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Yeasts are one of the predominant microbial groups in fermented meats. In this study, yeast communities of Chinese Dong fermented pork (Nanx Wudl) were investigated and the technological properties of 73 yeast isolates were evaluated. Through culture-dependent and high-throughput sequencing methods, the main yeast species identified included Pichia membranifaciens, Kazachstania bulderi, Millerozyma farinosa, Candida zeylanoides, Kazachstania exigua, Candida parapsilosis and Saccharomyces cerevisiae. Among these yeasts, P. membranifaciens, M. farinosa, K. exigua and K. bulderi were detected in fermented meats for the first time. A total of 73 yeast isolates was investigated for their lipolytic and proteolytic activities. All yeast species showed lipolytic activity, while proteolytic activity against meat protein was only detected in S. cerevisiae. Assay of aroma-producing potential was performed in a model simulating fermented sausage condition. Inoculation of yeast strains increased volatiles production, especially esters and alcohols. The highest ester production was observed in S. cerevisiae Y70 strain, followed by K. exigua Y12 and K. bulderi Y19. C. zeylanoides Y10 and S. cerevisiae Y70 were the highest producers of benzeneethanol and 3-methyl-1-butanol. S. cerevisiae Y70 with its highest production of branched alcohols and esters could be a promising candidate as aroma enhancer in the manufacture of fermented sausages.


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Predominant yeasts in Chinese Dong fermented pork (Nanx Wudl) and their aroma-producing properties in fermented sausage condition

Show Author's information Ruifang Mia,bXi Chena,b( )Suyue Xionga,bBiao Qia,bJiapeng Lia,bXiaoling Qiaoa,bWenhua Chena,bChao Qua,bShouwei Wanga,b( )
China Meat Research Center, Beijing 100068, China
Beijing Key Laboratory of Meat Processing Technology, Beijing 100068, China

Abstract

Yeasts are one of the predominant microbial groups in fermented meats. In this study, yeast communities of Chinese Dong fermented pork (Nanx Wudl) were investigated and the technological properties of 73 yeast isolates were evaluated. Through culture-dependent and high-throughput sequencing methods, the main yeast species identified included Pichia membranifaciens, Kazachstania bulderi, Millerozyma farinosa, Candida zeylanoides, Kazachstania exigua, Candida parapsilosis and Saccharomyces cerevisiae. Among these yeasts, P. membranifaciens, M. farinosa, K. exigua and K. bulderi were detected in fermented meats for the first time. A total of 73 yeast isolates was investigated for their lipolytic and proteolytic activities. All yeast species showed lipolytic activity, while proteolytic activity against meat protein was only detected in S. cerevisiae. Assay of aroma-producing potential was performed in a model simulating fermented sausage condition. Inoculation of yeast strains increased volatiles production, especially esters and alcohols. The highest ester production was observed in S. cerevisiae Y70 strain, followed by K. exigua Y12 and K. bulderi Y19. C. zeylanoides Y10 and S. cerevisiae Y70 were the highest producers of benzeneethanol and 3-methyl-1-butanol. S. cerevisiae Y70 with its highest production of branched alcohols and esters could be a promising candidate as aroma enhancer in the manufacture of fermented sausages.

Keywords: Yeast, Nanx Wudl, Fermented sausage, Aroma, Saccharomyces cerevisiae

References(49)

[1]

L.C. Shan, A. De Brún, M. Henchion, et al., Consumer evaluations of processed meat products reformulated to be healthier – a conjoint analysis study, Meat Sci. 131 (2017) 82-89. https://doi.org/10.1016/j.meatsci.2017.04.239

[2]

M.D. Aaslyng, C. Vestergaard, A.G. Koch, The effect of salt reduction on sensory quality and microbial growth in hotdog sausages, bacon, ham and salami, Meat Sci. 96 (2014) 47-55. https://doi.org/10.1016/j.meatsci.2013.06.004

[3]

A. Olivares, J.L. Navarro, M. Flores, Effect of fat content on aroma generation during processing of dry fermented sausages, Meat Sci. 87 (2011) 264-273. https://doi.org/10.1016/j.meatsci.2010.10.021

[4]

S. Corral, C. Belloch, J.J. López-Díez, et al., Yeast inoculation as a strategy to improve the physico-chemical and sensory properties of reduced salt fermented sausages produced with entire male fat, Meat Sci. 123 (2017) 1-7. https://doi.org/10.1016/j.meatsci.2016.08.007

