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Metabolic Characterization of <I>Bacillus</I>

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Metabolic Characterization of <I>Bacillus</I> 1605 Journal of Food Protection, Vol. 77, No. 9, 2014, Pages 1605–1611 doi:10.4315/0362-028X.JFP-14-145 Copyright G, International Association for Food Protection Research Note Metabolic Characterization of Bacillus subtilis and Bacillus amyloliquefaciens Strains Isolated from Traditional Dry-Cured Sausages AIDA CACHALDORA, SONIA FONSECA, MARI´AGO´ MEZ, INMACULADA FRANCO, AND JAVIER CARBALLO* Downloaded from http://meridian.allenpress.com/jfp/article-pdf/77/9/1605/1687240/0362-028x_jfp-14-145.pdf by guest on 26 September 2021 A´ rea de Tecnologı´a de los Alimentos, Facultad de Ciencias de Ourense, Universidad de Vigo, 32004 Ourense, Spain MS 14-145: Received 27 March 2014/Accepted 29 April 2014 ABSTRACT The aim of this study was to investigate the effect of pH, temperature, and NaCl on growth, proteolytic and lipolytic activities, and the ability to produce biogenic amines of 19 strains of Bacillus isolated from Androlla and Botillo (two Spanish traditional sausages) to elucidate the role of these bacteria in sausage manufacture. All strains grew in the presence of 10% salt and at pH values of 5.0 and 5.5, whereas only 9 strains grew at 10uC. Proteolytic activity was assessed by the agar plate method, which revealed that 100 and 94.7% of the strains were able to hydrolyze sarcoplasmic and myofibrillar proteins, respectively. These results were confirmed by electrophoretic assays. The titration method revealed that only two strains hydrolyzed pork fat to any extent, and the profiles of the fatty acids freed were different. Most strains produced biogenic amines, but the quantities were generally low. Raw-fermented sausages are widely consumed meat dairy products, spices, and meat and meat products; products in which the microbial activity plays an important however, these bacteria also play an important role in role during the manufacturing process. Microorganisms are production of fermented products because of their proteo- responsible for the fermentation process and mainly lytic activity (24, 30, 42). responsible for the proteolytic and lipolytic changes that Several Bacillus species (B. subtilis, B. amyloliquefa- occur during the ripening of these products, which ciens, B. pumilus, B. circulans, and B. megaterium) have determines their sensorial characteristics (texture, aroma, been isolated from traditional dry-cured sausages (3, 9, 30). and taste). The presence of Bacillus in fermented sausages seems to be The microbiota of traditional dry-cured sausages is important. In a recent study (14), Bacillus strains were the composed of a wide variety of microorganisms from the raw only microorganisms isolated on manitol salt agar from a materials and the environment (13, 16–18, 40). Two major fermented sausage (Galician chorizo) meat mix before groups of bacteria dominate most of the ripening time and stuffing, with counts of 4.99 log CFU/g. Bacillus in play well-known roles: lactic acid bacteria and gram- fermented sausages have proteolytic and lipolytic activities positive coagulase-negative cocci, mainly represented by (3), which could complement the effects of autochthonous Staphylococcus and Kocuria (8). Lactic acid bacteria enzymes from meat, lactic acid bacteria enzymes, and guarantee the safety of the products through the production coagulase-negative cocci enzymes during sausage ripening. of antimicrobial compounds such as lactic acid and Therefore, the presence of Bacillus should have an effect bacteriocins, and coagulase-negative cocci contribute to (positive or negative) on the organoleptic characteristics of color stability and enhance sensory properties due to the final products. liberation and degradation of amino acids and fatty acids Androlla and Botillo are two traditional sausages (41). However, other microbial groups such as enterobac- widely made and consumed in northwestern Spain (29). teria, Bacillus, and molds and yeasts may also proliferate, Bacillus microorganisms have not been counted directly in but their specific roles are not well understood (20). Androlla or Botillo sausages. However, mean counts on The genus Bacillus consists of a diverse array of gram- standard plate count agar plus 7.5% NaCl were 6.87 log positive aerobic and facultative anaerobic spore-forming CFU/g for Androlla sausages (17) and 6.56 log CFU/g for rods that can be isolated from a wide variety of sources. Botillo sausages (16); approximately 10% of the bacterial Many species are important as food-spoilage organisms and strains from these sausages isolated on the standard plate can contaminate fruits, vegetable products, milk and other count agar plus 7.5% NaCl culture