasts associated with softening and gas-pocket formation in olives. Appl. Microbiol. 23 (2), 316–320.
  • Yan P, Chai Z, Chang X, Zhao W, Yue H, Zhang T. 2015. Screening and identification of microorganism degrading nitrite in Chinese sauerkraut. Agro Food Ind. HiTech. 26, 20–23.
  • Yu J, Gao W, Qing M, Sun Z, Wang W, Liu W, Pan L, Sun T, Wang H, Bai N, Zhang H. 2012. Identification and characterization of lactic acid bacteria isolated from traditional pickles in Sichuan, China. J. Gen. Appl. Microbiol. 58 (3), 163–172.
  • Yue, XQ, Li X, Wu JR, Zhang M. 2013. Isolation and Identification of Lactobacillus from Naturally Fermented Sauerkraut Juices in Xifeng. Adv. Mater. Res Res. 726–731, 147–150.
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