[5]

L. Settanni, P. Barbaccia, A. Bonanno, et al., Evolution of indigenous starter microorganisms and physicochemical parameters in spontaneously fermented beef, horse, wild boar and pork salamis produced under controlled conditions, Food Microbiol. 87 (2020) 103385. https://doi.org/10.1016/j.fm.2019.103385

[6]

L.M. Mendoza, B. Padilla, C. Belloch, et al., Diversity and enzymatic profile of yeasts isolated from traditional llama meat sausages from north-western Andean region of Argentina, Food Res. Int. 62 (2014) 572-579. https://doi.org/10.1016/j.foodres.2014.04.008

[7]

M.J. Andrade, M. Rodríguez, B. Sánchez, et al., DNA typing methods for differentiation of yeasts related to dry-cured meat products, Int. J. Food Microbiol. 107 (2006) 48-58. https://doi.org/10.1016/j.ijfoodmicro.2005.08.011

[8]

M. Flores, S. Corral, L. Cano-García, et al., Yeast strains as potential aroma enhancers in dry fermented sausages, Int. J. Food Microbiol. 212 (2015) 16-24. https://doi.org/10.1016/j.ijfoodmicro.2015.02.028

[9]

I. Ozturk, Presence, changes and technological properties of yeast species during processing of pastirma, a Turkish dry-cured meat product, Food Cont. 50 (2015) 76-84. https://doi.org/10.1016/j.foodcont.2014.08.039

[10]

L. Cano-García, C. Belloch, M. Flores, Impact of Debaryomyces hansenii strains inoculation on the quality of slow dry-cured fermented sausages, Meat Sci. 96 (2014) 1469-1477. https://doi.org/10.1016/j.meatsci.2013.12.011

[11]

C. Chaves-López, A. Paparella, R. Tofalo, et al., Proteolytic activity of Saccharomyces cerevisiae strains associated with Italian dry-fermented sausages in a model system, Int. J. Food Microbiol. 150 (2011) 50-58. https://doi.org/10.1016/j.ijfoodmicro.2011.07.017

[12]

F. Patrignani, L. Iucci, M. Vallicelli, et al., Role of surface-inoculated Debaryomyces hansenii and Yarrowia lipolytica strains in dried fermented sausage manufacture. Part 2: evaluation of their effects on microbial evolution, lipolytic and proteolytic patterns, Meat Sci. 75 (2007) 676-686. https://doi.org/10.1016/j.meatsci.2006.09.016

[13]

S. Corral, C. Belloch, J.J. López-Díez, et al., Lipolysis and aroma generation as mechanisms involved in masking boar taint in sodium reduced fermented sausages inoculated with Debaryomyces hansenii yeast, J. Sci. Food Agr. 98 (2018) 2121-2130. https://doi.org/10.1002/jsfa.8694

[14]

M.J. Andrade, M. Rodríguez, E.M. Casado, et al., Differentiation of yeasts growing on dry-cured Iberian ham by mitochondrial DNA restriction analysis, RAPD-PCR and their volatile compounds production, Food Microbiol. 26 (2009) 578-586. https://doi.org/10.1016/j.fm.2009.03.014

[15]

M. Flores, M.A. Durá, A. Marco, et al., Effect of Debaryomyces spp. on aroma formation and sensory quality of dry-fermented sausages, Meat Sci. 68 (2004) 439-446. https://doi.org/10.1016/j.meatsci.2003.04.001

[16]

M.J. Andrade, L. Thorsen, A. Rodriguez, et al., Inhibition of ochratoxigenic moulds by Debaryomyces hansenii strains for biopreservation of dry-cured meat products, Int. J. Food Microbiol. 170 (2014) 70-77. https://doi.org/10.1016/j.ijfoodmicro.2013.11.004

[17]

B. Peromingo, M.J. Andrade, J. Delgado, et al., Biocontrol of aflatoxigenic Aspergillus parasiticus by native Debaryomyces hansenii in dry-cured meat products, Food Microbiol. 82 (2019) 269-276. https://doi.org/10.1016/j.fm.2019.01.024

[18]

J.M. Andrade, J.J. Córdoba, B. Sánchez, et al., Evaluation and selection of yeasts isolated from dry-cured Iberian ham by their volatile compound production, Food Chem. 113 (2009) 457-463. https://doi.org/10.1016/j.foodchem.2008.07.080

[19]

