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Journal of Food Science and Technology logoLink to Journal of Food Science and Technology
. 2024 Aug 21;62(4):787–798. doi: 10.1007/s13197-024-06068-z

Incorporating Ganoderma lucidum extract and powder with probiotic cultures (Lactobacillus acidophilus and Bifidobacterium animalis subsp. lactis) enhanced the functional, textural, and sensory qualities of yogurt

Azize Atik 1,✉, İlker Atik 1, Gökhan Akarca 2, Ayşe Janseli Denizkara 2
PMCID: PMC11914407  PMID: 40109686

Abstract

In this study, the extract and powder obtained from the Reishi mushroom (Ganoderma lucidum) were used in the production of yogurt, and also Lactobacillus acidophilus and Bifidobacterium animalis subsp. lactis bacteria were also inoculated. Furthermore, all values were also affected in parallel with the increase in the added ratio. Reishi mushroom powder and extract also increased the samples’ total antioxidant and phenolic values. Among the samples, the highest total phenolic content was found in the 2EA-coded sample with 2.415 mg GAE/g and the lowest in the control sample with 0.630 mg GAE/g. The highest antioxidant activity was determined in the 2PA-coded sample with a value of 0.198. The powder and extract showed a prebiotic effect by contributing positively to the development of probiotic bacteria added to yogurt. The count of probiotic bacteria in yogurts with Reishi mushroom powder and extract increased by approximately 1.4 log cfu/g. Using powder and extract of the Reishi mushroom in yogurt production gave yogurt significant functionality.

Keywords: Yogurt, Reishi mushroom, Powder, Lyophilized extract, Prebiotic

Introduction

Increasing nutritional awareness has changed consumer preferences toward natural and functional foods. In particular, the Covid-19 pandemic, which has affected the whole world, has increased the expectations for the food consumed to be environmentally sustainable and to support human health, significantly strengthening the immune system (Jaeger et al. 2023). For this reason, studies aimed at developing functional products or adding functional properties to traditional products have gained momentum. Functional foods are defined as foods that help the prevention or treatment of diseases that provide physiological benefits and meet the body’s need for essential nutrients (Dayısoylu et al. 2014). Especially milk and dairy products are the most studied product group in the production of commercial functional products.

One of the products considered the primary protein source among foods is milk and dairy products. At the same time, it is an indispensable element of daily nutrition with the vitamins and minerals it contains. In addition to the high nutritional value of milk proteins, various peptides released from these proteins during food processing and gastrointestinal digestion also have health-promoting and disease-preventing properties (Liu et al. 2022). Yogurt is the most popular dairy product. The fact that yogurt is so famous is due to its many health benefits and superior medicinal properties. Yogurt, a fermented product (Arab et al. 2023), contains vitamins such as thiamine and riboflavin and minerals such as magnesium, zinc, potassium, and calcium. The amount of these micronutrients in yogurt is higher than its raw material milk (Ahmad et al. 2022). The bioactive components, such as lactic acid formed during fermentation, effectively benefit the metabolism, especially the digestive system. It also has a unique taste thanks to lactic acid bacteria (Ahmad et al. 2023). The most common way to increase the functional qualities of yogurt is to add natural plant powders and extracts. Another method is to use probiotic strains in yogurt production. In this way, the physicochemical and sensory properties of yogurt can be improved (Abdullah et al. 2023).

Mushrooms, called “Food of the Gods” by the Romans, have become popular since ancient times. Because they contain essential nutrients such as proteins, polysaccharides, polyphenols, riboflavin, niacin, vitamin D, potassium and selenium (Leong et al. 2021). The fact that they contain ergothioneine, which humans cannot synthesize, makes mushrooms important in terms of nutrition (Lu et al. 2020). In addition, mushrooms are low-calorie products due to their low-fat content and rich in polyunsaturated fatty acids. In addition, they contain antioxidant, antibacterial, antiviral, anticancer, and anti-inflammatory properties, as well as secondary metabolites that improve the functioning of the cardiovascular system (Reis et al. 2017; Muszyńska et al. 2018). Therefore, mushrooms which are edible used in functional food formulations. Reishi mushroom (Ganoderma lucidum), called the “mushroom of immortality” due to its benefits in Chinese and Japanese literature, is widely used in traditional medicine (Turfan et al. 2016). G. lucidum is known to contain polysaccharides as well as various secondary metabolites such as triterpenoids, steroids, alkaloids, nucleotides, fatty acids and lactones. 90% of these mushrooms consist of water. The remaining dry matter consists of 10–40% macromolecules, 3–28% fats and other fibrous material, crude proteins, ash, vitamins, minerals, metallic components, inorganic substances, amino acids, and essential oils (Bhakshu et al. 2023). In addition, Reishi mushroom extract is frequently used in the treatment of cancer in Asian countries. 12 different bioactive components, mainly ethyl octadeca-9,12-dienoate, ethylhexadecanoate/ethyl palmitate, guaiacol, octadecanoic acid, ethylcyclohexane, have been identified in the extract of Reishi mushroom. Compounds such as triterpenes (ganoderic acids R and S, ganoderiol, ganodermanontriol, ganosporic acid A, ganoderol B),, meroterpenoids (lucidumin A, B, C, D), polysaccharides (heteropolysaccharide F31, ganoderan A and B, proteoglucan FYGL), oleic acid, sterols, etc., which have anti-inflammatory, antiallergic, neuroprotective, hypoglycemic, hypotensive, antibacterial, antifungal and antiviral effects, were detected in G lucidum extracts obtained in different solvents (Sułkowska-Ziaja et al. 2023). In addition, reishi mushroom contains polysaccharides (Garuba et al. 2020). It is known that aldo-hexose is a dominant compound in polysaccharides, and heteropolymers such as mannose, galactose, saccharides, fructose which is the substitution of β and α–d (or l) have 1-4, 1-3, 1-6 conformational structures. The polysaccharide framework is structurally heavy and may be responsible for the rigidity of G. lucidum (Bhakshu et al. 2023). Several factors influence the relationship between the structure and activity of G. lucidum polysaccharides; these include monosaccharide composition, glycoside linkages, side chain branching, and molecular weight. G. lucidum polysaccharides consist of homopolysaccharides and heteropolysaccharides. Homopolysaccharides can suppress tumor cell growth by inhibiting cyclin production and inducing cellular stress responses. In addition to this, heteropolysaccharides reported from G. lucidum also exhibit superior antitumor and immunomodulatory properties; these are attributed to a variety of different monosaccharides such as mannose, xylose, fucose, glucose, galactose, and arabinose as main components or in various combinations (Kou et al. 2023). These polysaccharides contribute significantly to the antibacterial, antioxidant, and antitumor properties of the mushroom Laboratory studies show that the extract kills tumor cells, and increases the activity of phagocytes (which engulf other cells), such as lymphocytes, natural killer cells (NK), such as T cells, and tumor necrosis factor cells (TNF), such as B cells (Santesso et al. 2016). G. lucidum, in addition to its nutritional elements, contains anti-nutrient components such as oxalate, phytate, tannin, etc. Studies show that the anti-nutrient factors found in G. lucidum are below permissible toxic levels (Essien et al. 2013). Additionally, proper food processing can reduce the negative effects of phytic acid, oxalates, and tannins. The fermentation process can significantly reduce phytic acid levels (Kumar et al. 2010). Heat treatments such as boiling, baking, and roasting can reduce the amount of oxalates and tannins (Akhtar et al. 2011).

