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Lactobacillus Allii Sp. Nov. Isolated from Scallion Kimchi

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Lactobacillus Allii Sp. Nov. Isolated from Scallion Kimchi TAXONOMIC DESCRIPTION Jung et al., Int J Syst Evol Microbiol 2017;67:4936–4942 DOI 10.1099/ijsem.0.002327 Lactobacillus allii sp. nov. isolated from scallion kimchi Min Young Jung, Se Hee Lee, Moeun Lee, Jung Hee Song and Ji Yoon Chang* Abstract A novel strain of lactic acid bacteria, WiKim39T, was isolated from a scallion kimchi sample consisting of fermented chili peppers and vegetables. The isolate was a Gram-positive, rod-shaped, non-motile, catalase-negative and facultatively anaerobic lactic acid bacterium. Phylogenetic analysis of the 16S rRNA gene sequence showed that strain WiKim39T belonged to the genus Lactobacillus, and shared 97.1–98.2 % pair-wise sequence similarities with related type strains, Lactobacillus nodensis, Lactobacillus insicii, Lactobacillus versmoldensis, Lactobacillus tucceti and Lactobacillus furfuricola. The G+C content of the strain based on its genome sequence was 35.3 mol%. The ANI values between WiKim39T and the closest relatives were lower than 80 %. Based on the phenotypic, biochemical, and phylogenetic analyses, strain WiKim39T represents a novel species of the genus Lactobacillus, for which the name Lactobacillus allii sp. nov. is proposed. The type strain is WiKim39T (=KCTC 21077T=JCM 31938T). Fermented foods and beverages not only provide important Strain WiKim39T was isolated from scallion kimchi in nutrients but also have great potential for maintaining Gwangju, Korea, using the dilution plating method with health and preventing disease, and they play an important MRS agar medium (MRSA; BBL) at 30 C for 48 h. Single role in the human diet worldwide [1, 2]. Kimchi is the most colonies on the plates were transferred to new plates and well-known traditional fermented food in Korea, and it is incubated on MRS agar at 30 C under anaerobic conditions. made from various raw materials, such as napa cabbage, The reference strains used in this study, Lactobacillus radish, red pepper, garlic, ginger, radish, and fermented sea- nodensis KACC 16346T, Lactobacillus insicii DSM 29801T, food (jeotgal) [3]. Kimchi contains various vitamins and Lactobacillus versmoldensis KCTC 3814T, Lactobacillus tuc- health-promoting components, and it provides health bene- ceti KCTC 21005T and Lactobacillus furfuricola KCTC fits such as antiobesity, anticancer, antioxidation, antimuta- 21034T, were cultured in MRS medium according to the cul- gen, and anti-atherosclerotic effects [4–6]. In addition, ture collection guidelines. Cells of strain WiKim39T grown many lactic acid bacteria (LAB) of the genera Leuconostoc, on MRS were Gram-stained and visualized under light Weissella and Lactobacillus are involved in the fermentation microscopy and transmission electron microscopy (TEM, process of kimchi [7]. The genus Lactobacillus belongs to Hitachi 7000 electron microscope). Bacterial growth at vari- the large group of LAB producing lactic acid by carbohy- ous pH values (3.0–10.0 in 0.5-unit increments) was mea- drate fermentation. These bacteria are characterized as sured by inoculating pH-adjusted MRS media with HCl or Gram-positive, non-spore-forming rods, which have a low KOH. The optimum growth temperature and tolerance to G+C content, and are catalase-negative, non-motile micro- NaCl of the cells were also measured. For these studies, cells organisms [8, 9]. Members of the genus Lactobacillus are were grown at temperatures ranging from 15 to 60 C and in usually found in plants; plant-derived materials such as 0–10 % (w/v) NaCl for 48 h. Growth was monitored by mea- silage, grains, and foods; and the gastrointestinal tract of suring OD600 using a UV-1600 spectrometer (Shimadzu). humans and animals. Lactobacillus strains are currently Growth under anaerobic conditions was tested on MRS agar used as probiotics, starters, and silage inoculants in food (Difco) using GasPak jars (BBL) at 30 C. Motility was and feed fermentation [10]. In the present study, a novel tested in MRS medium with 0.4 % agar. Physiological char- strain within the genus Lactobacillus, which is used in the acteristics (acid production, carbon-source utilization, food and feed industries, was isolated from scallion kimchi, enzyme activities, and biochemical features) were deter- and the phenotypic, chemotaxonomic, and molecular char- mined using the API 50CH, API ZYM, API 20E, and acteristics of the novel LAB strain WiKim39T are presented. API 20 Strep galleries according to the manufacturer’s Author affiliation: Microbiology and Functionality Research Group, World Institute of Kimchi, Gwangju 61755, Republic of Korea. *Correspondence: Ji Yoon Chang, [email protected] Keywords: Lactobacillus allii; kimchi; lactic acid bacteria; novel species. Abbreviations: ANI, average nucleotide identity; LAB, lactic acid bacteria; pheS, phenylalanyl-tRNA synthase alpha subunit; rpoA, RNA polymerase alpha subunit. The GenBank/EMBL/DDBJ accession numbers of the complete genome sequences of strain WiKim39T are CP019323 (chromosome) and CP019324 (plasmid). 