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Food Microbiology

Molecular and Biochemical Analysis of the Galactose Phenotype of Dairy Streptococcus thermophilus Strains Reveals Four Different Fermentation Profiles

Filip de Vin, Peter Rådström, Lieve Herman, Luc De Vuyst
Filip de Vin
1Research Group of Industrial Microbiology, Fermentation Technology and Downstream Processing (IMDO), Department of Applied Biological Sciences, Vrije Universiteit Brussel (VUB), Pleinlaan 2, B-1050 Brussels, Belgium
2Applied Microbiology, Lund Institute of Technology, Lund University, SE-221 00 Lund, Sweden
3Department for Animal Product Quality and Transformation Technology, Centre for Agricultural Research-Ghent, Brusselsesteenweg 370, B-9090 Melle, Belgium
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Peter Rådström
2Applied Microbiology, Lund Institute of Technology, Lund University, SE-221 00 Lund, Sweden
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Lieve Herman
3Department for Animal Product Quality and Transformation Technology, Centre for Agricultural Research-Ghent, Brusselsesteenweg 370, B-9090 Melle, Belgium
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Luc De Vuyst
1Research Group of Industrial Microbiology, Fermentation Technology and Downstream Processing (IMDO), Department of Applied Biological Sciences, Vrije Universiteit Brussel (VUB), Pleinlaan 2, B-1050 Brussels, Belgium
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  • For correspondence: ldvuyst@vub.ac.be
DOI: 10.1128/AEM.71.7.3659-3667.2005
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  • FIG. 1.
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    FIG. 1.

    Four typical batch fermentation profiles as found among 49 S. thermophilus strains when grown in M17 medium with 0.5% (wt/vol) lactose at 42°C. S. thermophilus IMDOST04, S. thermophilus IMDOST10, S. thermophilus IMDOST07, and S. thermophilus IMDOST40 are representative strains for fermentation profiles A, B, C, and D, respectively. The black arrows in fermentation profile C indicate the different sampling points for enzyme activity measurements. Symbols: ▴, galactose; ▵, lactic acid; ▪, OD620; □, lactose.

  • FIG. 2.
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    FIG. 2.

    Alignment of the eight different nucleotide sequences (NS) as found in the galR-galK intergenic region of 49 wild-type S. thermophilus strains. The intergenic region contains the promoter sequences for the galR and the gal genes. The promoter regions are defined according to Vaughan et al. (30). The −10 and −35 regions are underlined, and the transcriptional start sites are indicated at +1.

  • FIG. 3.
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    FIG. 3.

    Genetic relationship among the 49 S. thermophilus strains as estimated by clustering analysis of RAPD patterns obtained with primer XD9 (15). The dendrogram was generated by the unweighted pair group method. The three columns on the right give the strain name, the nucleotide sequence (NS) of the galR-galK intergenic region, and the type of fermentation profile. Galactose-positive strains are indicated with an asterisk.

Tables

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  • TABLE 1.

    Biokinetic parameters of Streptococcus thermophilus strains grown in M17 medium containing 0.5% (wt/vol) lactose