There are many studies on the use of probiotic bacteria in yoghurt production. Research on the use of probiotic cultures and Reishi mushrooms in improving both the biofunctional and technofunctional qualities of yoghurt is quite limited. In this study, powder and extract obtained from Reishi mushroom were used separately in the production of yoğurt. In addition, probiotic Lactobacillus acidophilus and Bifidobacterium animalis subsp. lactis bacteria were also inoculated. The effect of reishi mushroom on both probiotic bacteria and the microbiological, physicochemical and sensory properties of yoghurt was examined. It was aimed to reveal the physical, chemical, microbiological, textural, and sensory differences between the yogurts obtained as a result of the study.

Materials and methods

Materials

Reishi mushroom (Ganoderma lucidum) was obtained from a local market operating in Afyonkarahisar, Turkey. The raw bovine milk used in yogurt production was obtained from a local farmer and brought to the laboratory immediately in the cold chain. Lactobacillus delbrueckii subsp. bulgaricus (Lyofast SP5, Italy) and Streptococcus thermophilus (Cryofast ST051, Italy) were used as starter cultures for the production of yogurts, and Bifidobacterium animalis spp. lactis (Pro Lafti B-94) and Lactobacillus acidophilus (Pro Lafti L10) were used as probiotic cultures.

Methods

Preparation of Reishi mushroom (Ganoderma lucidum) powder and extract

Reishi mushroom powder was produced according to the method with minor modifications described by Kilinc et al. (2022). The raw mushrooms were freeze-dried using a laboratory-scale lyophilizer (Telstar, Lyquest). Sliced mushrooms were pre-frozen at − 24 °C for 48 h. It was then lyophilized in a lyophilizer at − 45 °C for 48 h.

The extract was prepared using the Akarca & Başpınar (2019) method with minor modifications. The distilled water with a volume of 400 mL was added to 250 g of chopped mushroom sample. The samples were mixed in a dark room at 65 °C for 24 h at 120 rpm with the help of a shaker. The resulting mixture was transferred to a rotary evaporator after filtering through a sterilized 22 mm filter paper (Heidolph Hei-VAP value). Then, the obtained liquid extract was dried in a lyophilizer and turned into powder.

Preparation of yogurt

The method of Sahingil and Hayaloglu (2022) was revised and used to produce yogurt. Raw bovine milk which was pasteurized at 85 °C for 5 min quickly cooled to 45 °C before incubation. Pasteurized milk was divided into three equal volumes, and starter cultures Lactobacillus delbrueckii subsp. bulgaricus (Lyofast SP5, Italy), and Streptococcus thermophilus (Cryofast ST051, Italy), and probiotic cultures Bifidobacterium animalis subsp. lactis (Pro Lafti B-94), and Lactobacillus acidophilus (Pro Lafti L10), and the mixtures of two probiotic cultures were inoculated into each milk and mixed for 5 min. Inoculated milk was divided into sterile jars of 200 ml. Before fermentation, Reishi mushroom powder and Reishi mushroom extract were added to the samples at a rate of 0.1% and 0.2% (w/v, %), respectively, and allowed to incubation. Within the scope of the research, samples and their codes are given in Table 1.

Table 1.

Samples and their codes

Codes Sample
C Control
AC Control with L. acidophilus
1EA 1% Reishi mushroom extract with L. acidophilus
2EA 2% Reishi mushroom extract with L. acidophilus
1PA 1% Reishi mushroom powder with L. acidophilus
2PA 2% Reishi mushroom powder with L. acidophilus
BC Control with B. animalis subsp. lactis
1EB 1% Reishi mushroom extract with B. animalis subsp. lactis
2EB 2% Reishi mushroom extract with B. animalis subsp. lactis
1PB 1% Reishi mushroom powder with B. animalis subsp. lactis
2PB 2% Reishi mushroom powder with B. animalis subsp. lactis
ABC Control with both B. animalis subsp. lactis, and L. acidophilus
1EAB 1% Reishi mushroom extract with both B. animalis subsp. lactis, and L. acidophilus
2EAB 2% Reishi mushroom extract with both B. animalis subsp. lactis, and L. acidophilus
1PAB 1% Reishi mushroom powder with both B. animalis subsp. lactis, and L. acidophilus
2PAB 2% Reishi mushroom powder with both B. animalis subsp. lactis, and L. acidophilus
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Mineral content

Mineral analysis was conducted for reishi mushroom powder and extract. First of all, 0.5 g of dried mushroom was burned using 10 mL of HNO3 + H2SO4 in a microwave combustion system (Mars 5, CEM Corporation, USA). For this purpose wet combustion method was used. Mineral contents of the obtained filtrates were determined by using the ICP-AES (inductively-coupled plasma spectrosmeter) device (Vista Series, Varian International, AG, Switzerland) (Skujins 1998).

