Growth ofDebaryomyces hansenii andSaccharomyces cerevisiae in relation to pH and salinity

doi:10.1016/0147-5975(81)90025-6

Experimental Mycology

Volume 5, Issue 3, September 1981, Pages 217-228

Experimental Mycolog...

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Abstract

Debaryomyces hansenii is able to grow more readily in the presence of high concentrations of sodium and in alkaline media thanSaccharomyces cerevisiae. However, pH 5.2 depresses growth (cell numbers) of both yeasts. The effect can be reduced by the salts of weak acids in the medium. Increased cell numbers are accompanied by increased cell potassium concentration. WhenD. hansenii grows in alkaline medium, it is better able to select for potassium against sodium than when it is grown in more acid medium. The ability of bicarbonate to stimulate growth ofD. hansenii but notS. cerevisiae in acid pH, and the lack of proton excretion byD. hansenii in alkaline medium suggest that for yeast: (i) the production of an alkaline cytoplasm removes hydrogen ions from competing with sodium for exchange with potassium across the plasmalemma, and (ii) there may be a bicarbonate pump at that membrane not present inS. cerevisiae.

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Indicator fungi were originally isolated from spoilt fermented milk products. A CDIM was developed on the basis of defined media previously reported for growth of LAB (Morishita, Fukada, Shirota, & Yura, 1974; Møretrø, Hagen, & Axelsson, 1998; Saguir & de Nadra, 2007; Savijoki, Suokko, Palva, & Varmanen, 2006b), PAB (Dherbécourt, Maillard, Catheline, & Thierry, 2008; Glatz & Anderson, 1988), moulds (Bockelmann, Portius, Lick, & Heller, 1999; Emeh & Marth, 1976; Meyers & Knight, 1958) and yeasts (Andersen, Renshaw, & Wiebe, 2003; Hobot & Jennings, 1981), respectively. The medium was combined based on the published minimum requirements of any of the species investigated.
There is a growing interest for using natural preservatives in the food and dairy industries including the application of bacterial cultures to inhibit fungal spoilage. Several antifungal metabolites from bacteria have been identified, but their relative importance has been difficult to establish. In dynamic systems such as fermented milk products, the complexity of the food matrix affects detection, identification and quantification of antifungal metabolites, and thereby the understanding of the bacterial–fungal interactions. To ease the identification and quantification of bacterial metabolites (as judged by ultra-performance liquid chromatography/mass spectrometry) a chemically defined interaction medium (CDIM) was developed. The medium supported growth of antifungal cultures such as Lactobacillus paracasei and Propionibacterium freudenreichii, as well as spoilage moulds and yeasts isolated from fermented milk products. Both strong and weak antifungal interactions observed in milk could be reproduced in CDIM. The medium seems suitable for studying antifungal activity of bacterial cultures.
The effect of medium structure complexity on the growth of Saccharomyces cerevisiae in gelatin-dextran systems
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As such, it is important to characterize the growth behavior of spoilage yeasts, and more specifically S. cerevisiae, as a function of different environmental factors in order to prevent food spoilers from growing. Abundant literature is available on unraveling the effect of environmental factors such as temperature, pH and water activity on the growth of S. cerevisiae in liquid systems (Arroyo-López et al., 2009; Hobot and Jennings, 1981; Kalathenos et al., 1995; Nielsen and Arneborg, 2007; Praphailong and Fleet, 1997; Thomas et al., 2002; Watson, 1970). However, most food products have a (semi-)solid structure, causing micro-organisms to be immobilized and forced to grow as colonies.
As most food systems are (semi-)solid, the effect of food structure on bacterial growth has been widely acknowledged. However, studies on the growth dynamics of yeasts have neglected the effect of food structure.
In this paper, the growth dynamics of the spoilage yeast Saccharomyces cerevisiae was investigated at 23.5 °C in broth, singular, homogeneous biopolymer systems and binary biopolymer systems with a heterogeneous microstructure. The biopolymers gelatin and dextran were used to introduce the different levels of structure. The metabolizing ability of gelatin and dextran by S. cerevisiae was examined. To study microbial behavior in the binary systems at the micro level, mixtures were imaged with confocal laser scanning microscopy (CLSM). Growth dynamics and microscopic images of S. cerevisiae were compared with those obtained for Escherichia coli in the same model system (Boons et al., 2014). Different phase-separated, heterogeneous microstructures were obtained by changing the amount of added gelatin and dextran. Regardless of the microstructure, S. cerevisiae was preferentially located in the dextran phase. Metabolizing ability-tests indicated that gelatin could be consumed by S. cerevisiae but in the presence of glucose, no change in gelatin concentration was observed. No indication of dextran metabolizing ability was observed. When supplementing broth with gelatin or dextran alone, an enhanced growth rate and maximum cell density were observed. This enhancement was further increased by adding a second biopolymer, introducing a heterogeneous microstructure and hence increasing the medium structure complexity.
