Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Debaryomyces hansenii Strains from Valle De Los Pedroches Iberian Dry Meat Products: Isolation, Identification, Characterization, and Selection for Starter Cultures

  • Ramos, Jose (Departamento de Microbiologia, Escuela Tecnica Superior de Ingenieria Agronomica y de Montes, Universidad de Cordoba, Campus de Rabanales) ;
  • Melero, Yessica (Departamento de Microbiologia, Escuela Tecnica Superior de Ingenieria Agronomica y de Montes, Universidad de Cordoba, Campus de Rabanales) ;
  • Ramos-Moreno, Laura (Departamento de Microbiologia, Escuela Tecnica Superior de Ingenieria Agronomica y de Montes, Universidad de Cordoba, Campus de Rabanales) ;
  • Michan, Carmen (Departamento de Bioquimica y Biologia Molecular, Facultad de Ciencias, Universidad de Cordoba, Campus de Rabanales) ;
  • Cabezas, Lourdes (Departamento de Bromatologia y Tecnologia de los Alimentos, Facultad de Veterinaria, Universidad de Cordoba, Campus de Rabanales)
  • Received : 2017.04.19
  • Accepted : 2017.06.26
  • Published : 2017.09.28
Download PDF
⟨ Previous Next ⟩

Abstract

Yeasts, filamentous fungi, and bacteria colonize the surface of fermented sausages during the ripening process. The source of this microbiota is their surrounding environment, and is influenced by the maturing conditions and starter cultures. Debaryomyces hansenii was previously isolated from several dry-cured meat products and associated with the lipolytic and proteolytic changes that occur in these products, influencing their taste and flavor. Therefore, this study isolated the yeast microbiota present in the casing from different meat products ("lomo," "chorizo," and "$salchich{\acute{o}}n$") from the Valle de los Pedroches region in southern Spain. D. hansenii was by far the most abundant species in each product, as all 22 selected isolates were identified as D. hansenii by biochemical and/or molecular methods. In contrast, no yeasts were found in the meat batter. These data constitute the first study of the yeasts present in "lomo" sausages and particularly the highly appreciated Valle de los Pedroches "lomo" sausages. Furthermore, the resistance of these isolates to different pHs, temperatures, and saline stress was studied, together with their catabolic characteristics. Based on the results, certain isolates are proposed as valuable candidate starter cultures that could improve both the manufacture and the flavor of such dry-cured meat products, and provide an understanding of new mechanisms involved in stress tolerance. Applied medium-scale industrial tests are currently in progress.