Organic acid

Organic acid analysis was performed only for reishi mushroom powder and extract. For the determination of the organic acid amounts of the samples an HPLC (Shimadzu Prominence) was used. Firstly, 4 g of samples were taken, and 20 mL of 0.01 N H2SO4 was added. Subsequently, it was then vortexed, filtered using a 0.45-micron filter paper, and injected into the system (Guzel Seydim et al. 2000). System features for the HPLC used were as follows: CBM: 20ACBM; Detector: DAD (SPD-M20A); Column Furnace: CTO-10ASVp; Pump: LC20 AT; Autosampler: SIL 20ACHT; Computer Program: LC Solution; Column: ODS 4 (250 mm*4.6 mm, 5 µm) (GP Sciences, Inertsil ODS-4, Japan); and Mobile phase: ultrapure water pH adjusted to 3 with orthophosphoric acid (Aktas et al. 2005).

pH value

For the measurement of the pH values of the samples a calibrated pH meter was used (HANNA, HI 2215 pH/ORP meter) (Sözeri et al. 2023).

Dry matter (%)

Total dry matter was determined according to AOAC (2005).

Syneresis value % (w/w)

The % syneresis values of the yogurt samples were determined using the centrifugation method. For this purpose, on the 1st day of storage, yogurt samples (m0 = 25 g) were weighed and transferred to centrifuge tubes. It was then centrifuged for 25 min at 25 °C. The supernatant (separated yogurt juice) was separated and weighed (m). The syneresis value was calculated according to the following equation (Bhullar et al. 2002).

Syneresis value = (m0/m) × 100.

Total phenolic content

Two grams of yogurt sample, acidified with 0.1% HCl and added 60 mL of 60% (v/v) ethanol, was ultrasonically extracted at 43 °C 200 W for 16 min. After that, the mixture was vacuum filtered. This procedure was performed twice. The two filtrates were combined and concentrated using a rotary evaporator at 42 °C to remove the ethanol contained therein. It was diluted to 25 mL for measurement. The total phenolic contents of the samples were measured using the Folin-Ciocalteu reagent, and the results are given as milligram Gallic acid equivalents (GAE)/100 g (Khalil et al. 2022).

Antioxidant activity

The DPPH radical (2,2-diphenyl-1-picrylhydrazyl radical) was used for the determination of the antioxidant activity of yogurt samples (Amadarshanie et al. 2022). A concentration series of yogurt samples were prepared in methanol, and absorbance was taken at 517 nm. After that, DPPH solution was added into the samples and kept in the dark environment at 25 °C for 15 min. Then absorbance values were taken at 517 nm. The standard used in the assay was gallic acid (GA). The DPPH radical scavenging activity was expressed as mg GA equivalent per 1 g. Samples were analyzed in triplicate.

Color

The color analysis of the yogurt samples was conducted in terms of L*, a*, and b* values using a colorimeter (Minolta Co., Osaka, Japan). All samples were measured at least three times (Wang et al. 2023).

Texture analysis

A TA.XT Plus Texture Analyzer was used to determine the consistency, firmness, and viscosity index values of yogurt samples (Stable Micro Systems) (Kilinc et al. 2022).

Apparent viscosity

A viscometer (Brookfield DV-I+) was used to measure the viscosity values of the samples (Gomes et al. 2023).

Microbiological analysis

Serial dilutions were prepared from the yogurt samples before the analyses, and the analyses were carried out using the spread plate technique from these dilutions. Streptococcus agar (11,007, Merck Millipore, Germany) was used for the counts of S. thermophilus species of the samples, while Lactobacillus bulgaricus agar (17,154, Merck Millipore, Germany) was used for the counts of L. delbrueckii subsp. bulgaricus. Then, the counts were determined after incubating for 48–72 h at 45 °C under anaerobic conditions (Bracquart 1981).

100 µL of the dilution prepared for this purpose was taken and spread on the MRS-Salicin Agar and RCA—Aniline blue-Dicloxacillin agar surfaces. It was then incubated under anaerobic conditions at 45 °C for 48–72 h.

Sensory analysis

The sensory analysis of the samples was carried out using the scoring test technique, as stated in Altuğ and Elmacı (2005). The samples were scored by 20 trained panelists from Afyon Kocatepe University, Department of Food Engineering. Samples were served to the panelists randomly at room temperature in daylight. The hedonic scale was used to evaluate the samples. Samples were scored on seven parameters: consistency, grittiness, sourness, flavour, colour, odour, and general preference.

Statistical analysis

The results obtained in the study were made in two parallels using a SPSS software program V 23.0.0. The variation analysis was performed on the data obtained from the study. Significant differences were determined by Duncan’s multiple-range tests (*P < 0.05).

Results and discussion

Physicochemical changes

Mineral substance, organic acid and antioxidant activity values of Reishi mushroom powder and extract were given in Table 2. Mineral substance, organic acid content and antioxidant activity of Reishi mushroom powder were found to be higher than the extract. Although Reishi mushroom contains many essential mineral substances, it was determined that it is especially rich in potassium (powder: 75.88; extract: 28.85). Reishi mushroom powder and extract were found to contain high amounts of lactic acid and acetic acid. These organic acids are effective in the aroma occurence of Reishi mushroom. Antioxidant activity was determined as 7.07 in reishi mushroom powder and 0.843 in the mushroom extract. The pH, dry matter, % syneresis, antioxidant activity and total phenolic content values of yogurts produced by adding two different probiotic bacteria and Reishi mushroom powder and extract at two different rates are given in Table 3. Sample diversity (Reishi mushroom powder/extract addition, probiotic bacteria addition) affected pH value highly significant (P < 0.01), while % dry matter, % syneresis, antioxidant activity and total phenolic content very highly significant (P < 0.0001). In addition, sample diversity showed a positive correlative effect at the level of 0.01 on dry matter and antioxidant activity, and a negative correlative effect at the level of 0.01 on % syneresis.

