Selection of Debaryomyces hansenii isolates to improve quality of dry fermented sausage

Figures & data

Table 1. Information of Debaryomyces hansenii isolates from fermented foods.

Fermented food	Food number	Isolate
Cheese	Cheese-1	D. hansenii SMFM2021-C1
	Cheese-2	D. hansenii SMFM2021-C3
	Cheese-2	D. hansenii SMFM2021-C4
	Cheese-3	D. hansenii SMFM2021-C5
	Cheese-2	D. hansenii SMFM2021-C7
	Cheese-4	D. hansenii SMFM2021-C8
	Cheese-5	D. hansenii SMFM2021-C9
	Cheese-6	D. hansenii SMFM2021-C10
	Cheese-7	D. hansenii SMFM2021-C12
	Cheese-8	D. hansenii SMFM2021-C14
	Cheese-8	D. hansenii SMFM2021-C15
Fermented sausage	Fermented sausage-1	D. hansenii SMFM2021-S1
	Fermented sausage-1	D. hansenii SMFM2021-S2
	Fermented sausage-1	D. hansenii SMFM2021-S3
	Fermented sausage-1	D. hansenii SMFM2021-S4
	Fermented sausage-2	D. hansenii SMFM2021-S5
	Fermented sausage-3	D. hansenii SMFM2021-S6
	Fermented sausage-4	D. hansenii SMFM2021-S8
Dry aged beef	Dry aged beef-1	D. hansenii SMFM2021-SL1
	Dry aged beef-1	D. hansenii SMFM2021-SL2
	Dry aged beef-1	D. hansenii SMFM2021-SL3
Soybean paste	Soybean paste-1	D. hansenii SMFM2021-D1

Table 2. Information of non-Debaryomyces hansenii isolates from fermented foods.

Sympathetic name	Fermented food	Isolates number
Wickerhamomyces anomalus	Meju	12
	Nuruk	9
	Gochujang	1
Candida zelanoides	Fermented sausage	6
	Dry-aged beef	2
Saccharomyces cerevisiae	Makgeolli	1
	Wine	1
Debaryomyces spp.	Fermented sausage	1
Zygosaccharomyces rouxii	Soybean paste	5
	Gochujang	2
Yarrowia galli	Fermented sausage	1
Torulaspora delbrueckii	Fermented sausage	1
Unknown	-	7
Total		49

Table 3. Lipolytic enzyme activity of Debaryomyces hansenii isolates.

D. hansenii isolates	Lipolytic enzyme activity
D. hansenii SMFM2021-C1	-1)
D. hansenii SMFM2021-C3	++2)
D. hansenii SMFM2021-C4	-
D. hansenii SMFM2021-C5	++
D. hansenii SMFM2021-C7	-
D. hansenii SMFM2021-C8	++
D. hansenii SMFM2021-C9	++
D. hansenii SMFM2021-C10	+3)
D. hansenii SMFM2021-C12	++
D. hansenii SMFM2021-C14	++
D. hansenii SMFM2021-C15	+
D. hansenii SMFM2021-S1	-
D. hansenii SMFM2021-S2	+
D. hansenii SMFM2021-S3	++
D. hansenii SMFM2021-S4	-
D. hansenii SMFM2021-S5	++
D. hansenii SMFM2021-S6	+
D. hansenii SMFM2021-S8	+
D. hansenii SMFM2021-SL1	++
D. hansenii SMFM2021-SL2	+
D. hansenii SMFM2021-SL3	++
D. hansenii SMFM2021-D1	++

¹⁾-: no fluorescence in a lipolysis medium

²⁾++: high fluorescence in a lipolysis medium

³⁾+: medium fluorescence in a lipolysis medium

Figure 1. Growth rates of Debaryomyces hansenii isolates at 25°C under acidic environment at pH 3.5.