Keywords

References

  1. Cocolin L, Urso R, Rantsiou K, Cantoni C, Comi G. 2006. Dynamics and characterization of yeasts during natural fermentation of Italian sausages. FEMS Yeast Res. 6: 692-701. https://doi.org/10.1111/j.1567-1364.2006.00050.x
  2. Encinas JP, Lopez-Diaz TM, Garcia-Lopez ML, Otero A, Moreno B. 2000. Yeast populations on Spanish fermented sausages. Meat Sci. 54: 203-208. https://doi.org/10.1016/S0309-1740(99)00080-7
  3. Samelis J, Stavropoulos S, Kakouri A, Metaxopoulos J. 1994. Quantification and characterization of microbial populations associated with natural fermented Greek dry salami. Food Microbiol. 11: 447-460. https://doi.org/10.1006/fmic.1994.1050
  4. Aquilanti L, Santarelli S, Silvestri G, Osimani A, Petruzzelli A, Clementi F. 2007. The microbial ecology of a typical Italian salami during its natural fermentation. Int. J. Food Microbiol. 120: 136-145. https://doi.org/10.1016/j.ijfoodmicro.2007.06.010
  5. Coppola S, Mauriello G, Aponte M, Moschetti G, Villani F. 2000. Microbial succession during ripening of Naples-type salami, a southern Italian fermented sausage. Meat Sci. 56: 321-329. https://doi.org/10.1016/S0309-1740(00)00046-2
  6. Cano-Garcia L, Belloch C, Flores M. 2014. Impact of Debaryomyces hansenii strains inoculation on the quality of slow dry-cured fermented sausages. Meat Sci. 96: 1469-1477. https://doi.org/10.1016/j.meatsci.2013.12.011
  7. Cano-Garcia L, Rivera-Jimenez S, Belloch C, Flores M. 2014. Generation of aroma compounds in a fermented sausage meat model system by Debaryomyces hansenii strains. Food Chem. 151: 364-373. https://doi.org/10.1016/j.foodchem.2013.11.051
  8. Flores M, Dura MA, Marco A, Toldra F. 2004. Effect of Debaryomyces spp. on aroma formation and sensory quality of dry-fermented sausages. Meat Sci. 68: 439-446. https://doi.org/10.1016/j.meatsci.2003.04.001
  9. Ozturk I, Sagdic O. 2014. Biodiversity of yeast mycobiota in "sucuk," a traditional Turkish fermented dry sausage: phenotypic and genotypic identification, functional and technological properties. J. Food Sci. 79: M2315-M2322. https://doi.org/10.1111/1750-3841.12662
  10. Cocolin L, Dolci P, Rantsiou K. 2011. Biodiversity and dynamics of meat fermentations: the contribution of molecular methods for a better comprehension of a complex ecosystem. Meat Sci. 89: 296-302. https://doi.org/10.1016/j.meatsci.2011.04.011
  11. Leroy F, Verluyten J, De Vuyst L. 2006. Functional meat starter cultures for improved sausage fermentation. Int. J. Food Microbiol. 106: 270-285. https://doi.org/10.1016/j.ijfoodmicro.2005.06.027
  12. Flores J, Marcus JR, Nieto P, Navarro JL, Lorenzo P. 1997. Effect of processing conditions on proteolysis and taste of dry-cured sausages. Eur. Food Res. Technol. 204: 168-172.
  13. Hugas M, Monfort J. 1997. Bacterial starter cultures for meat fermentation. Food Chem. 59: 547-554. https://doi.org/10.1016/S0308-8146(97)00005-8
  14. Kumar P, Chatli MK, Verma AK, Mehta N, Malav OP, Kumar D, et al. 2017. Quality, functionality and shelf life of fermented meat and meat products: a review. Crit. Rev. Food Sci. Nutr. 57: 2844-2856. https://doi.org/10.1080/10408398.2015.1074533
  15. Ravyts F, De Vuyst L, Leroy F. 2012. Bacterial diversity and functionalities in food fermentations. Eng. Life Sci. 12: 356-367. https://doi.org/10.1002/elsc.201100119
  16. Fleet GH. 1990. Yeasts in dairy products. J. Appl. Bacteriol. 68: 199-211. https://doi.org/10.1111/j.1365-2672.1990.tb02566.x
  17. Kurita O, Yamazaki E. 2002. Growth under alkaline conditions of the salt-tolerant yeast Debaryomyces hansenii IFO10939. Curr. Microbiol. 45: 277-280. https://doi.org/10.1007/s00284-002-3735-4
  18. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I, et al. 2004. Genome evolution in yeasts. Nature 430: 35-44. https://doi.org/10.1038/nature02579
  19. Souciet JL, Dujon B, Gaillardin C, Johnston M, Baret PV, Cliften P, et al. 2009. Comparative genomics of protoploid Saccharomycetaceae. Genome Res. 19: 1696-1709. https://doi.org/10.1101/gr.091546.109
  20. Prista C, Michán C, Miranda IM, Ramos J. 2016. The halotolerant Debaryomyces hansenii, the Cinderella of nonconventional yeasts. Yeast 33: 523-533. https://doi.org/10.1002/yea.3177
  21. Quiros M, Wrent P, Valderrama MJ, de Siloniz MI, Peinado JM. 2005. A beta-glucuronidase-based agar medium for the differential detection of the yeast Debaryomyces hansenii from foods. J. Food Prot. 68: 808-814. https://doi.org/10.4315/0362-028X-68.4.808