L. Cano-García, M. Flores, C. Belloch, Molecular characterization and aromatic potential of Debaryomyces hansenii strains isolated from naturally fermented sausages, Food Res. Int. 52 (2013) 42-49. https://doi.org/10.1016/j.foodres.2013.02.047

[20]

L. Cano-Garcia, S. Rivera-Jimenez, C. Belloch, et al., Generation of aroma compounds in a fermented sausage meat model system by Debaryomyces hansenii strains, Food Chem. 151 (2014) 364-373. https://doi.org/10.1016/j.foodchem.2013.11.051

[21]

C.E.D.S. Cruxen, G.D. Funck, L. Haubert, et al., Selection of native bacterial starter culture in the production of fermented meat sausages: application potential, safety aspects, and emerging technologies, Food Res. Int. 122 (2019) 371-382. https://doi.org/10.1016/j.foodres.2019.04.018

[22]

M. Mrkonjic Fuka, I. Tanuwidjaja, A. Zgomba Maksimovic, et al., Bacterial diversity of naturally fermented game meat sausages: sources of new starter cultures, LWT-Food Sci. Technol. 118 (2020) 108782. https://doi.org/10.1016/j.lwt.2019.108782

[23]

Z.J. Li, H.H. Jiang, L.M. Li, Characterization of microbial flora associated with Nanx Wudl - a traditional tong nationality fermented meat, Chin. J. Microecol. 14 (2002) 19-22

[24]

Z.J. Li, H.H. Jiang, Alteration of microbes flora of Chinese traditional sour meat during fermentation, Microbiology China 31 (2004) 9-13

[25]

C.Q. Zhou, Y.F. Li, M.Y. Du, Study on microbial flora of traditional fermentative sour meat in YU-QIAN district, Sci. Tech. Food Industry 31 (2010) 171-175

[26]

N.A. Bokulich, D.A. Mills, Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities, Appl. Environ. Microbiol. 79 (2013) 2519-2526. https://doi.org/10.1128/aem.03870-12

[27]

T. Rognes, T. Flouri, B. Nichols, et al., VSEARCH: a versatile open source tool for metagenomics, PeerJ 4 (2016) e2584. https://doi.org/10.7717/peerj.2584

[28]

B. Esteve-Zarzoso, C. Belloch, F. Uruburu, et al., Identification of yeasts by RFLP analysis of the 5.8S rRNA gene and the two ribosomal internal transcribed spacers, Int. J. Syst. Bacteriol. 49 (1999) 329-337. https://doi.org/10.1099/00207713-49-1-329

[29]

C.P. Kurtzman, C.J. Robnett, Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences, Antonie van Leeuwenhoek 73 (1998) 331-371. https://doi.org/10.1023/A:1001761008817

[30]

P. Buzzini, A. Martini, Extracellular enzymatic activity profiles in yeast and yeast-like strains isolated from tropical environments, J. Appl. Microbiol. 93 (2002) 1020-1025. https://doi.org/10.1046/j.1365-2672.2002.01783.x

[31]

H.D. Paik, J.Y. Lee, Investigation of reduction and tolerance capability of lactic acid bacteria isolated from kimchi against nitrate and nitrite in fermented sausage condition, Meat Sci. 97 (2014) 609-614. https://doi.org/10.1016/j.meatsci.2014.03.013

[32]

L. Gao, T. Liu, X. An, et al., Analysis of volatile flavor compounds influencing Chinese-type soy sauces using GC-MS combined with HS-SPME and discrimination with electronic nose, J. Food Sci. Technol. 54 (2017) 130-143. https://doi.org/10.1007/s13197-016-2444-0

[33]

K.A. Gutsche, T.B. Tran, R.F. Vogel, Production of volatile compounds by Lactobacillus sakei from branched chain alpha-keto acids, Food Microbiol. 29 (2012) 224-228. https://doi.org/10.1016/j.fm.2011.06.010

[34]
D.Y.C. Fung, Microbiological safety of meat | Yeasts and Molds, in Encyclopedia of Meat Sciences (Second Edition), M. Dikeman and C. Devine, Editors. 2014, Academic Press: Oxford. p. 395-404.
DOI
[35]
J. Samelis, J.N. Sofos, 9 - Yeasts in meat and meat products, in Yeasts in Food, T. Boekhout and V. Robert, Editors. 2003, Woodhead Publishing. p. 239-265.
DOI
[36]