The results obtained indicate that food structure complexity plays a significant role in the growth dynamics of S. cerevisiae, an important food spoiler.
Contribution of volatiles to the antifungal effect of Lactobacillus paracasei in defined medium and yogurt
2015, International Journal of Food Microbiology
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To test the antifungal activity of L. paracasei DGCC 2132 in yogurt, UHT-milk (MILSANI®) was inoculated with 10 DCU/100 L YO-MIX™ 410 starter culture (DuPont Nutrition Biosciences ApS, Denmark) and 107 CFU/mL of L. paracasei DGCC 2132 followed by fermentation at 43 °C for 7 h. Yogurt without added L. paracasei DGCC 2132 was used as control. A chemically defined interaction medium (CDIM) used for growth of L. paracasei DGCC 2132 and antifungal activity tests was prepared based on defined media previously reported for growth of fungi (Andersen et al., 2003; Bockelmann et al., 1999; Emeh and Marth, 1976; Hobot and Jennings, 1981; Meyers and Knight, 1958), LAB (Morishita et al., 1974; Møretrø et al., 1998; Saguir and de Nadra, 2007; Savijoki et al., 2006) and other potential antifungal species such as propionic acid bacteria (Dherbécourt et al., 2008; Glatz and Anderson, 1988). CDIM (200 mL) was inoculated with L. paracasei DGCC 2132 (107 CFU/mL) in 250 mL blue cap flasks and fermented at 37 °C for 22 h to obtain a cell-containing fermentate (C-fermentate).
Lactic acid bacteria with antifungal properties can be used to control spoilage of food and feed. Previously, most of the identified metabolites have been isolated from cell-free fermentate of lactic acid bacteria with methods suboptimal for detecting possible contribution from volatiles to the antifungal activity. The role of volatile compounds in the antifungal activity of Lactobacillus paracasei DGCC 2132 in a chemically defined interaction medium (CDIM) and yogurt was therefore investigated with a sampling technique minimizing volatile loss. Diacetyl was identified as the major volatile produced by L. paracasei DGCC 2132 in CDIM. When the strain was added to a yogurt medium diacetyl as well as other volatiles also increased but the metabolome was more complex. Removal of L. paracasei DGCC 2132 cells from CDIM fermentate resulted in loss of both volatiles, including diacetyl, and the antifungal activity towards two strains of Penicillium spp. When adding diacetyl to CDIM or yogurt without L. paracasei DGCC 2132, marked inhibition was observed. Besides diacetyl, the antifungal properties of acetoin were examined, but no antifungal activity was observed. Overall, the results demonstrate the contribution of diacetyl in the antifungal effect of L. paracasei DGCC 2132 and indicate that the importance of volatiles may have been previously underestimated.
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Citation Excerpt :
The halotolerant, non-pathogenic, oleaginous yeast Debaryomyces hansenii is found in the sea and other hyperosmotic habitats [1,2]. D. hansenii grows in various environmental conditions including different salt concentrations [3–5], low temperatures [3] and different pHs [3,6]. In addition, D. hansenii assimilates many different carbon sources [7–9].
The branched respiratory chain in mitochondria from the halotolerant yeast Debaryomyces hansenii contains the classical complexes I, II, III and IV plus a cyanide-insensitive, AMP-activated, alternative-oxidase (AOX). Two additional alternative oxidoreductases were found in this organism: an alternative NADH dehydrogenase (NDH2e) and a mitochondrial isoform of glycerol-phosphate dehydrogenase (_MitGPDH). These monomeric enzymes lack proton pump activity. They are located on the outer face of the inner mitochondrial membrane. NDH2e oxidizes exogenous NADH in a rotenone-insensitive, flavone-sensitive, process. AOX seems to be constitutive; nonetheless, most electrons are transferred to the cytochromic pathway. Respiratory supercomplexes containing complexes I, III and IV in different stoichiometries were detected. Dimeric complex V was also detected. In-gel activity of NADH dehydrogenase, mass spectrometry, and cytochrome c oxidase and ATPase activities led to determine the composition of the putative supercomplexes. Molecular weights were estimated by comparison with those from the yeast Y. lipolytica and they were IV₂, I–IV, III₂–IV₄, V₂, I–III₂, I–III₂–IV, I–III₂–IV₂, I–III₂–IV₃ and I–III₂–IV₄. Binding of the alternative enzymes to supercomplexes was not detected. This is the first report on the structure and organization of the mitochondrial respiratory chain from D. hansenii.
The effect of pH, sodium chloride, sucrose, sorbate and benzoate on the growth of food spoilage yeasts
1997, Food Microbiology
