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Isolation and Identification of Lactic Acid Bacteria in Traditional Fermented Sushi, Funazushi, from Japan

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Isolation and Identification of Lactic Acid Bacteria in Traditional Fermented Sushi, Funazushi, from Japan Food Sci. Technol. Res., 18 (1), 77–82, 2012 Isolation and Identification of Lactic Acid Bacteria in Traditional Fermented Sushi, Funazushi, from Japan 1 2 1 1* Harutoshi Tsuda , Kenzo kuboTa , Teruki MaTsuMoTo and Yoshiko ishiMi 1 National Institute of Health and Nutrition, 1-23-1 Toyama, Shinjuku-ku, Tokyo 162-8063, Japan 2 Department of Biotechnology, Faculty of Life Sciences, Ritsumeikan University, 1-1-1, Nojihigashi, Kusatsu, Shiga 525-8577, Japan Received June 21, 2011; Accepted September 8, 2011 The lactic acid bacterial flora in commercial and homemade Funazushi (fermented crucian carp and rice) were investigated. Funazushi is a fermented fish product that continues to be produced in the traditional style in Japan. Lactic acid bacteria in four commercial and five homemade Funazushi were enumerated. The viable counts of commercial samples ranged from 3.0 × 103 to 2.7 × 105 cfu/g, with an average of 2.4 × 104 cfu/g, while the viable counts of homemade samples ranged from 2.0 × 102 to 2.6 × 107 cfu/g, with an average of 1.3 × 105 cfu/g. Twenty-seven lactic acid bacteria isolates were obtained from the commercial samples, and identified as Streptococcus salivarius, Lactobacillus buchneri, and Lactobacillus parabuchneri. Forty-eight isolates were obtained from the homemade samples, and identified as Lactoba- cillus plantarum, Lb. buchneri, Lactobacillus alimentarius, Lactobacillus farciminis, Lactobacillus acidipis- cis, and Lactobacillus casei. Lb. buchneri was the predominant species in commercial Funazushi, while Lb. plantarum and Lb. buchneri were the predominant species in the homemade products. Keywords: lactic acid bacteria, microbial flora, fermented fish product, funazushi Introduction rel, and 8. the fish is fermented under the pressure of stones Fermented fish products called “narezushi” have long for 1 year (Fujii, 2001). been produced in Japan. Narezushi is a general term for Lactic acid bacteria (LAB) are the main fermentative mi- fermented cured fish and boiled rice. The fish and rice are croorganisms in Funazushi. Determination of the microflora usually fermented in barrels, under the pressure of stones, for of Funazushi using culture-based methods and molecular more than one year (Fujii et al., 2011). Many kinds of nar- biological techniques has been reported (Fujii et al., 2008, ezushi, e.g., Funazushi, sabanarezushi, and izushi, are known Fujii et al., 2011, Isobe et al., 2002). These studies investi- in Japan, and Funazushi is thought to have remained true gated one or two samples; therefore, investigation of mul- to the traditional style (Fujii et al., 2008). Funazushi is pro- tiple Funazushi samples would be worthwhile. duced around Lake Biwa in Shiga Prefecture and is a unique Funazushi has been experimentally noted to have benefi- sour tasting product of lactic fermented funa (crucian carp, cial health effects, including the cure of diarrhea (Ohshima Carassius buergeri grandoculis) and rice. The production and Fujii, 1994). Furthermore, Funazushi may be a good process of commercial Funazushi is as follows: 1. the scales, source of useful microorganisms. In the present study, we gills, and internal organs of crucian carp are removed, 2. the isolated and identified the LAB in commercial and home- carp is cured, 3. the fish is fermented in barrels under the made Funazushi. A comparison of commercial and home- pressure of stones for 1 year (a few months in the homemade made products would help in understanding the LAB micro- process), 4. the salt is washed out from the fish, 5. salted rice flora of Funazushi. Furthermore, these data could be useful is stuffed into the fish abdominal cavity, 6. the carp and salt- not only for the development of more efficient fermentation ed rice are placed in barrels, 7. salt water is added to the bar- and preservation techniques for traditional fermented fish products, but also in the investigation of the source of the *To whom correspondence should be addressed. beneficial health effects of Funazushi. E-mail: [email protected] 78 h. Tsuda et al. Materials and Methods Tween 80 1.0 g/L, and L-cysteine HCl monohydrate 0.1 g/L, Salinity of Funazushi Salinity of Funazushi samples BCP 60 mg/L, pH 6.8 ± 0.2). The test strain was subcultured was determined with an atomic absorption spectrometer in 5 mL TYLG broth at 30℃ for 24 - 48 h, and the culture (Spectra AA220, Varian Techtron Pty Ltd., Victoria, Austra- was centrifuged (1,000 × g, 10 min). The cells were washed lia) (AOAC 969.23). Samples were generated by mixing an with 5 mL sterile 0.85 % NaCl solution