Elsevier

International Dairy Journal

Volume 72, September 2017, Pages 44-54
International Dairy Journal

Use of smear bacteria and yeasts to modify flavour and appearance of Cheddar cheese

https://doi.org/10.1016/j.idairyj.2017.04.001Get rights and content

Abstract

The strains Staphylococcus saprophyticus DPC5671 and Corynebacterium casei DPC5298 were applied in combination with Debaryomyces hansenii DPC6258 to the surface of young Cheddar cheese curd to obtain two different smear-ripened cheeses. A surface microbiota developed over the incubation period, comprising of both yeast and bacteria; pulsed field gel electrophoresis confirmed that the inoculated strains of S. saprophyticus DPC5671 or C. casei DPC5298 were the dominant bacterial strains on the surface of the cheese at the end of the ripening period. The smear cultures changed the appearance and aroma, which were significantly different from the control cheese. The approach presented in this study represents a method for the development of new cheese varieties with novel aromas within a short ripening time.

Introduction

Smear cheese is a traditional dairy product, which plays an important role in both small and industrial scale dairy production. Smear cheese is characterised by a short ripening time and strong aroma produced by the growth of smear microbiota on the cheese surface. Smear-ripened cheeses are manufactured by inoculating the surface of the cheese curd, dipping, spraying or brushing with a mixture of bacteria and yeasts. The traditional method of production is called “old-young smearing” and consists of washing young curds with the brine from old cheese, to encourage the transfer of the microbiota from the old to the young cheeses (Desmasures et al., 2015, Fox et al., 2017a).

The microbiota on the surface of the smear cheese is composed of a variety of microorganisms that coexist in symbiotic relationships. Yeasts are normally the first resident microorganisms to establish themselves on the surface of the cheese due to their tolerance to low pH and salt. Yeasts metabolise lactate, producing H2O and CO2 and increase the pH (Cholet et al., 2007, Corsetti et al., 2001). Moreover, they produce metabolites and growth factors (vitamins and amino acids) which encourage the growth of Gram-positive bacteria, such as Corynebacterium, Staphylococcus and Brevibacterium species (Cogan et al., 2014, Larpin et al., 2011).

The growth of smear microorganisms on the surface of cheese curd modifies the appearance, aroma, proteolysis and lipolysis of the cheese within a relatively short ripening time (McSweeney, 2004). The combined growth of the bacteria and yeasts on the surface of the cheese results in the production of proteolytic and lipolytic enzymes, increasing the amount of free amino acids (FAAs) and free fatty acids (FFAs) (McSweeney and Sousa, 2000, Sousa et al., 2001). Yeasts and Gram-positive bacteria isolated from smear cheeses have a wide range of proteolytic enzymes that display various peptidase activities, with FAAs increasing within the cheese as a consequence. Additionally, yeasts and Gram-positive bacteria possess esterolytic/lipolytic enzymes capable of catabolising triacylglycerols in cheese, producing FFAs (Curtin et al., 2002, Fox et al., 2017b).

The further metabolism of FAAs and FFAs during the ripening produces flavour compounds important for cheese aroma. The catabolism of FAAs, especially of branched chain amino acids, aromatic amino acids and sulphur amino acids, produces mainly aldehydes, alcohols, carboxylic acids and sulphur compounds. Moreover, FFAs are involved in reactions leading to the production of flavour compounds such as secondary alcohols, carboxylic acids, esters, lactones and ketones (McSweeney and Sousa, 2000, Singh et al., 2003, Smit et al., 2005, Yvon and Rijnen, 2001).

The characteristics of smear-ripened cheese are not strictly controlled inside artisanal smear cheese plants. The resulting product is also affected by the final microbial consortia of the cheese, which is influenced by the individual in-house microbiota of the cheese-making facilities. Microorganisms detected in the environment of artisanal cheese-making plants have also been found on the surface of smear cheeses, indicating a strong relationship between product and the environment in which the cheese is manufactured and ripened (Bokulich and Mills, 2013, Goerges et al., 2008, Mounier et al., 2006a).

In previous studies, smear strains were added to the cheese surface or as adjunct cultures to the milk during manufacture of smear-ripened cheese; however, some of the added strains were not detected at the end of ripening (Feurer et al., 2004, Goerges et al., 2008). These commercial smear strains have to compete with the in-house microbiota and do not always successfully establish themselves on the cheese surface (Bokulich and Mills, 2013, Feurer et al., 2004, Goerges et al., 2008). It is likely that the relationship within the smear microbiota promotes the survival of a particular group of microorganisms to the detriment of others.

With the abolition of the milk quotas within the EU in 2015 there is a renewed interest in developing novel cheeses with a range of flavours. There is a progressive increase in global cheese consumption, with an annual production in Ireland of 207,100 tonnes in 2015 (data from Eurostat). Therefore the aim of this work was to develop a novel cheese with diverse aromas and short ripening time using cheese curd made in a traditional Cheddar cheese plant. Ripening time for Cheddar cheese can be from a little as 3 months for mild cheese up to > 9–12 months for mature/extra mature varieties. In this study, the ability of smear bacteria and yeast to grow on the surface of young Cheddar cheese curd was investigated to produce a cheese variety with different flavour and appearance compared with Cheddar cheese within a short time frame of 35 days.