002327 ã 2017 IUMS This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited. 4936 Jung et al., Int J Syst Evol Microbiol 2017;67:4936–4942 instructions (bioMerieux). Catalase activity was determined version 7 [16] after multiple sequence alignment of the data by assessing the production of oxygen bubbles in 3 % (v/v) using CLUSTAL_X [17]. Phylogenic trees were constructed aqueous hydrogen peroxide solution. Oxidase activity was using the neighbour-joining (NJ), minimum-evolution, and measured using an Oxy-swab (bioMerieux) according to the maximum-likelihood methods, and bootstrap values were manufacturer’s recommendations. For haemolysis testing, calculated on the basis of 1000 replications. the bacteria were streaked on MRS agar containing 5 % Based on the pairwise 16S rRNA gene sequence similarities, (w/v) sheep’s blood and incubated for 48 h at 30 C. Tellur- T the closest phylogenetic relatives to strain WiKim39 were ite tolerance tests were performed by supplementation with T Lactobacillus nodensis DSM 19682 (98.2 %), Lactobacillus 0.04 % K TeO (Sigma-Aldrich). Lactic acid production was T 2 3 insicii TMW1.2011 (98.1 %), Lactobacillus versmoldensis quantified using a DL-lactic acid assay kit (Megazyme KU-3T (97.5 %), Lactobacillus tucceti CECT 5920T (97.3 %), International). and Lactobacillus furfuricola JCM 18764T (97.1 %). The 16S Cells of strain WiKim39T were rods with an average length rRNA analysis clearly indicated that the isolate represented of 0.6Â1.8–2.5 µm. The strain was identified as a facultative a novel genomic species in the genus Lactobacillus, as none anaerobe, and it grew at temperatures from 25 to 37 C and of the valid described species showed more than 98.7 % 16S at a pH from 4.5 to 9.0 with optimum growth at 30 C and rRNA similarity [18]. The phylogenetic relationships T pH 6.5–7.0. No growth was observed at 20 C and pH between strain WiKim39 and related Lactobacillus species 4.0 or 40 C and 7 % (w/v) NaCl lÀ1. Positive reactions are shown in Fig. 1. were observed in tests for the production of acid from D- Phylogenetic analysis based on the housekeeping genes galactose, D-glucose, D-fructose, N-acetylglucosamine, encoding phenylalanyl-tRNA synthase alpha subunit (pheS) amygdalin, arbutin, aesculin ferric citrate, salicin, D-cellobi- and RNA polymerase alpha subunit (rpoA) showed that the ose, D-maltose, D-lactose, D-sucrose, and gentiobiose. In closest phylogenetic relative strains of strain WiKim39T addition, enzyme detection with an API zym kit was posi- were type strains of Lactobacillus nodensis, Lactobacillus tive for alkaline phosphatase, esterase, leucine arylamidase, insicii, and Lactobacillus tucceti, with 84.4–87.6 % pheS gene valine arylamidase, acid phosphatase, naphtol-AS-BI-phos- sequence similarity and 89.5–94.5 % rpoA gene sequence phohydrolase, a-glucosidase, b-glucosidase, and N-acetyl- similarity (Fig. 2). These gene sequence divergence values b-glucosaminidase. No esterase lipase, cystine arylamidase, for pheS and rpoA between strain WiKim39T and reference trypsin, a-chymotrypsin, a-galactosidase, b-galactosidase, strains indicate that strain WiKim39T represents a novel b-glucuronidase, a-mannosidase, or a-fucosidase activities species within the genus Lactobacillus [19]. were observed. Biochemical features were negative for DNA–DNA hybridization was performed using the fluoro- nitrate and nitrite reduction; production of indole, H2S, ure- ase, pyrrolidonyl arylamidase, arginine dihydrolase; or metric hybridization method in microdilution wells as T described previously [20]. The DNA–DNA hybridization hydrolysis of gelatin and hippurate. WiKim39 showed T g values between strain WiKim39 and Lactobacillus nodensis non-haemolysis ( -haemolysis) and tellurite tolerance. The T T novel species could be differentiated from all other tested KACC 16346 , Lactobacillus insicii DSM 29801 , Lactoba- cillus versmoldensis KCTC 3814T, Lactobacillus tucceti reference type strains using its physiological properties T T (Table 1). It was found to produce D- and L-lactic acid at a KCTC 21005 , and Lactobacillus furfuricola KCTC 21034 ratio of 52 : 48. Previously reported reference strains pro- were 51.5, 48.1, 39.2, 29.3, and 30.7 %, respectively. The – duce significantly more L-lactic acid than D-lactic acid, DNA DNA relatedness values between the novel isolate T whereas strain WiKim39 produced slightly
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