    StrainSource (original reference)aμmax (h−1)bYX/SbYP/SbYGal,LacbFermentation profile
    IMDOST01Greek yogurt (ACA-DC 492)1.930.370.480.47B
    IMDOST02Greek yogurt (ACA-DC 491)1.820.360.560.42B
    IMDOST03Greek yogurt (ACA-DC 490)1.880.330.560.44B
    IMDOST04Unknown (5FT)1.820.350.500.44B
    IMDOST05Greek yogurt (ACA-DC 611)1.580.340.560.41B
    IMDOST06Unknown [(t) 359]1.520.310.460.45B
    IMDOST07Greek yogurt (ACA-DC 511)1.710.370.510.51C
    IMDOST08Greek yogurt (ACA-DC 595.1)1.460.330.620.38C
    IMDOST09Greek yogurt (ACA-DC 615)1.730.380.660.42C
    IMDOST10Greek yogurt (ACA-DC 619)1.740.360.440.44B
    IMDOST11Industrial yogurt starter (UN 1YRF)1.680.410.610.33C
    IMDOST12Industrial yogurt starter (UN 7FT)1.440.320.480.45A
    IMDOST13Greek yogurt (ACA-DC 602.1)1.720.320.490.43B
    IMDOST14Industrial yogurt starter (UN 4L)2.020.360.450.43B
    IMDOST15Greek yogurt (ACA-DC 487)1.310.310.390.44B
    IMDOST16Greek yogurt (ACA-DC 486)1.620.320.400.45B
    IMDOST17Greek yogurt (ACA-DC 482)1.620.330.460.44B
    IMDOST18Greek yogurt (ACA-DC 481)1.850.360.450.42B
    IMDOST19Industrial yogurt starter (UN 5FR)1.630.340.450.42B
    IMDOST21Greek yogurt (ACA-DC 489)1.890.510.580.43B
    IMDOST22Greek yogurt (ACA-DC 488)1.580.400.680.41C
    IMDOST23Greek yogurt (ACA-DC 623.1)1.580.480.670.34C
    IMDOST24Industrial yogurt starter (Yoplait C417)1.610.460.670.34C
    IMDOST25Industrial yogurt starter (UN 7FT)1.740.390.520.47B
    IMDOST26Unknown (510)1.410.410.490.44B
    IMDOST27Industrial yogurt starter (UN 6FC)1.640.370.460.42B
    IMDOST28Unknown (NR)1.780.340.460.44A
    IMDOST29Industrial yogurt starter (UN ATX)1.730.360.370.42B
    IMDOST30Unknown (4)1.660.410.470.49B
    IMDOST31Yoghurt (NCFB 2393)1.800.390.520.41B
    IMDOST32Greek yogurt (ACA-DC 613)1.960.340.440.39B
    IMDOST33Unknown (Gal+)1.960.380.490.44B
    IMDOST34Greek yogurt (ACA-DC 638)1.530.390.590.37B
    IMDOST36Industrial yogurt starter (LY03)1.660.340.420.51B
    IMDOST37Industrial yogurt starter (Sfi20)1.750.370.460.42B
    IMDOST38Industrial yogurt starter (BTC)1.550.320.470.45B
    IMDOST39Greek yogurt (ACA-DC 480)1.750.330.440.41B
    IMDOST40Industrial yogurt starter (EU20)1.760.800.950D
    IMDOST41Industrial yogurt starter (STCH101)2.190.400.500.50A
    IMDOST42Romanian yogurt (ACA-DC ST111)1.380.340.360.47A
    MB1655Pasteurized milk (NCFB 575)2.000.460.460.36B
    MB1656Gruyère cheese starter (NCFB 2564)1.060.280.460.45B
    MB1657Unknown (NCFB 489)1.590.380.530.40A
    MB1658Unknown (LMG 13564)1.760.460.490.46A
    MB1661Unknown2.010.470.440.38B
    MB1663Unknown (NCFB 2075)1.650.420.470.40B
    MB1664Unknown (NCFB 1242)1.850.450.500.37A
    MB1665Unknown1.910.460.580.31A
    MB1667Pasteurized milk (NCFB 574)1.770.410.580.51A
    • ↵ a ACA-DC, Collection of the Laboratory of Dairy Research, Agricultural University of Athens, Athens, Greece, LMG, BCCMTM/LMG Bacteria Culture Collection, Laboratory of Microbiology, Ghent University, Ghent, Belgium; NCFB, National Collection of Food Bacteria, Reading, United Kingdom; UN, Université de Nancy, Nancy, France.

    • ↵ b μmax, maximum specific growth rate (h−1); YX/S, cell yield coefficient (OD620 · g of substrate−1); YP/S, product yield coefficient (g of product · g of substrate−1); YGal,Lac, galactose-lactose exchange coefficient (g of galactose · g of lactose−1).

  • TABLE 2.

    Primers used in this study

    PrimerSequence
    galR FW15′-TCC TAT TCA GGT TTA TGG TT-3′
    galR REV15′-CGG AAC TAC TGT ATG GAA AA-3′
    galK FW25′-TGG TGT AGA AGC AGA TCA TA-3′
    galK REV25′-TCC AGG CGT TCC AAT TTA AT-3′
    galT FW35′-TAT GAG GAA TTG GAC CGT AT-3′
    galT REV35′-AAA CGA ACA ACA CGG TGA TT-3′
    galE FW45′-ATT AGG TGG AGC TGG TTA TA-3′
    galE REV45′-TAA CGA AGA GGG ACA TAC TT-3′
    galM FW55′-ACT TGC TAC CTC GAA TTG AA-3′
    galM REV55′-GAG ACT TCA TCT GAC CTT TA-3′
    galRK FW65′-ATC CGA TTT CAT CAG CGA TA-3′
    galRK REV65′-CGT AAG TAC CTA GGG TAA TA-3′
  • TABLE 3.