Figure 2. Tolerance of Debaryomyces hansenii isolates to 2 M NaCl stresses (C9: D. hansenii SMFM2021-C9; C10: D. hansenii SMFM2021-C10; C12: D. hansenii SMFM2021-C12; C14: D. hansenii SMFM2021-C14; SL1: D. hansenii SMFM2021-SL1; SL2: D. hansenii SMFM2021-SL2; SL3: D. hansenii SMFM2021-SL3; D1: D. hansenii SMFM2021-D1; S2: D. hansenii SMFM2021-S2; S8: D. hansenii SMFM2021-S8).

Table 4. Microbiological cell counts (Log CFU/g; mean ± standard deviation) in dry fermented sausages inoculated with Debaryomyces hansenii isolates SMFM2021-C14, SMFM2021-S8, and SMFM2021-SL3 during fermentation and aging at 15–20°C for 3 weeks.

Week	Treatments	E. coli O157:H7	Coliform	L. monocytogenes	Salmonella	P. pentosaceus	Yeast	S. xylosus
0	Control	<0.5^1	1.3±0.3	<0.5	<0.5	6.3±0.1^A	3.0±0.1^B	6.7±0.1^AB
	D. hansenii SMFM2021-C14	<0.5	1.5±0.2	<0.5	<0.5	6.1±0.1^B	5.7±0.1^A	6.6±0.1^B
	D. hansenii SMFM2021-S8	<0.5	1.5±0.2	<0.5	<0.5	6.1±0.1^B	5.6±0.1^A	6.8±0.1^AB
	D. hansenii SMFM2021-SL3	<0.5	1.6±0.3	<0.5	<0.5	5.7±0.1^C	5.7±0.1^A	6.4±0.1^C
1	Control	<0.5	0.6±0.2	<0.5	<0.5	6.6±0.1^B	5.3±0.3^B	7.7±0.4^AB
	D. hansenii SMFM2021-C14	<0.5	0.7±0.2	<0.5	<0.5	6.7±0.3^AB	7.7±0.8^A	7.6±0.5^B
	D. hansenii SMFM2021-S8	<0.5	0.8±0.3	<0.5	<0.5	7.1±0.6^A	7.8±0.4^A	8.2±0.3^A
	D. hansenii SMFM2021-SL3	<0.5	0.6±0.2	<0.5	<0.5	6.9±0.1^AB	7.7±0.2^A	7.9±0.2^AB
2	Control	<0.5	0.6±0.2	<0.5	<0.5	6.5±0.2^A	5.7±0.2^C	7.8±0.2^B
	D. hansenii SMFM2021-C14	<0.5	0.8±0.6	<0.5	<0.5	6.7±0.2^A	8.1±0.2^A	7.9±0.1^AB
	D. hansenii SMFM2021-S8	<0.5	0.6±0.3	<0.5	<0.5	6.7±0.3^A	7.9±0.3^A	8.2±0.4^A
	D. hansenii SMFM2021-SL3	<0.5	0.9±0.4	<0.5	<0.5	6.6±0.2^A	7.3±0.1^B	7.7±0.3^B
3	Control	<0.5	0.8±0.4	<0.5	<0.5	6.5±0.2^B	5.1±0.2^C	7.3±0.3^C
	D. hansenii SMFM2021-C14	<0.5	0.6±0.4	<0.5	<0.5	6.7±0.2^A	7.4±0.3^A	7.6±0.2^B
	D. hansenii SMFM2021-S8	<0.5	0.7±0.6	<0.5	<0.5	6.6±0.2^AB	7.4±0.3^A	7.9±0.1^A
	D. hansenii SMFM2021-SL3	<0.5	0.7±0.3	<0.5	<0.5	6.6±0.3^AB	7.0±0.2^B	7.6±0.1^B

¹⁾Below detection limit

^A-C)Values with different capital letters within same week differ significantly (p < .05).

Figure 3. Weight loss (a), changes in reducing sugar (b), and changes in volatile basic nitrogen concentrations (c) of dry fermented sausage inoculated with Debaryomyces hansenii isolates SMFM2021-C14, SMFM2021-S8, and SMFM2021-SL3 during fermentation and aging at 15–20°C for 3 weeks.