Table 2.

Mineral content (mg/L), organic acid (ng/mL) and antioxidant activity values of Reishi mushroom powder and extract

Mineral content (mg/L)
Ca K Mg Na P Se Fe Zn
Powder 2.68 ± 0.08 75.88 ± 1.91 2.55 ± 0.31 0.48 ± 0.08 35.53 ± 2.39 0.112 ± 0.03 1.016 ± 1.013 0.797 ± 0.081
Extract 0.99 ± 0.02 28.85 ± 5.10 0.76 ± 0.17 0.111 ± 0.04 9.84 ± 2.12 0.07 ± 0.01 0.547 ± 0.13 0.278 ± 0.06
Organic acids
Acetic acid Citric acid Lactic acid Succinic acid Fumaric acid
Powder 125.57 ± 5.87 0.010 ± 0.004 224.42 ± 13.88 14.28 ± 1.46 3.27 ± 0.67
Extract 52.38 ± 5.87 nd 90.50 ± 9.38 2.28 ± 0.91 0.90 ± 0.04
Antioxidant activity
Powder 7.07 ± 0.57
Extract 0.843 ± 0.12
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nd not detected

Table 3.

Change in pH, dry matter (%), syneresis (%), total phenolic content (TPC), and antioxidant activity on yogurt samplesa

Samples pH Dry matter (%) Syneresis (%) Total phenolic content (mg GAE/g) Antioxidant activity
C 4.26 ± 0.03ab 13.87 ± 0.10jk 78.06 ± 0.56b 0.630 ± 0.007n 0.069 ± 0.004h
AC 4.19 ± 0.01bcd 13.97 ± 0.11j 79.74 ± 0.44a 1.170 ± 0.007j 0.071 ± 0.004g
BC 4.23 ± 0.03abc 13.72 ± 0.16k 78.16 ± 0.09b 0.670 ± 0.014m 0.074 ± 0.003fg
ABC 4.21 ± 0.02bcd 13.85 ± 0.09jk 77.85 ± 0.25bc 0.755 ± 0.011l 0.072 ± 0.005fg
1EA 4.29 ± 0.01a 14.74 ± 0.06h 76.68 ± 0.28cde 1.365 ± 0.019i 0.085 ± 0.004efg
2EA 4.17 ± 0.01cde 15.75 ± 0.13f 75.93 ± 0.23efg 2.415 ± 0.013a 0.094 ± 0.003def
1EB 4.26 ± 0.01ab 14.38 ± 0.08i 74.74 ± 0.53g 1.548 ± 0.014g 0.086 ± 0.004efg
2EB 4.25 ± 0.06ab 15.03 ± 0.11g 70.84 ± 0.54i 1.511 ± 0.002h 0.113 ± 0.24cd
1EAB 4.17 ± 0.01cde 17.66 ± 0.14b 74.97 ± 0.12fg 2.050 ± 0.015b 0.091 ± 0.005efg
2EAB 4.14 ± 0.01de 18.13 ± 0.08a 72.54 ± 0.47h 1.994 ± 0.005c 0.174 ± 0.011b
1PA 4.25 ± 0.01ab 16.28 ± 0.06e 77.29 ± 0.26bcd 1.915 ± 0.008e 0.079 ± 0.006efg
2PA 4.21 ± 0.08bcd 18.12 ± 0.04a 76.86 ± 0.09bcde 2.056 ± 0.001b 0.198 ± 0.004a
1PB 4.20 ± 0.03bcd 16.56 ± 0.13d 76.09 ± 0.45def 0.767 ± 0.005l 0.088 ± 0.006efg
2PB 4.10 ± 0.01e 17.18 ± 0.05c 73.27 ± 1.77h 0.909 ± 0.004k 0.128 ± 0.010c
1PAB 4.24 ± 0.01ab 17.66 ± 0.14b 75.21 ± 0.10fg 1.665 ± 0.007f 0.100 ± 0.004de
2PAB 4.17 ± 0.01cde 18.13 ± 0.08a 72.79 ± 0.32h 1.957 ± 0.018d 0.178 ± 0.004b
P value 0.001 < 0.0001 < 0.0001 < 0.0001 < 0.0001
r − 0.361 0.833** − 0.578** 0.158 0.552**
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aC, Control; AC, L. acidophilus control; BC, B. animalis subsp. lactis control; ABC, L. acidophilus + B. animalis subsp. lactis control; 1EA, 1% extract and L. acidophilus; 2EA, 2% extract and L. acidophilus; 1EB, 1% extract and B. animalis subsp. lactis; 2EB, 2% extract and B. animalis subsp. lactis; 1EAB, 1% extract and L. acidophilus + B. animalis subsp. lactis; 2EAB, 2% extract and L. acidophilus + B. animalis subsp. lactis; 1PA, 1% powder and L. acidophilus; 2PA, 2% powder and L. acidophilus; 1PB, 1% powder and B. animalis subsp. lactis; 2PB, 2% powder and B. animalis subsp. lactis 1PAB, 1% powder and L. acidophilus + B. animalis subsp. lactis; 2PAB, 2% powder and L. acidophilus + B. animalis subsp. lactis

a–n (↓):Values with the different letters in the same column for each analysis differ significantly (P < 0.05)

P < 0.0001: Very highly significant, P < 0.01: Highly significant

Correlation significance is indicated by asterisks: **significant at the 0.01 level (2-tailed)

Among the yogurt samples, the highest pH value was detected at 4.29 in 1EA-coded sample and the lowest at 4.10 in 2PB-coded sample (Table 3). The addition of Reishi mushroom powder was more effective than the addition of extract, while the addition of L. acidophilus was more effective than the addition of B. animalis subsp. lactis on the decrease in the pH values (P < 0.05). In addition, using the two bacteria together and increasing the amount of added powder/extract caused a further decrease in the pH value. Our research findings were consistent with the results of Hamed et al. (2021). They determined a similar change in pH values by adding peanut skin extract powder to the yogurt formulation.