  22. Atanassova MR, Fernandez-Otero C, Rodriguez-Alonso P, Fernandez-No IC, Garabal JI, Centeno JA. 2016. Characterization of yeasts isolated from artisanal short-ripened cows' cheeses produced in Galicia (NW Spain). Food Microbiol. 53: 172-181. https://doi.org/10.1016/j.fm.2015.09.012
  23. Green MR, Sambrook J. 2012. Molecular Cloning: A Laboratory Manual, 4th Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
  24. Gardini F, Suzzi G, Lombardi A, Galgano F, Crudele MA, Andrighetto C, et al. 2001. A survey of yeasts in traditional sausages of southern Italy. FEMS Yeast Res. 1: 161-167. https://doi.org/10.1111/j.1567-1364.2001.tb00027.x
  25. Capita R, Llorente-Marigomez S, Prieto M, Alonso-Calleja C. 2006. Microbiological profiles, pH, and titratable acidity of chorizo and salchichon (two Spanish dry fermented sausages) manufactured with ostrich, deer, or pork meat. J. Food Prot. 69: 1183-1189. https://doi.org/10.4315/0362-028X-69.5.1183
  26. Choe HS, Shim K, Jung JH, Chung YH, Shin D. 2014. Effects of ripening conditions on the 'lomo embuchado' sausage quality. Korean J. Food Sci. Anim. Resour. 34: 333-338. https://doi.org/10.5851/kosfa.2014.34.3.333
  27. Fonseca S, Cachaldora A, Gomez M, Franco I, Carballo J. 2013. Monitoring the bacterial population dynamics during the ripening of Galician chorizo, a traditional dry fermented Spanish sausage. Food Microbiol. 33: 77-84. https://doi.org/10.1016/j.fm.2012.08.015
  28. Fonseca S, Ivette Ouoba LI, Franco I, Carballo J. 2013. Use of molecular methods to characterize the bacterial community and to monitor different native starter cultures throughout the ripening of Galician chorizo. Food Microbiol. 34: 215-226. https://doi.org/10.1016/j.fm.2012.12.006
  29. Pateiro M, Bermudez R, Lorenzo JM, Franco D. 2015. Effect of addition of natural antioxidants on the shelf-life of "chorizo", a spanish dry-cured sausage. Antioxidants (Basel) 4: 42-67. https://doi.org/10.3390/antiox4010042
  30. Asefa DT, Gjerde RO, Sidhu MS, Langsrud S, Kure CF, Nesbakken T, et al. 2009. Moulds contaminants on Norwegian dry-cured meat products. Int. J. Food Microbiol. 128: 435-439. https://doi.org/10.1016/j.ijfoodmicro.2008.09.024
  31. Iacumin L, Chiesa L, Boscolo D, Manzano M, Cantoni C, Orlic S, et al. 2009. Moulds and ochratoxin A on surfaces of artisanal and industrial dry sausages. Food Microbiol. 26: 65-70. https://doi.org/10.1016/j.fm.2008.07.006
  32. Iacumin L, Manzano M, Panseri S, Chiesa L, Comi G. 2016. A new cause of spoilage in goose sausages. Food Microbiol. 58: 56-62. https://doi.org/10.1016/j.fm.2016.03.007
  33. Sonjak S, Licen M, Frisvad JC, Gunde-Cimerman N. 2011. The mycobiota of three dry-cured meat products from Slovenia. Food Microbiol. 28: 373-376. https://doi.org/10.1016/j.fm.2010.09.007
  34. Andrade MA, Cordoba JJ, Casado EM, Cordoba MG, Rodriguez M. 2010. Effect of selected strains of Debaryomyces hansenii on the volatile compound production of dry fermented sausage "salchichon". Meat Sci. 85: 256-264. https://doi.org/10.1016/j.meatsci.2010.01.009
  35. Quiros M, Martorell P, Querol A, Barrio E, Peinado JM, de Siloniz MI. 2008. Four new Candida cretensis strains isolated from Spanish fermented sausages (chorizo): taxonomic and phylogenetic implications. FEMS Yeast Res. 8: 485-491. https://doi.org/10.1111/j.1567-1364.2007.00341.x
  36. Casquete R, Benito MJ, Martín A, Ruiz-Moyano S, Saranda E, Córdoba MG. 2012. Microbiological quality of salchichon and chorizo, traditional Iberian dry-fermented sausages from two different industries, inoculated with autochthonous starter cultures. Food Control 24: 191-198. https://doi.org/10.1016/j.foodcont.2011.09.026
  37. Rubio B, Martinez B, Sanchez MJ, Dolores Garcia-Cachan MA, Rovira J, Jaime I. 2007. Study of the shelf life of a dry fermented sausage "salchichon" made from raw material enriched in monounsaturated and polyunsaturated fatty acids and stored under modified atmospheres. Meat Sci. 76: 128-137. https://doi.org/10.1016/j.meatsci.2006.10.021
  38. Ruiz-Moyano S, Martin A, Benito MJ, Hernandez A, Casquete R, de Guia Cordoba M. 2011. Application of Lactobacillus fermentum HL57 and Pediococcus acidilactici SP979 as potential probiotics in the manufacture of traditional Iberian dry-fermented sausages. Food Microbiol. 28: 839-847. https://doi.org/10.1016/j.fm.2011.01.006