Table 5. Water activity (A_w) and pH (mean ± standard deviation) of dry fermented sausages inoculated with Debaryomyces hansenii isolates SMFM2021-C14, SMFM2021-S8, and SMFM2021-SL3 during fermentation and aging at 15–20°C for 3 weeks.

Treatments	Water activity (Aw)				pH
	Fermentation and aging (week)				Fermentation and aging (week)
	0	1	2	3	0	1	2	3
Control	0.998 ± 0.002^Aa	0.954 ± 0.012^Ab	0.866 ± 0.017^ABc	0.794 ± 0.003^Ad	5.99 ± 0.02^Aa	5.25 ± 0.01^ABb	5.25 ± 0.03^Cb	5.21 ± 0.02^Bc
D. hansenii SMFM2021-C14	0.981 ± 0.008^Aa	0.951 ± 0.009^Ab	0.887 ± 0.018^ABc	0.773 ± 0.008^Bd	5.98 ± 0.03^Aa	5.27 ± 0.15^Abc	5.37 ± 0.05^Bb	5.21 ± 0.06^Bc
D. hansenii SMFM2021-S8	0.980 ± 0.003^Aa	0.947 ± 0.014^Ab	0.898 ± 0.014^Ac	0.796 ± 0.010^Ad	5.99 ± 0.02^Aa	5.15 ± 0.08^Cd	5.46 ± 0.01^Ab	5.33 ± 0.10^Ac
D. hansenii SMFM2021-SL3	0.968 ± 0.034^Aa	0.958 ± 0.010^Aa	0.859 ± 0.049^Bb	0.797 ± 0.005^Ac	5.97 ± 0.00^Aa	5.16 ± 0.02^BCd	5.35 ± 0.02^Bb	5.30 ± 0.03^Ac

^a-d)Values with different small letters within the same row differ significantly (p < .05)

^A-C)Values with different capital letters within the same column differ significantly (p < .05)

Table 6. Changes in the thiobarbituric acid reactive substance (malondialdehyde/kg; mean ± standard deviation) in dry fermented sausages inoculated with Debaryomyces hansenii isolates SMFM2021-C14, SMFM2021-S8, and SMFM2021-SL3 during fermentation and aging at 15–20°C for 3 weeks.

Treatments	Fermentation and aging (week)
	0	1	2	3
Control	0.55 ± 0.04^Aa	0.49 ± 0.02^Ab	0.40 ± 0.02^Ac	0.38 ± 0.00^Ac
D. hansenii SMFM2021-C14	0.57 ± 0.04^Aa	0.39 ± 0.03^Bb	0.38 ± 0.01^Bb	0.40 ± 0.01^Ab
D. hansenii SMFM2021-S8	0.51 ± 0.05^Aa	0.33 ± 0.01^Cb	0.36 ± 0.01^Cb	0.34 ± 0.01^Bb
D. hansenii SMFM2021-SL3	0.55 ± 0.04^Aa	0.33 ± 0.03^Cc	0.40 ± 0.00^Ab	0.40 ± 0.02^Ab

^a-c)Values with different small letters within the same row differ significantly (p < .05)

^A-C)Values with different capital letters within the same column differ significantly (p < .05)

Table 7. Color (mean ± standard deviation) of dry fermented sausages inoculated with Debaryomyces hansenii isolates SMFM2021-C14, SMFM2021-S8, and SMFM2021-SL3 during fermentation and aging at 15–20°C for 3 weeks.