The % dry matter content of the samples increased in parallel with the added amount of Reishi mushroom powder/extract (P < 0.05). The effect of the addition of powder or extract on the increase in the % dry matter content was similar (P < 0.05). Furthermore, the addition of B. animalis subsp. lactis, and L. acidophilus, and these two bacteria together did not affect the dry matter change (P > 0.05).

The % syneresis values of yogurt samples decreased in parallel with the addition and amount of powder/extract (P < 0.05). It was determined that the reducing effect of adding mushroom extract on % syneresis was higher than adding powder (Table 3). Besides, the addition of L. acidophilus increased the syneresis value in yogurt. The addition of mushroom extract/powder had a lowering effect on syneresis by binding the water in yogurt. Furthermore, since the addition of L. acidophilus bacteria in yogurt increased the current acidity level, the water-holding capacity of yogurt decreased, and accordingly, the rate of syneresis increased. In a study in which retrograde corn starch was added to yogurt as dietary fiber, it was similarly stated that starch addition reduced syneresis (Dircio‑Morales et al. 2023).

The samples’ total phenolic content (TPC) increased in direct proportion to the added Reishi powder and extract (P < 0.05). In particular, the mushroom powder caused a more significant increase in TPC than its extract (P < 0.05).

Among the yogurt samples, the highest TPC was found in the 2EA-coded sample with 2.415 mg GAE/g, and the lowest TPC was found in the control sample with 0.630 mg GAE/g (Table 3). TPC was higher in the yoğurt samples produced with the addition of L. acidophilus compared to the samples produced with the addition of B. animalis subsp. lactis. This may be related to the metabolites released by the culture used during the fermentation process. As it is known, phenolic compounds may be found in milk depending on the animal’s nutritional status, the milk’s chemical composition, and the phenolic compounds’ metabolism (Vázquez et al. 2015). The presence of TPC in control samples could be attributed to several reasons. First, the transfer of polyphenolic compounds from animal feed to milk and interactions between a specific non-reactive Folin-Ciocalteu reagent and some food ingredients may be effective. Various nutrients such as aromatic amino acids, sugars, some inorganic and non-phenolic organic substances may interact with this reagent, resulting in higher false results (Tami et al. 2022). Second, fermentation may have an effect on the phenolic content. This situation is closely related to the phenolic acid metabolism of the strain used (He et al. 2022).

Mushrooms are known to be the source of many antioxidant compounds (Reis et al. 2017). For this reason, it is expected that adding the Reishi mushroom increases the antioxidant activity in yogurt. The highest antioxidant activity among the samples was determined in the 2PA-coded sample with a value of 0.198, and the 2PAB-coded sample with a value of 0.178 followed this sample (Table 4). The addition of Reishi mushroom extract during production showed a more pronounced effect on antioxidant activity than its powder (P < 0.05). In addition, antioxidant activity increased in direct proportion to the added amount. On the other hand, the addition of two different probiotic bacteria had effects on antioxidant activity. (P < 0.05). The study results are similar to the studies on yogurt functionally developed with phenolic-rich products (Baria et al. 2021).

Table 4.

Change in color values of yogurt samplesa

Samples L* a* b*
C 90.24 ± 0.09a − 0.11 ± 0.01g 5.31 ± 0.06j
AC 90.26 ± 0.11a − 0.51 ± 0.01j 9.19 ± 0.08a
BC 90.22 ± 0.08a − 0.23 ± 0.06h 6.64 ± 0.13g
ABC 90.18 ± 0.05a − 0.41 ± 0.04i 9.01 ± 0.06ab
1EA 89.67 ± 0.31b − 0.09 ± 0.06f 8.00 ± 0.13d
2EA 89.47 ± 0.18bc 0.03 ± 0.02e 6.57 ± 0.08gh
1EB 89.30 ± 0.06ef − 0.49 ± 0.04h 8.95 ± 0.08b
2EB 89.33 ± 0.17bcd 0.07 ± 0.02e 7.73 ± 0.06e
1EAB 88.32 ± 0.25ef − 0.40 ± 0.06h 8.59 ± 0.09c
2EAB 88.11 ± 0.38fg 0.10 ± 0.03e 7.43 ± 0.10f
1PA 89.17 ± 0.03bcd 0.42 ± 0.06d 8.10 ± 0.11d
2PA 89.05 ± 0.04cd 0.70 ± 0.08c 5.56 ± 0.04i
1PB 88.83 ± 0.10de 0.52 ± 0.07d 6.63 ± 0.04g
2PB 88.32 ± 0.04bcd 1.15 ± 0.06a 6.39 ± 0.09h
1PAB 87.72 ± 0.49gh 0.69 ± 0.04c 7.56 ± 0.13ef
2PAB 87.52 ± 0.35h 0.93 ± 0.04b 5.58 ± 0.05i
P value < 0.0001 < 0.0001 < 0.0001
r − 0.861** 0.872** − 0.462*
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aC, Control; AC, L. acidophilus control; BC, B. animalis subsp. lactis control; ABC, L. acidophilus + B. animalis subsp. lactis control; 1EA, 1% extract and L. acidophilus; 2EA, 2% extract and L. acidophilus; 1EB, 1% extract and B. animalis subsp. lactis; 2EB, 2% extract and B. animalis subsp. lactis; 1EAB, 1% extract and L. acidophilus + B. animalis subsp. lactis; 2EAB, 2% extract and L. acidophilus + B. animalis subsp. lactis; 1PA, 1% powder and L. acidophilus; 2PA, 2% powder and L. acidophilus; 1PB, 1% powder and B. animalis subsp. lactis; 2PB, 2% powder and B. animalis subsp. lactis 1PAB, 1% powder and L. acidophilus + B. animalis subsp. lactis; 2PAB, 2% powder and L. acidophilus + B. animalis subsp. lactis

a–j (↓):Values with the different letters in the same column for each analysis differ significantly (P < 0.05)

P < 0.0001: Very highly significant

Correlation significance is indicated by asterisks: **significant at the 0.01 level (2-tailed); *significant at the 0.05 level (2-tailed)

The effect of sample diversity on all color values (L*, a*, b*) was very highly significant (P < 0.0001). In addition, sample diversity showed a positive correlative effect at the level of 0.01 on the L* value and at the level of 0.05 on the b* value, while it had a negative correlative effect at the level of 0.01 on the a* value (Table 4).