medium were later identified as Bacillus species. * Author for correspondence. Tel: z 34-988-387052; Fax: z 34-988- The aim of this study was to determine the growth and 387001; E-mail: [email protected]. metabolic properties of 19 strains of Bacillus isolated from 1606 CACHALDORA ET AL. J. Food Prot., Vol. 77, No. 9 TABLE 1. Bacillus strain identity, source sausage, lipolytic activity assessed by titration method, and biogenic amine productiona Biogenic amines (ppm) Lipolytic activity Strain no. Species Source (% oleic acid) Putrescine Cadaverine SA06 B. subtilis Androlla 0.22 (0.20–0.24) 18.43 (16.80–20.03) 0.43 (0.41–0.45) SA26 B. amyloliquefaciens Androlla 0.94 (0.92–0.96) 1.22 (1.22–1.22) 3.07 (3.07–3.07) SA28 B. subtilis Androlla 1.26 (1.23–1.29) 0.70 (0.60–0.80) 0.44 (0.31–0.57) SA35 B. amyloliquefaciens Androlla 1.17 (1.14–1.20) 0.76 (0.68–0.84) 1.08 (0.76–1.40) SA37 B. amyloliquefaciens Androlla 0.76 (0.74–0.78) 2.49 (2.46–2.52) 0.53 (0.34–0.72) SA39 B. amyloliquefaciens Androlla 1.08 (1.06–1.10) 2.27 (2.25–2.29) 0.56 (0.29–0.83) SA43 B. amyloliquefaciens Androlla 1.34 (1.30–1.38) 3.27 (3.15–3.39) 2.52 (2.51–2.53) SA50 B. subtilis Androlla 0.15 (0.12–0.18) 1.19 (1.19–1.19) 4.29 (4.29–4.29) SB01 B. subtilis Botillo 0.04 (0.02–0.06) 1.27 (1.27–1.27) 3.08 (3.08–3.08) Downloaded from http://meridian.allenpress.com/jfp/article-pdf/77/9/1605/1687240/0362-028x_jfp-14-145.pdf by guest on 26 September 2021 SB05 B. subtilis Botillo 0.45 (0.10–0.80) 0.57 (0.56–0.58) 0.58 (0.51–0.65) SB07 B. subtilis Botillo 13.86 (13.58–14.14) 0.39 (0.38–0.40) 0.59 (0.32–0.86) SB09 B. amyloliquefaciens Botillo 0.15 (0.12–0.18) 1.33 (1.16–1.50) 0.62 (0.54–0.70) SB13 B. subtilis Botillo 21.19 (21.03–21.35) 0.86 (0.61–1.11) 0.52 (0.39–0.65) SB14 B. subtilis Botillo 0.26 (0.04–0.48) ND ND SB15 B. subtilis Botillo 1.64 (1.61–1.69) ND ND SB16 B. subtilis Botillo 1.03 (0.84–1.22) ND ND SB17 B. subtilis Botillo 0.90 (0.85–0.95) ND ND SB18 B. subtilis Botillo 0.47 (0.47–0.47) ND ND SB26 B. subtilis Botillo 0.31 (0.29–0.33) 1.75 (1.54–1.96) 0.50 (0.44–0.56) a Values are means (ranges) of two replicates. ND, not detected. Androlla and Botillo sausages. This is the first step in Effect of pH, temperature, and NaCl on microbial selecting appropriate strains for further studies (inoculation growth. Each strain was tested for its ability to grow at 10uCin of experimental sausages and analysis of their physico- BHI broth at pH 7.0, in BHI broth adjusted to pH 5 and 5.5 with chemical, microbiological, and organoleptic characteristics), lactic acid, and in BHI broth supplemented with 10 and 15% NaCl. determining the role of Bacillus spp. in the ripening of the Ten microliters of an overnight culture of each strain was inoculated into 5 ml of these test media, and the growth was fermented sausages, and understanding the effect of this scored as positive or negative after incubation at 37uC for 72 h. group of microorganisms on the quality of the final Growth was scored as positive when tubes were more turbid than products. the noninoculated and incubated tubes used as control. MATERIALS AND METHODS Proteolytic activity: qualitative assessment by the agar Bacillus strains and preparation of cell suspensions. The plate method. Sarcoplasmic and myofibrillar proteins were B. subtilis and B. amyloliquefaciens strains used in this study extracted according to the method of Fadda et al. (10). (Table 1) were isolated on standard plate count agar (Oxoid, Sarcoplasmic proteins were sterilized by filtration through a Basingstoke, UK) plus 7.5% NaCl (16, 17). For the Androlla and polyvinylidene fluoride filter (0.22-mm pore size; Millipore, Botillo sausages, 13 of the 200 isolates and 17 of the 150 isolates, Billerica, MA). Myofibrillar proteins were extracted under sterile respectively, found on standard plate count agar plus 7.5% NaCl conditions. The sarcoplasmic and myofibrillar proteins were added were later determined to be Bacillus spp. Strains were identified by at concentrations of 0.5 and 0.2 mg/ml, respectively, to sterile sequencing the 16S rRNA gene and comparing the obtained medium containing 0.25% yeast extract, 0.1% glucose, and 1.5% sequences with those available in the GenBank database (National agar. The medium was poured into petri dishes, and after Center for Biotechnology Information, Bethesda, MD). The solidification, three wells were bored in the agar in each plate, genomic DNA extracted from the Bacillus isolates was then and 40 ml of cell suspension was pipetted into each well. After subjected to repetitive sequence–based PCR analysis using the incubation at 37uC for 48 h, the agar disc was removed from each single oligonucleotide primer (GTG)5 as described by Fonseca dish and stained for 30 min in 0.05% (wt/vol) Coomassie blue et al.
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