Treatments	Lightness (L* value)				Redness (a* value)				Yellowness (b* value)
	Fermentation and aging (week)				Fermentation and aging (week)				Fermentation and aging (week)
	0	1	2	3	0	1	2	3	0	1	2	3
Control	67.27 ±1.59^Aa	61.46 ±1.72^Bb	56.06 ±0.71^Cc	52.03 ±1.50^Bd	10.11 ±0.99^Ad	11.79 ±1.16^Ab	13.43 ±0.57^Ac	14.97 ±0.76^Ba	14.61 ±1.08^Aa	11.43 ±0.26^ABc	11.18 ±0.51^Bc	12.29 ±0.82^Bb
D. hansenii SMFM2021-C14	68.65 ±1.36^Aa	62.89 ±1.75^ABb	57.82 ±1.13^Bc	54.28 ±3.06^Ad	9.94 ±0.78^Ac	10.71 ±1.47^Bc	12.34 ±0.64^Bb	14.36 ±1.02^Ba	14.23 ±0.53^Aa	11.13 ± 0.44A^Bc	11.26 ±0.72^Bbc	11.70 ±0.88^Bb
D. hansenii SMFM2021-S8	68.74 ±1.37^Aa	62.01 ±0.72^ABb	59.28 ±0.40^Ac	54.11 ±1.70^Ad	9.72 ±0.37^Ac	11.58 ±0.47^ABb	11.87 ±0.61^Bb	14.96 ±0.40^Aa	14.45 ±0.32^Aa	11.52 ± 0.47^Ac	11.90 ±0.32^Ac	13.30 ±0.44^Ab
D. hansenii SMFM2021-SL3	67.89 ±1.85^Aa	63.10 ±1.73^ABb	57.97 ±1.89^Bc	55.93 ±1.32^Ad	9.51 ±1.08^Ad	10.81 ±0.86^ABc	11.86 ±0.94^Bb	13.87 ±0.94^Aa	14.14 ±0.95^Aa	11.02 ±0.65^Bc	11.54 ±0.36^ABc	13.18 ±0.69^Ab

^a-c)Values with different small letters within the same row differ significantly (p < .05)

^A-C)Values with different capital letters within the same column differ significantly (p < .05)

Table 8. Texture profile (g; mean ± standard deviation) of dry fermented sausage inoculated with Debaryomyces hansenii isolates SMFM2021-C14, SMFM2021-S8, and SMFM2021-SL3 during fermentation and aging at 15–20°C for 3 weeks.

Treatment	Hardness				Springiness				Chewiness				Gumminess
	Fermentation and aging (week)				Fermentation and aging (week)				Fermentation and aging (week)				Fermentation and aging (week)
	0	1	2	3	0	1	2	3	0	1	2	3	0	1	2	3
Control	174.24 ±34.24^Ac	2593.79 ±239.21^Ab	4480.22 ±430.28^Aa	NA*	0.98 ±0.04^Aa	0.82 ±0.04^Ac	0.90 ±0.08 ^Bb	NA*	138.84 ±33.40^Ac	1636.72 ±277.21^Ab	3434.79 ±479.69^Aa	NA*	141.85 ±34.60^Ac	1981.14 ±280.57^Ab	3785.34 ±350.72^Aa	NA*
D. hansenii SMFM2021-C14	179.01 ±23.28^Ac	2171.09 ±333.83^Bb	4593.42 ±288.95^Aa		0.95 ±0.05^Aa	0.89 ±0.09^Aa	0.95 ±0.07^ABa		136.96 ±27.58^Ac	1507.92 ±172.49^ABb	3430.04 ±363.50^Aa		142.75 ±24.68^Ac	1693.04 ±222.69^Bb	3614.58 ±210.13^Aa
D. hansenii SMFM2021-S8	154.26 ±28.42^Ac	2088.58 ±301.14^Bb	3368.10 ±339.06^Ba		0.96 ±0.05^Aa	0.82 ±0.08^Ab	0.99 ±0.04^Aa		113.87 ±24.33^Ac	1274.62 ±223.55^Bb	2983.25 ±430.38^Ba		118.39 ±25.59^Ac	1551.43 ±216.74^Bb	2998.54 ±365.85^Ba
D. hansenii SMFM2021-SL3	160.90 ±23.34^Ac	2206.14 ±153.79^Bb	3469.73 ±389.14^Ba		0.96 ±0.06^Aa	0.91 ±0.18^Aa	0.93 ±0.07^ABa		120.02 ±24.82^Ac	1560.24 ±359.43^Ab	2551.86 ±94.95^Ca		124.56 ±22.43^Ac	1704.49 ±109.06^Bb	2747.25 ±366.83^Ba

^a-c)Values with different small letters within the same row differ significantly (p < .05)

^A-C)Values with different capital letters within the same column differ significantly (p < .05)

*Not analyzed

Table 9. Free fatty acids composition (%; mean ± standard deviation) of dry fermented sausages inoculated with Debaryomyces hansenii isolates SMFM2021-C14, SMFM2021-S8, and SMFM2021-SL3.