L* value, which is an indicator of brightness in foods, decreased with the addition of extract and powder in yogurt samples (P < 0.05). The effect of the addition of Reishi mushroom powder on the decrease of L* value was more significant compared to the addition of extract. Then again, the addition of probiotic bacteria in yogurt production did not show any significant effect on the change of the L* value (P > 0.05).

The highest L* value was found in the AC-coded sample (90.26) among the samples, whereas the lowest L* value was in the 2PAB-coded sample (87.52) (Table 4).

G. lucidum has an irregular, bright yellow–brown surface, darkens, and turns reddish brown as it matures (Sułkowska-Ziaja et al. 2023). Therefore, a decrease in L* in samples with added extract and powder is an expected situation. Also the decrease in L* value is related to the increase in phenolic components depending on the added powder and extract concentration. The results align with a similar study on yogurt with added black carrot concentrate (Baria et al. 2021).

The addition of Reishi mushroom powder/extract to the yogurt samples caused the a* value to go from green to red, and the a* value increased in parallel with the increase in the amount added (P < 0.05). The mushroom powder showed a more increasing effect on the a* value than the extract. Also, the addition of B. animalis subsp. lactis similarly increased the a* value compared to the addition of L. acidophilus. However, the addition of two bacteria together decreased the a* value compared to the control sample (P < 0.05). Among the samples, the highest a* value was determined in 2PB-coded sample (1.15), followed by 2PAB (0.93) and 2PA-coded (0.70) samples, respectively (Table 4).

The b* value of the samples decreased due to the addition of powder/extract (P < 0.05). The use of Reishi powder in production of yogurt was more effective in the decrease of b* value compared to the use of the extract, and this effect increased depending on the amount used. Furthermore, the probiotic bacteria addition in yogurt production also increased the b* value. The addition of L. acidophilus caused a more significant increase in b* value compared to the addition of B. animalis subsp. lactis (P < 0.05). Among the fifteen different yogurt samples, the lowest b* value was found in the C-coded sample (5.31), while the highest b* value was found in the AC-coded sample (9.19) (Table 4). The results are in line with the study of Baria et al. (2021) on yogurt supplemented with black carrot concentrate. The surface of G. lucidum is irregular, lumpy and reddish brown. The color of the corky context can vary from whitish to cream to brown to purple-brown (Sułkowska-Ziaja et al. 2023). The reason for the increase in a* value and decrease in b* value in samples with extract and powder added may also be related to the natural color of the mushroom.

The effect of sample diversity on all textural properties (firmness, consistency, index of viscosity, and viscosity) was very highly significant (P < 0.0001). Furthermore, sample diversity showed a positive correlative effect at the level of 0.01 on the firmness value, while it had a negative correlative effect at the level of 0.01 on the viscosity value, and at the level of 0.05 on the index of viscosity value (Table 5).

Table 5.

Change in textural properties of yoghurt samplesa

Samples Firmness Consistency Index of viscosity Viscosity (cP)
C 140.13 ± 4.88j 1867.42 ± 22.41l − 167.45 ± 3.53a 568.00 ± 10.32i
AC 159.205 ± 3.30i 2755.32 ± 16.26k − 277.54 ± 4.52b 660.00 ± 14.12h
BC 174.425 ± 1.56i 2802.24 ± 8.48jk − 289.61 ± 2.87c 700.00 ± 28.28g
ABC 170.875 ± 1.77i 2765.52 ± 11.32k − 281.84 ± 1.47bc 685.00 ± 12.23gh
1EA 231.695 ± 4.31h 3107.81 ± 27.58g − 308.18 ± 4.86d 710.00 ± 14.14g
2EA 290.655 ± 4.38g 3542.15 ± 77.40d − 353.43 ± 7.21ef 790.00 ± 14.14ef
1EB 363.940 ± 7.95f 3460.03 ± 74.25e − 339.99 ± 2.02d 790.00 ± 14.14ef
2EB 446.425 ± 10.90d 3757.52 ± 34.22c − 372.87 ± 3.80g 990.00 ± 14.14c
1EAB 300.325 ± 5.68g 3302.48 ± 21.41f − 334.52 ± 5.78d 780.00 ± 14.14ef
2EAB 383.415 ± 8.78e 3401.99 ± 43.38e − 341.77 ± 4.00de 815.00 ± 21.21e
1PA 495.320 ± 11.30c 3863.08 ± 26.11b − 417.03 ± 9.16h 885.00 ± 7.07d
2PA 555.750 ± 16.25a 3947.73 ± 41.72a − 470.32 ± 2.27i 1335.00 ± 21.21a
1PB 502.331 ± 3.95ab 2899.13 ± 7.92ik − 317.72 ± 3.39d 770.00 ± 14.14f
2PB 522.944 ± 15.98b 2991.43 ± 13.87g − 338.52 ± 3.38d 855.00 ± 21.21d
1PAB 481.925 ± 4.67c 2790.01 ± 14.77jk − 316.60 ± 5.44d 800.00 ± 7.07ef
2PAB 494.330 ± 8.20c 2853.68 ± 12.69ij − 358.65 ± 10.56f 1095.00 ± 7.07b
P value < 0.0001 < 0.0001 < 0.0001 < 0.0001
R 0.891** − 0.034 − 0.396* − 0.802**
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aC, Control; AC, L. acidophilus control; BC, B. animalis subsp. lactis control; ABC, L. acidophilus + B. animalis subsp. lactis control; 1EA, 1% extract and L. acidophilus; 2EA, 2% extract and L. acidophilus; 1EB, 1% extract and B. animalis subsp. lactis; 2EB, 2% extract and B. animalis subsp. lactis; 1EAB, 1% extract and L. acidophilus + B. animalis subsp. lactis; 2EAB, 2% extract and L. acidophilus + B. animalis subsp. lactis; 1PA, 1% powder and L. acidophilus; 2PA, 2% powder and L. acidophilus; 1PB, 1% powder and B. animalis subsp. lactis; 2PB, 2% powder and B. animalis subsp. lactis 1PAB, 1% powder and L. acidophilus + B. animalis subsp. lactis; 2PAB, 2% powder and L. acidophilus + B. animalis subsp. lactis