  39. Flores M, Corral S, Cano-Garcia L, Salvador A, Belloch C. 2015. Yeast strains as potential aroma enhancers in dry fermented sausages. Int. J. Food Microbiol. 212: 16-24. https://doi.org/10.1016/j.ijfoodmicro.2015.02.028
  40. Hospital XF, Hierro E, Stringer S, Fernandez M. 2016. A study on the toxigenesis by Clostridium botulinum in nitrate and nitrite-reduced dry fermented sausages. Int. J. Food Microbiol. 218: 66-70. https://doi.org/10.1016/j.ijfoodmicro.2015.11.009
  41. Corral S, Leitner E, Siegmund B, Flores M. 2016. Determination of sulfur and nitrogen compounds during the processing of dry fermented sausages and their relation to amino acid generation. Food Chem. 190: 657-664. https://doi.org/10.1016/j.foodchem.2015.06.009
  42. Zdolec N, Hadziosmanovic M, Kozacinski L, Cvrtila Z, Filipovic I, Skrivanko M, et al. 2008. Microbial and physicochemical succession in fermented sausages produced with bacteriocinogenic culture of Lactobacillus sakei and semipurified bacteriocin mesenterocin Y. Meat Sci. 80: 480-487. https://doi.org/10.1016/j.meatsci.2008.01.012
  43. Suizu T, Tsutsumi H, Kawado A, Inose T, Suginami K, Murata K. 1995. Analysis of lysine-dependent yeast sporulation: a decrease in cyclic AMP is not required for initiation of meiosis and sporulation in Saccharomyces cerevisiae. Microbiology 141: 2463-2469. https://doi.org/10.1099/13500872-141-10-2463
  44. Prista C, Loureiro-Dias MC, Montiel V, Garcia R, Ramos J. 2005. Mechanisms underlying the halotolerant way of Debaryomyces hansenii. FEMS Yeast Res. 5: 693-701. https://doi.org/10.1016/j.femsyr.2004.12.009
  45. Bover-Cid S, Torriani S, Gatto V, Tofalo R, Suzzi G, Belletti N, Gardini F. 2009. Relationships between microbial population dynamics and putrescine and cadaverine accumulation during dry fermented sausage ripening. J. Appl. Microbiol. 106: 1397-1407. https://doi.org/10.1111/j.1365-2672.2008.04108.x
  46. Michan C, Martinez JL, Alvarez MC, Turk M, Sychrova H, Ramos J. 2013. Salt and oxidative stress tolerance in Debaryomyces hansenii and Debaryomyces fabryi. FEMS Yeast Res. 13: 180-188. https://doi.org/10.1111/1567-1364.12020
  47. Almagro A, Prista C, Castro S, Quintas C, Madeira-Lopes A, Ramos J, Loureiro-Dias MC. 2000. Effects of salts on Debaryomyces hansenii and Saccharomyces cerevisiae under stress conditions. Int. J. Food Microbiol. 56: 191-197. https://doi.org/10.1016/S0168-1605(00)00220-8
  48. Norkrans B, Kylin A. 1969. Regulation of the potassium to sodium ratio and of the osmotic potential in relation to salt tolerance in yeasts. J. Bacteriol. 100: 836-845.
  49. Karsloglu B, Cicek UE, Kolsarici N, Candogan K. 2014. Lipolytic changes in fermented sausages produced with Turkey meat: effects of starter culture and heat treatment. Korean J. Food Sci. Anim. Resour. 34: 40-48. https://doi.org/10.5851/kosfa.2014.34.1.40
  50. Diaz O, Fernandez M, De Fernando GD, de la Hoz L, Ordonez JA. 1997. Proteolysis in dry fermented sausages: the effect of selected exogenous proteases. Meat Sci. 46: 115-128. https://doi.org/10.1016/S0309-1740(97)00013-2
  51. Bruna JM, Hierro EM, de la Hoz L, Mottram DS, Fernandez M, Ordonez JA. 2003. Changes in selected biochemical and sensory parameters as affected by the superficial inoculation of Penicillium camemberti on dry fermented sausages. Int. J. Food Microbiol. 85: 111-125. https://doi.org/10.1016/S0168-1605(02)00505-6

Cited by

  1. The Microbiome of an Active Meat Curing Brine vol.9, pp.None, 2017, https://doi.org/10.3389/fmicb.2018.03346
  2. Overlapping responses between salt and oxidative stress in Debaryomyces hansenii vol.35, pp.11, 2019, https://doi.org/10.1007/s11274-019-2753-3
  3. Cell Factories for Industrial Production Processes: Current Issues and Emerging Solutions vol.8, pp.7, 2020, https://doi.org/10.3390/pr8070768
  4. Characterization of the microbiota and chemical properties of pork loins during dry aging vol.10, pp.1, 2017, https://doi.org/10.1002/mbo3.1157
  5. A physiological characterization in controlled bioreactors reveals a novel survival strategy for Debaryomyces hansenii at high salinity vol.38, pp.5, 2017, https://doi.org/10.1002/yea.3544
  6. Debaryomyces hansenii Is a Real Tool to Improve a Diversity of Characteristics in Sausages and Dry-Meat Products vol.9, pp.7, 2017, https://doi.org/10.3390/microorganisms9071512
  7. Technological properties and flavour formation potential of yeast strains isolated from traditional dry fermented sausages in Northeast China vol.154, pp.None, 2017, https://doi.org/10.1016/j.lwt.2021.112853