Free fatty acid	Fermentation and aging (week)
	0	3
	Control	Control	D. hansenii SMFM2021-C14	D. hansenii SMFM2021-S8	D. hansenii SMFM2021-SL3
Butyric acid	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A
Caproic acid	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A
Caprylic acid	0.008 ± 0.004^A	0.008 ± 0.002^A	0.009 ± 0.000^A	0.010 ± 0.000^A	0.009 ± 0.000^A
Capric acid	0.087 ± 0.003^A	0.083 ± 0.001^B	0.083 ± 0.001^B	0.084 ± 0.002^AB	0.082 ± 0.002^B
Undecanoic acid	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A
Lauric acid	0.212 ± 0.006^C	0.216 ± 0.001^BC	0.216 ± 0.002^BC	0.221 ± 0.004^AB	0.225 ± 0.000^A
Tridecanoic acid	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A
Myristic acid	1.764 ± 0.008^AB	1.770 ± 0.002^A	1.764 ± 0.005^AB	1.755 ± 0.007^BC	1.747 ± 0.004^C
Myristoleic acid	0.036 ± 0.001^B	0.040 ± 0.002^A	0.038 ± 0.000^AB	0.039 ± 0.002^A	0.039 ± 0.000^A
Pentadecanoic acid	0.097 ± 0.006^B	0.097 ± 0.004^B	0.098 ± 0.001^B	0.101 ± 0.001^B	0.108 ± 0.003^A
Pentadecanoic acid	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A
Palmitic acid	23.226 ± 0.040^A	23.147 ± 0.071^A	23.205 ± 0.074^A	22.972 ± 0.152^B	22.925 ± 0.041^B
Palmitoleic acid	2.279 ± 0.067^A	2.236 ± 0.016^AB	2.271 ± 0.010^AB	2.210 ± 0.009^B	2.248 ± 0.038^AB
Margaric acid	0.509 ± 0.017^D	0.520 ± 0.010^CD	0.531 ± 0.001^BC	0.541 ± 0.008^B	0.587 ± 0.005^A
Heptadecenoic acid	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A
Stearic acid	11.643 ± 0.031^A	11.591 ± 0.164^AB	11.559 ± 0.059^AB	11.640 ± 0.052^A	11.479 ± 0.029^B
Oleic acid (trans)	0.430 ± 0.017^A	0.436 ± 0.005^A	0.430 ± 0.009^A	0.432 ± 0.003^A	0.431 ± 0.005^A
Oleic acid (cis)	42.557 ± 0.090^A	42.432 ± 0.043^B	42.470 ± 0.033^AB	42.504 ± 0.030^AB	42.439 ± 0.098^AB
Linoleic acid (trans)	0.269 ± 0.004^B	0.337 ± 0.031^A	0.264 ± 0.018^B	0.271 ± 0.031^B	0.286 ± 0.010^B
Linoleic acid (cis)	13.560 ± 0.096^C	13.785 ± 0.198^BC	13.783 ± 0.060^BC	13.892 ± 0.151^AB	14.086 ± 0.112^A
Arachidic acid	0.174 ± 0.001^BC	0.175 ± 0.003^AB	0.173 ± 0.000^BC	0.177 ± 0.002^A	0.171 ± 0.000^C
γ-linolenic acid	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A
Linolenic acid	0.639 ± 0.007^B	0.641 ± 0.015^B	0.648 ± 0.003^B	0.651 ± 0.011^B	0.669 ± 0.006^A