    Lactose repression of the gal genes

    StrainLactose depletionSpecific enzyme activitya (U · mg of protein−1)
    GalKGalTGAIE
    IMDOST07Before0.10 ± 0.02A6.0 ± 0.1A0.62 ± 0.00B
    After0.19 ± 0.03B11.8 ± 0.1B0.22 ± 0.00A
    IMDOST22BeforeNot detected3.7 ± 0.0A0.52 ± 0.01B
    AfterNot detected7.5 ± 0.1B0.28 ± 0.00A
    • ↵ a Means ± standard deviations. Mean values for each strain in each column with a common superscript did not differ at α = 0.05.

  • TABLE 4.

    Biokinetic parameters and specific activities of the enzymes of the Leloir operon for Gal-positive Streptococcus thermophilus strains grown in M17 medium containing 0.5% (wt/vol) galactose

    Strainaμmax (h−1)bYX/SbYP/SbgalR-galK regionGalK (U · mg−1)cGalT (U · mg−1)cGalE (U · mg−1)c
    IMDOST070.990.580.87NS10.41 ± 0.02A18.7 ± 0.2E0.33 ± 0.01B
    IMDOST081.490.480.90NS2Not detected10.3 ± 0.1C0.44 ± 0.01C
    IMDOST091.510.510.90NS2Not detected10.2 ± 0.1C0.83 ± 0.01H
    IMDOST110.730.540.89NS2Not detected9.3 ± 0.3B0.53 ± 0.001E
    IMDOST220.650.570.88NS2Not detected9.3 ± 0.4B0.68 ± 0.01G
    IMDOST231.020.660.87NS2Not detected9.4 ± 0.4B0.50 ± 0.01D
    IMDOST240.720.590.96NS6Not detected13.0 ± 0.6D0.62 ± 0.01F
    IMDOST401.710.660.98NS31.04 ± 0.05B2.7 ± 0.2A0.27 ± 0.01A
    • ↵ a The source and the original reference are given in Table 1.

    • ↵ b μmax, maximum specific growth rate (h−1); YX/S, cell yield coefficient (OD620 · g of substrate−1); YP/S, product yield coefficient (g of product · g of substrate−1)

    • ↵ c Means ± standard deviations. Mean values in each column with a common superscript did not differ at α = 0.05.

  • TABLE 5.

    Number of differences in the amino acid sequence of the translated Leloir genes of IMDOST22, IMDOST36, IMDOST40, and IMDOST42, with regard to the galactose-negative S. thermophilus strains CNRZ 302 and A147a

    U61402IMDOST22 (Gal+)IMDOST36 (Gal−)IMDOST40 (Gal+)IMDOST42 (Gal−)M38175IMDOST22 (Gal+)IMDOST36 (Gal−)IMDOST40 (Gal+)IMDOST42 (Gal−)
    GalRFrameshift0Frameshift1GalE7474
    GalK111115GalM133104
    GalT114136
    • ↵ a The latter two strains have accession numbers U61402 and M38175 , respectively.

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Molecular and Biochemical Analysis of the Galactose Phenotype of Dairy Streptococcus thermophilus Strains Reveals Four Different Fermentation Profiles
Filip de Vin, Peter Rådström, Lieve Herman, Luc De Vuyst
Applied and Environmental Microbiology Jul 2005, 71 (7) 3659-3667; DOI: 10.1128/AEM.71.7.3659-3667.2005

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Molecular and Biochemical Analysis of the Galactose Phenotype of Dairy Streptococcus thermophilus Strains Reveals Four Different Fermentation Profiles
Filip de Vin, Peter Rådström, Lieve Herman, Luc De Vuyst
Applied and Environmental Microbiology Jul 2005, 71 (7) 3659-3667; DOI: 10.1128/AEM.71.7.3659-3667.2005
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KEYWORDS

Bacterial Proteins
cheese
galactose
Streptococcus thermophilus
Yogurt

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