and 50 μL of this cell equal amount of fish muscle and rice. suspension was inoculated into each sugar medium, and in- Enumeration and isolation of lactic acid bacteria Nine cubated for 7 days. The color change of BCP in the medium Funazushi samples were used (Fig. 1). Four samples were by acid production was determined. purchased from four different companies in Shiga Prefecture, 16S rRNA gene analysis Total DNA was extracted from and five samples were home produced in Shiga Prefecture. bacterial strains (Reyes-Gavilan et al., 1992). The 16S rRNA All samples were brought to the laboratory in a cooler box gene was amplified by PCR using Takara EX Taq (Takara (approximately 10℃) and stored in the refrigerator (4℃) un- Bio, Shiga, Japan). The bacteria-specific primer sequences til analyzed. were 5′-GTTTGATCCTGGCTCA-3′ (10F) and 5′-TAC- Samples (1 g) were serially diluted in sterile 0.85% NaCl CAGGGTATCTAATCC-3′ (800R), and PCR was performed solution (10 mL), plated on Plate Count Agar with bromocre- for 30 cycles (30 sec 94℃, 60 sec 55℃ and 60 sec 70℃). sol purple (BCP agar, Nissui, Japan) and MRS agar (Oxoid, PCR products were purified with phenol extraction and etha- Hampshire, England) containing cycloheximide (10 mg/L), nol precipitation. The purified fragments were sequenced. and incubated at 20 and 37℃ for 3−5 days. Colonies were Sequencing reactions of the purified fragments were per- enumerated, and individual colonies were picked randomly formed in a BioRad DNA Engine Dyad PTC-220 Peltier and purified by streaking. Thermal Cycler using an ABI BigDye Terminator v3.1 The strains were incubated in TYLG broth (tryptone 10 Cycle Sequencing Kit with AmpliTaq DNA polymerase (FS g/L, yeast extract 5.0 g/L, lactose 5.0 g/L, glucose 5.0 g/L, enzyme, Applied Biosystems, CA, USA). The fluorescent- Tween 80 1.0 g/L, and L-cysteine HCl monohydrate 0.1 g/ labeled fragments were purified with an ethanol precipitation L, pH 6.8 ± 0.2) and stock cultures were maintained in 10% reconstituted skim milk at −20℃. Identification and characterization of lactic acid bacteria The isolated strains were identified based on their physiolog- ical and biochemical characteristics as described by de Vos et al. (2009) and Wood and Holzapfel (1995), as well as by 16S rRNA sequence analysis. The tests included Gram-staining, catalase test, growth temperature test, production of gas from glucose, the type of lactic acid isomer, NH3 production from arginine, salt toler- ance and carbohydrate (22 sugars) fermentation. The growth at 10, 40, and 45℃ for lactococci and at 15 and 45℃ for lactobacilli in TYLG broth containing 0.006% BCP, incubated for 7 days, was determined. The production of gas from glucose was determined according to the descrip- tion of Harrigan and McCance (1966). The types of lactic acid isomers produced from glucose were assayed by high- pressure liquid chromatography on a Sumichiral OA-5000 column (Otsuka et al., 1994). Salt tolerance was determined in TYLG broth containing 6.5 and 10% NaCl (w/v) after 3 days incubation. The carbohydrate fermentation profile of all strains was determined as follows. Twenty-two sugars were used (Table 1). Individual sugars were prepared as 5.0% (w/v) solutions, except esculin (2.5% w/v), and the solutions were sterilized using a 0.22 μm filter (Sartorius, Minisart, Germa- Fig. 1. Map of Shiga prefecture, Japan, showing the sam- ny). Next, 0.5 mL of the sterile sugar filtrate was added to 4.5 pling locations. mL of basal medium (tryptone 10 g/L, yeast extract 5.0 g/L, △, commercial Funazushi; ○, homemade Funazushi. Lactic Acid Bacteria in Japanese Traditional Fermented Fish Products, Funazushi 79 Table 1. Taxonomic properties of lactic acid bacteria isolated from commercial Funazushi. No. of isolates 8 17 2 Cell shape cocci rod rod Growth at 10℃ − 15℃ + + 40℃ + 45℃ − − − NH3 from arginine − + + Gas from glucose − + + Lactic acid isomer L DL DL Growth at 6.5% NaCl − Acid detected (No. of + isolates) Amygdalin 2 0 0 D-Arabinose 0 17 2 D-Cellobiose 8 0 0 Esculin 8 0 0 D-Fructose 8 17 2 D-Galactose 2 15 2 D-Glucose 8 17 2 D-Lactose 2 6 0 D-Maltose 8 15 2 D-Mannitol 0 0 0 D-Mannose 8 0 0 D-Melezitose 0 0 2 D-Melibiose 0 16 2 Na-Gluconate 0 17 2 L-Raffinose 8 3 2 L-Rhamnose 0 0 0 D-Ribose 0 14 2 Salicin 8 0 0 D-Sorbitol 8 0 0 Sucrose 8 0 2 D-Trehalose 6 0 0 D-Xylose 0 11 0 16S rRNA sequence Streptococcus Lactobacillus Lactobacillus (No. of tested isolates) salivarius (3) buchneri (14) parabuchneri (1) protocol. The samples were resuspended in distilled water 105 cfu (colony forming unit)/g, with an average of 2.4 × 104 and subjected to electrophoresis in an ABI 3730xl sequencer cfu/g. The viable counts of homemade samples ranged from (Applied Biosystems), and the obtained sequences were ana- 2.0 × 102 to 2.6 × 107 cfu/g, with an average of 1.3 × 105 cfu/g.
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