Gadoleic acid	0.952 ± 0.007^A	0.960 ± 0.009^A	0.941 ± 0.003^A	0.957 ± 0.001^A	0.947 ± 0.025^A
Heneicosanoic acid	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A
Eicosadienoic acid	0.634 ± 0.011^B	0.634 ± 0.003^B	0.635 ± 0.003^B	0.651 ± 0.005^A	0.657 ± 0.006^A
Behenic acid	0.012 ± 0.000^A	0.012 ± 0.002^A	0.013 ± 0.002^A	0.013 ± 0.000^A	0.012 ± 0.000^A
Dihomo-gamma-linolenic acid	0.152 ± 0.005^A	0.148 ± 0.003^A	0.150 ± 0.001^A	0.150 ± 0.002^A	0.147 ± 0.000^A
Erucic acid	0.055 ± 0.011^A	0.045 ± 0.000^B	0.042 ± 0.002^B	0.044 ± 0.000^B	0.042 ± 0.000^B
Eicosatrienoic acid	0.101 ± 0.002^B	0.104 ± 0.002^A	0.103 ± 0.001^AB	0.104 ± 0.001^AB	0.105 ± 0.000^A
Arachidonic acid	0.519 ± 0.016^A	0.505 ± 0.022^A	0.498 ± 0.004^AB	0.507 ± 0.007^A	0.479 ± 0.002^B
Tricosanoic acid	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A	0.000 ± 0.000^A
Brassic acid	0.012 ± 0.000^B	0.013 ± 0.000^A	0.012 ± 0.000^B	0.013 ± 0.000^A	0.012 ± 0.000^B
Lignoceric acid	0.012 ± 0.000^A	0.009 ± 0.002^B	0.009 ± 0.000^B	0.010 ± 0.000^B	0.009 ± 0.000^B
EPA	0.010 ± 0.003^A	0.010 ± 0.000^A	0.011 ± 0.002^A	0.010 ± 0.000^A	0.010 ± 0.002^A
Nervonic acid	0.028 ± 0.004^A	0.030 ± 0.010^A	0.024 ± 0.003^A	0.025 ± 0.003^A	0.034 ± 0.002^A
DHA	0.022 ± 0.003^A	0.019 ± 0.000^A	0.020 ± 0.002^A	0.019 ± 0.000^A	0.019 ± 0.002^A
SFA^1)	37.744 ± 0.053^A	37.625 ± 0.231^A	37.660 ± 0.121^A	37.480 ± 0.186^AB	37.352 ± 0.023^B
USFA^2)	62.256 ± 0.053^B	62.375 ± 0.231^B	62.340 ± 0.121^B	62.520 ± 0.186^AB	62.648 ± 0.023^A
MUFA^3)	46.338 ± 0.128^A	46.179 ± 0.049^B	46.216 ± 0.033^AB	46.238 ± 0.028^AB	46.180 ± 0.117^B
PUFA^4)	15.918 ± 0.082^C	16.196 ± 0.219^ABC	16.124 ± 0.088^BC	16.326 ± 0.272^AB	16.468 ± 0.124^A
USFA/SFA	1.649 ± 0.004^B	1.658 ± 0.016^B	1.655 ± 0.008^B	1.668 ± 0.013^AB	1.677 ± 0.002^A
Total fatty acids	16.497 ± 0.229^E	31.042 ± 0.152^D	33.846 ± 0.246^A	31.967 ± 0.184^C	33.358 ± 0.048^B
ω−3	0.772 ± 0.002^B	0.774 ± 0.017^B	0.782 ± 0.004^B	0.787 ± 0.012^B	0.802 ± 0.005^A
ω−6	0.671 ± 0.021^A	0.653 ± 0.024^A	0.648 ± 0.005^AB	0.649 ± 0.008^A	0.626 ± 0.002^B
ω−6/ω−3	0.869 ± 0.026^A	0.844 ± 0.049^A	0.829 ± 0.006^A	0.826 ± 0.003^A	0.780 ± 0.005^B

¹⁾Saturated fatty acid

²⁾Unsaturated fatty acid

³⁾Monounsaturated fatty acid

⁴⁾Polyunsaturated fatty acid