a–l (↓):Values with the different letters in the same column for each analysis differ significantly (P < 0.05)

P < 0.0001: Very highly significant

Correlation significance is indicated by asterisks: **significant at the 0.01 level (2-tailed); *significant at the 0.05 level (2-tailed)

Reishi mushroom powder/extract addition provided improvement in textural proporties of yogurt samples (P < 0.05). The increase in the values by adding mushroom powder was more than adding the extract, and the values increased in parallel with the added amount. Adding probiotic bacteria in yogurt production caused an increase in textural values, and B. animalis subsp. lactis, one of the two added probiotic bacteria, showed a more significant effect on the increase in texture values compared to L. acidophilus (P < 0.05).

The firmness value was determined as the highest in the 2PA-coded sample (555.750) among the samples, while the lowest was detected in the C-coded sample (140.13). It is thought that the polysaccharides found in Reishi mushrooms are effective in the increase in the firmness value. Reishi mushroom (G. lucidum) is known to contain abundant polysaccharides (Bhakshu et al. 2023). These polysaccharides increased the water-holding capacity of yogurt and caused an increase in firmness value.

Similarly, the highest value in consistency values was determined in the 2PA-coded sample (Table 5). Mushrooms are rich in dietary fiber, also known as polysaccharides other than starch (Wang et al. 2021). These polysaccharides from the mushroom kept the free water and increased the serum concentration, resulting in an increase in the consistency values. The values we obtained in our research are similar to the results of Kilinc et al. (2022).

Parallel to the results obtained in the other two textural properties, the highest values in the index of viscosity and viscosity values were determined in the 2PA-coded sample, whereas the C-coded samples gave the lowest values again (Table 5).

Protein and fiber compounds increase the water-holding capacity, leading to viscous gels forming (Marand et al. 2020). For this reason, the fiber and protein from the added Reishi mushroom increased the apparent viscosity by forming a more robust three-dimensional network structure with the water in yogurt. On the other hand, protein–phenolic compound interactions can modify the functional properties of food proteins. This interaction can affect protein derivatives’ solubility by inducing protein crosslinking and changing the net charge on protein molecules. As a result of this interaction, the secondary and tertiary structures of the proteins change and acquire a hydrophilic structure. This change in hydrophilic/hydrophobic properties can effect not only solubility behavior but also other functional properties such as emulsification, foaming properties, and gelation (Hamed et al. 2021). This mechanism can explain the apparent viscosity-increasing effect of the addition of the Reishi mushroom extract.

Microbiological changes

The effect of sample diversity on all the counts obtained as a result of the microbiological analysis was very highly significant (P < 0.0001; Table 6). Reishi mushroom powder/extract addition caused a decrease in the counts of L. delbrueckii subsp. bulgaricus and S. thermophilus. Similarly, the addition of probiotic bacteria in yogurt production caused a decrease in the counts of L. delbrueckii subsp. bulgaricus and S. thermophilus (P < 0.05; Table 6). Among the samples, the counts of L. delbrueckii subsp. bulgaricus and S. thermophilus was determined as the highest in the C-coded sample and the lowest in the 1EB-coded sample.

Table 6.

Microbial count of yoghurt samples (log cfu/g)a

Samples S. thermophilus L.delbrueckii subsp. bulgaricus L. acidophilus B. animalis subsp. lactis
C 7.11 ± 0.01a 6.99 ± 0.08a 0.94 ± 0.04f 0.83 ± 0.02h
AC 6.95 ± 0.01b 5.93 ± 0.12gh 6.14 ± 0.11c 1.92 ± 0.11g
BC 6.72 ± 0.05c 5.77 ± 0.09hi 1.53 ± 0.09d 6.14 ± 0.07d
ABC 6.80 ± 0.03bc 5.90 ± 0.15gh 6.10 ± 0.1 7c 6.25 ± 0.05cd
1EA 6.60 ± 0.04de 5.56 ± 0.27i 6.76 ± 0.07b 4.57 ± 0.38f
2EA 6.77 ± 0.02c 6.66 ± 0.05bc 7.03 ± 0.13b 1.91 ± 0.19g
1 EB 6.19 ± 0.08g 5.72 ± 0.25hi 1.50 ± 0.28d 7.27 ± 0.06ab
2 EB 6.79 ± 0.03c 6.97 ± 0.04a 1.39 ± 0.13de 7.56 ± 0.04a
1EAB 6.54 ± 0.03def 6.35 ± 0.04def 6.26 ± 0.02c 6.65 ± 0.14c
2EAB 7.03 ± 0.01ab 6.40 ± 0.09cde 6.42 ± 0.02c 6.95 ± 0.08bc
1PA 6.20 ± 0.06g 5.68 ± 0.21hi 7.41 ± 0.03a 2.01 ± 0.15g
2PA 6.60 ± 0.04de 6.08 ± 0.07fg 7.52 ± 0.02a 2.14 ± 0.26g
1 PB 6.48 ± 0.03f 6.16 ± 0.04efg 1.50 ± 0.28d 7.39 ± 0.04a
2 PB 6.52 ± 0.05ef 6.89 ± 0.13ab 1.15 ± 0.21e 7.58 ± 0.03a
1PAB 6.62 ± 0.01d 5.98 ± 0.06gh 6.20 ± 0.05c 5.78 ± 0.16e
2PAB 7.02 ± 0.04ab 6.58 ± 0.10cd 6.42 ± 0.09c 6.10 ± 0.09de
P value < 0.0001  < 0.0001  < 0.0001  < 0.0001
R − 0.031 0.0348 0.049 0.294
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aC, Control; AC, L. acidophilus control; BC, B. animalis subsp. lactis control; ABC, L. acidophilus + B. animalis subsp. lactis control; 1EA, 1% extract and L. acidophilus; 2EA, 2% extract and L. acidophilus; 1EB, 1% extract and B. animalis subsp. lactis; 2EB, 2% extract and B. animalis subsp. lactis; 1EAB, 1% extract and L. acidophilus + B. animalis subsp. lactis; 2EAB, 2% extract and L. acidophilus + B. animalis subsp. lactis; 1PA, 1% powder and L. acidophilus; 2PA, 2% powder and L. acidophilus; 1PB, 1% powder and B. animalis subsp. lactis; 2PB, 2% powder and B. animalis subsp. lactis 1PAB, 1% powder and L. acidophilus + B. animalis subsp. lactis; 2PAB, 2% powder and L. acidophilus + B. animalis subsp. lactis