Section snippets

Preparation of smear suspensions

For the preparation of the Debaryomyces hansenii DPC6258 suspension, the strain was streaked onto yeast extract glucose chloramphenicol agar (YGC agar; Becton, Dickinson and Company, City West, Dublin, Ireland) and incubated aerobically at 25 °C for 96 h. Using a 5 μL loop, the strain was inoculated into 10 mL of trypticase soy broth (TSB; Becton, Dickinson and Company) and incubated, shaking at 100 rpm, at 25 °C. When the OD600 reached ∼1, the cells were centrifuged at 6000 × g at 4 °C for

Growth of the strains and pH development

PFGE analysis established that the inoculated cultures of S. saprophyticus DPC5671 and C. casei DPC5298 were the dominant bacterial strains isolated at the end of ripening (day 35) (Supplementary data). The total count of yeasts and smear bacteria during ripening is shown in Fig. 1. A significant interactive effect (P < 0.05) between ripening time and smear treatments was observed for the growth of the surface microbiota. No significant differences were observed in the growth of yeast and

Discussion

C. casei and S. saprophyticus, bacteria commonly isolated from smear-ripened cheeses (e.g., Limburger, Reblochon, Livarot, Tilsit, Gubbeen) (Cogan et al., 2014, Larpin et al., 2011), do not belong to the traditional microbiota of Cheddar cheese, although in this study both strains established themselves on the surface of young Cheddar cheese curd and they were the dominant population on the cheese surface throughout the ripening.

C. casei DPC5298 or S. saprophyticus DPC5671 in combination with

Conclusion

The cheese-making method described in this paper gives a new approach for the production of novel smear cheeses starting from a Cheddar cheese curd. Both the yeast and bacterial cultures were able to establish themselves on the surface of the cheese and become the dominant microbiota on the cheese surface, producing a cheese variety with acceptable appearance and novel flavour and aroma profiles. The method proposed could be used as a model to produce novel cheese types with a range of flavours

Acknowledgements

The authors wish to thank to Sarah Henneberry, David Mannion and Hope Faulkner for their assistance in the analysis. Andrea Bertuzzi is currently in a receipt of Teagasc Walsh Fellowship.

References (58)

  • M.N. Leclercq-Perlat et al.

    Comparison of volatile compounds produced in model cheese medium deacidified by Debaryomyces hansenii or Kluyveromyces marxianus

    Journal of Dairy Science

    (2004)
  • D.T. Mannion et al.

    Comparison and validation of 2 analytical methods for the determination of free fatty acids in dairy products by gas chromatography with flame ionization detection

    Journal of Dairy Science

    (2016)
  • A. McDermott et al.

    Prediction of individual milk proteins including free amino acids in bovine milk using mid-infrared spectroscopy and their correlations with milk processing characteristics

    Journal of Dairy Science

    (2016)
  • M.C. Qian et al.

    Identification of aroma compounds in Parmigiano-Reggiano cheese by gas chromatography/olfactometry

    Journal of Dairy Science

    (2002)
  • N.M. Rynne et al.

    Effect of milk pasteurisation temperature and in situ whey protein denaturation on the composition, texture and heat-induced functionality of half-fat Cheddar cheese

    International Dairy Journal

    (2004)
  • G. Smit et al.

    Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products

    FEMS Microbiology Reviews

    (2005)
  • M.J. Sousa et al.

    Advances in the study of proteolysis during cheese ripening

    International Dairy Journal

    (2001)
  • R. Talon et al.

    Production of esters by Staphylococci

    International Journal of Food Microbiology

    (1998)
  • R. Talon et al.

    Hydrolysis of esters by Staphylococci

    International Journal of Food Microbiology

    (1997)
  • T. van den Tempel et al.

    The technological characteristics of Debaryomyces hansenii and Yarrowia lipolytica and their potential as starter cultures for production of Danablu

    International Dairy Journal

    (2000)
  • M. Thomsen et al.

    Investigating semi-hard cheese aroma: Relationship between sensory profiles and gas chromatography-olfactometry data

    International Dairy Journal

    (2012)
  • G. Urbach

    Relations between cheese flavour and chemical composition

    International Dairy Journal

    (1993)
  • C. Varming et al.

    Flavour compounds and sensory characteristics of cheese powders made from matured cheeses

    International Dairy Journal

    (2013)
  • M. Yvon et al.

    Cheese flavour formation by amino acid catabolism

    International Dairy Journal

    (2001)
  • M. Alewijn

    Formation of fat-derived flavour compounds during the ripening of Gouda-type cheese

    (2006)
  • K. Arfi et al.

    Production of volatile compounds by cheese-ripening yeasts: Requirement for a methanethiol donor for S-methyl thioacetate synthesis by Kluyveromyces lactis

    Applied Microbiology and Biotechnology

    (2002)
  • T.L. Bannerman et al.

    Pulsed-field gel electrophoresis as a replacement for bacteriophage typing of Staphylococcus aureus

    Journal of Clinical Microbiology

    (1995)
  • L. Barron et al.

    Variations in volatile compounds and flavour in Idiazabal cheese manufactured from ewe's milk in farmhouse and factory

    Journal of the Science of Food and Agriculture

    (2005)
  • T. Bintsis et al.

    Protease, peptidase and esterase activities by lactobacilli and yeast isolates from Feta cheese brine

    Journal of Applied Microbiology

    (2003)
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