The effects of pH, concentration of NaCl, concentration of sucrose and concentrations of sorbic and benzoic acids on growth were examined for 30 strains of food spoilage yeasts, representingDebaryomyces hansenii, Yarrowia lipolytica, Kloeckera apiculata, Zygosaccharomyces bailii, Zygosaccharomyces rouxii, Kluyveromyces marxianus, Pichia membranaefaciens, Pichia anomalaandSaccharomyces cerevisiae.Zygosaccharomyces bailiidid not grow at pH 7.0 andZ. rouxii, Kl. apiculataandP. membranaefaciensdid not grow at pH 8.0. OnlyKl. apiculatagrew at pH 1.5–2.0. The remaining species grew at pH 2.5–8.0. None of the species grew at 20% NaCl but strains ofD. hansenii, Z. rouxiiandP. anomalagrew at 15% NaCl.S. cerevisiaeandK. marxianuswere the least salt tolerant, showing no growth at 7.5% NaCl and 10% NaCl, respectively. Medium pH influenced growth in the presence of NaCl. ForY. lipolytica, D. hanseniiandS. cerevisiae, greatest tolerance of NaCl occurred at pH 5.0–7.0, but forKl.apiculata, D. membranaefaciensandZ. bailiibest tolerance occurred at pH 3.0.K. apiculatagrew in the presence of 12.5% NaCl at pH 2.0. All yeasts grew at 50% sucrose, withZ. rouxii, Z. bailiiandP. anomalaandD. hanseniigrowing at 60–70% sucrose. Medium pH in the range 2.0–7.0 had little effect on ability to grow in the presence of high sucrose concentrations.Z. bailiiandY. lipolyticawere the species most tolerant of sorbate and benzoate preservatives (750–1200 mg l⁻¹) at pH 5.0.
Effect of sodium chloride on growth characteristics of the marine yeast Debaryomyces hansenii in batch and continuous culture under carbon and potassium limitation
1990, Mycological Research
Debaryomyces hansenii has been grown in relatively large volume (> 1 l) batch culture in media with initial pH of 5·0, 7·2 and 8·3 in the presence and absence of added 1·5 m-NaCl. The pH of the medium was either maintained or allowed to change. The characteristics of growth appeared to be very similar in all treatments, except that the lag phase was extended by the presence of 1·5 MNaCl.
The yeast was also grown in continuous culture under carbon limitation in the presence or absence of added 1·5 M-NaCl with the pH either uncontrolled or maintained at pH 8·3. Step-up studies showed that the yeast adjusts osmotically by two mechanisms. One is relatively short-term and involves an influx of sodium while the other involves the loss of sodium from the cell. Both are associated with the synthesis of glycerol. Analysis of yields of biomass and mol content of solutes within the cells, both per mol of glucose utilized, showed that at the lower specific growth rates cells were glucose-limited but energy-limited at higher rates. The specific growth rate at which the cells became energy-limited was lower in saline media (and lowest when the pH was maintained at 8·3). When the culture was glucose limited, in non-saline conditions, growth was very much dependent on the absorption of potassium, whose intracellular content per mol of glucose utilized was much greater than that of any other measured solute. In saline conditions with an acidic medium, much of the glucose utilized was expended in generating the appropriate solute potential primarily with glycerol and sodium. The conditions under which the cells are energy-limited are considered in relation to the futile cycling of glycerol and the maintenance of an appropriate gradient of protons across the plasmalemma in an alkaline medium. Potassium-limitation in continuous culture was studied in media of low salinity and of high salinity (0·5 m-NaCl) with the pH either uncontrolled externally or maintained at either 5·5 or 8·3. The major osmolytes appeared to be potassium and glycerol in low salinity media and sodium, glycerol and arabitol in 0·5 m-NaCl. The relationship between yield and the internal concentration of potassium per mol of glucose utilized for any one medium indicated that the production of biomass and the uptake of potassium are closely related. Glycerol concentration per mol of glucose utilized was proportional to yield in all media; at pH 8·3 in the 0·5 m-NaCl medium relatively less arabitol was produced. The highest cellular concentrations of sodium and glycerol were observed in this medium at the higher specific growth rates. These studies confirm previous data showing that in saline media growth of the yeast under alkaline conditions is physiologically different from that in acid conditions.

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¹: Present address: Biozentrum der Universita¨t Basel, Abteilung Mikrobiologie, Klingelbergstrasse 70, CH-4056 Basel, Switzerland.

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Growth ofDebaryomyces hansenii andSaccharomyces cerevisiae in relation to pH and salinity

Abstract

Biochim. Biophys. Acta

Advan. Microbial Physiol.

Trans. Brit. Mycol. Soc.

Arch. Biochem. Biophys.

Biochim. Biophys. Acta

Biochem. J.

Polyhydric alcohol production and intracellular amino acid pool in relation to halotolerance of the yeastDebaryomyces hansenii

Arch. Microbiol.

The stoicheiometry of the absorption of protons with phosphate and L-glutamate by yeasts of the genusSaccharomyces

Biochem. J.

Biological production of acid and alkali. 1. Quantitative relations of succinic and carbonic acids to the potassium and hydrogen exchange in fermenting yeast

Biochem. J.

The nature of cation exchange during yeast fermentation with formation of 0.02 normal H ion

Biochem. J.

Control of and by pH