a–i (↓):Values with the different letters in the same column for each analysis differ significantly (P < 0.05)

P < 0.0001: Very highly significant

The use of Reishi mushroom powder/extract had a positive effect on the counts of B. animalis subsp. lactis and L. acidophilus (P < 0.05). Using the powder form of Reishi mushroom was more significant in the increase of B. animalis subsp. lactis and L. acidophilus counts. In addition, the increase in the amount used positively affected the increase in the counts of probiotic bacteria. Among the samples, the highest B. animalis subsp. lactis and L. acidophilus counts were detected in 2PB-coded (7.58 log cfu/g) and 2PA-coded (7.52 log cfu/g) samples (Table 6).

It is thought that the prebiotic effect of the polysaccharides in the added powder and their use as nutrients for bacteria may cause this situation. Previous studies have shown that mushroom extracts help probiotic bacteria growth rates, and the symbiotic effect of the extract could be successful with some Lactobacillus strains (Pelaes Vital et al. 2015). This symbiotic effect caused an increase in the count of bacteria with the addition of the extract.

The sensory evaluation of yogurts was based on consistency, grittiness, sourness, taste/flavour, colour, odour, and general preference.

The starter culture used in yoghurt production affects acidity, textural, and sensory properties. The probiotic cultures used in the study and the added Reishi mushroom powder and extract changed textural and sensory properties of yogurts (P < 0.05). Sensory evaluation of yoghurts was made based on consistency, grittiness, sourness, taste, color, smell, and general preference. The sensory results of the samples are given in Fig. 1. As seen in the radar chart, an increase is observed in the consistency and sourness values depending on the addition of powder and extract. The reason for the increase in consistency is that the polysaccharides from the mushrooms increase the water-holding capacity. This is related to sourness and acidity that develops due to microorganism activity. In addition, it is thought that the umami taste produced by free amino acids, 5’-nucleotides, volatile compounds, and other components which are responsible for the unique aroma of mushrooms may have an effect on the sour taste (Sun et al. 2020). It was also determined that volatile compounds coming from the mushrooms were effective on the odor of the samples. It was determined that there was a decrease in color values, especially in powder-added samples. Although the change in color and grittiness are factors that reduce the general preference it is thought that especially the improvement of consistency causes a positive effect on general preference. General preference scores were similar to control samples.

Fig. 1.

Fig. 1

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Sensory analysis results of yogurt samples

Conclusion

In this study, extract and powder obtained from Reishi mushroom (Ganoderma lucidum) were used separately in the production of yogurt, and probiotic Bifidobacterium animalis subsp. lactis and Lactobacillus acidophilus bacteria were added to increase the functional quality of yogurt. In this way, a functionally enriched fermented milk product was obtained.

The added Reishi mushroom powder has been revealed to affect the physicochemical, microbiological, textural, and sensory properties more than the extract. In addition, it has been determined that the addition of probiotic bacteria (especially L. acidophilus) improves the physicochemical properties of yoğurt and gives it sensory appreciation.

Interest in functional foods is ever-increasing. Milk and dairy products are the most studied products in functional food production. Generally, studies on the use of probiotic cultures are common. This study aimed to improve the physicochemical and textural properties of yogurt by adding Reishi mushroom powder and extract at different rates to probiotic yogurts produced using L. acidophilus and B. animalis subsp. lactis probiotic cultures. At the end of the study, the total phenolic content (TPC) and antioxidant activity increased in the yogurts obtained. Reishi mushroom-originated polysaccharides improved the textural and rheological properties by increasing the water-holding capacity of yogurt. Furthermore, these polysaccharides, which are dietary fibers, acted as prebiotics and encouraged the development of probiotic cultures. Since the number of living cultures is an important factor in probiotic yogurts, it is an important finding that the addition of mushroom powder and extract increases the number of living organisms. For this reason, it is thought that the results of the research will be helpful for further studies in improving the functional, rheological, and sensory properties of probiotic yogurts.

Authors’ contribution

Azize Atik: Conceptualization, Investigation, Writing—Original Draft Preparation. İlker Atik: Conceptualization, Investigation, Writing—Reviewing and Editing Gökhan Akarca: Methodology, Supervision, Validation. Ayşe Janseli Denizkara: Data Curation, Formal analysis.

Funding

No financial support was received for this research.

Data and materials availability

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Code availability

Not applicable.

Declarations

Conflict of interest

The authors declare no conflict of interest.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Not applicable.

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