D.S. Nielsen, T. Jacobsen, L. Jespersen, et al., Occurrence and growth of yeasts in processed meat products - implications for potential spoilage, Meat Sci. 80 (2008) 919-926. https://doi.org/10.1016/j.meatsci.2008.04.011

[37]

S. Dorn-In, C.S. Hölzel, T. Janke, et al., PCR-SSCP-based reconstruction of the original fungal flora of heat-processed meat products, Int. J. Food Microbiol. 162 (2013) 71-81. https://doi.org/10.1016/j.ijfoodmicro.2012.12.022

[38]

H. Csoma, N. Zakany, A. Capece, et al., Biological diversity of Saccharomyces yeasts of spontaneously fermenting wines in four wine regions: comparative genotypic and phenotypic analysis, Int. J. Food Microbiol. 140 (2010) 239-248. https://doi.org/10.1016/j.ijfoodmicro.2010.03.024

[39]

L. De Vuyst, H. Harth, S. Van Kerrebroeck, et al., Yeast diversity of sourdoughs and associated metabolic properties and functionalities, Int. J. Food Microbiol. 239 (2016) 26-34. https://doi.org/10.1016/j.ijfoodmicro.2016.07.018

[40]

J.S. Saez, C.A. Lopes, V.E. Kirs, et al., Production of volatile phenols by Pichia manshurica and Pichia membranifaciens isolated from spoiled wines and cellar environment in Patagonia, Food Microbiol. 28 (2011) 503-509. https://doi.org/10.1016/j.fm.2010.10.019

[41]

P.R. Sternes, D. Lee, D.R. Kutyna, et al., A combined meta-barcoding and shotgun metagenomic analysis of spontaneous wine fermentation, Gigascience 6 (2017) 1-10. https://doi.org/10.1093/gigascience/gix040

[42]

J. Sun, C.C. Cao, M.Q. Feng, et al., Technological and safety characterization of coagulase-negative staphylococci with high protease activity isolated from traditional Chinese fermented sausages, LWT-Food Sci. Technol. 114 (2019) 108371. https://doi.org/10.1016/j.lwt.2019.108371

[43]

M. Flores, F. Toldrá, Microbial enzymatic activities for improved fermented meats, Trends Food Sci. Tech. 22 (2011) 81-90. https://doi.org/10.1016/j.tifs.2010.09.007

[44]

C. Montanari, E. Bargossi, A. Gardini, et al., Correlation between volatile profiles of Italian fermented sausages and their size and starter culture, Food Chem. 192 (2016) 736-744. https://doi.org/10.1016/j.foodchem.2015.07.062

[45]

A. Olivares, J.L. Navarro, M. Flores, Establishment of the contribution of volatile compounds to the aroma of fermented sausages at different stages of processing and storage, Food Chem. 115 (2009) 1464-1472. https://doi.org/10.1016/j.foodchem.2009.01.083

[46]

A. Marco, J.L. Navarro, M. Flores, Volatile compounds of dry-fermented sausages as affected by solid-phase microextraction (SPME), Food Chem. 84 (2004) 633-641. https://doi.org/10.1016/S0308-8146(03)00288-7

[47]

A. Martín, Effect of Penicillium chrysogenum and Debaryomyces hansenii on the volatile compounds during controlled ripening of pork loins, Int. J. Food Microbiol. 84 (2003) 327-338. https://doi.org/10.1016/S0168-1605(02)00474-9

[48]

L.H. Stahnke, A. Holck, A. Jensen, et al., Maturity acceleration of Italian dried sausage by Staphylococcus carnosus—relationship between maturity and flavor compounds, J. Food Sci. 67 (2002) 1914-1921. https://doi.org/10.1111/j.1365-2621.2002.tb08746.x

[49]

L. Iucci, F. Patrignani, N. Belletti, et al., Role of surface-inoculated Debaryomyces hansenii and Yarrowia lipolytica strains in dried fermented sausage manufacture. Part 2: evaluation of their effects on sensory quality and biogenic amine content, Meat Sci. 75 (2007) 669-675. https://doi.org/10.1016/j.meatsci.2006.09.016

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Publication history

Received: 27 March 2020
Revised: 13 July 2020
Accepted: 27 July 2020
Published: 22 March 2021
Issue date: March 2021

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© 2021 Beijing Academy of Food Sciences.

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Acknowledgements

The authors acknowledge the financial support of the National Key R & D Program of China (grant no. 2018YFD0400404).

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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