Abstract
A novel Gram-stain-positive, non-motile, non-spore-forming, rod-shaped, facultatively anaerobic, designated strain HSLZ-75T, was isolated from the solid-state vinegar culture of Zhenjiang aromatic vinegar. Strain HSLZ-75T grew at 20–40 °C (optimum 35 °C), pH 3.0–5.0 (optimum pH 4.0) and 0–5% (w/v) NaCl (optimum 0%). Heterolactic fermentation characterised the metabolism of strain HSLZ-75T. d- and l-lactic acid were produced from glucose in a ratio of 91:9. The major cellular fatty acids ( > 10%) consisted of C16:0, C18:1ω9c, summed feature 8 (C18:1ω7c and/or C18:1ω6c) and C19:0 cyclo ω8c. The polar lipids consisted of diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, one unidentified aminophospholipid, one unidentified phospholipid and six unknown lipids. The cell wall was found to contain meso-diaminopimelic acid-type peptidoglycan. The 16S rRNA gene sequence of strain HSLZ-75T showed the highest similarity of 88.0% with Lactobacillus fructivorans DSM 20203T. Phylogenetic analysis indicated that strain HSLZ-75T belonged to family Lactobacillaceae and formed a distinct lineage with the type strain of Lactobacillus caviae. The complete genome of strain HSLZ-75T contained a circular chromosome of 1,616,430 bp with 1570 genes and 39.7 mol% G + C content. The average nucleotide identity values between strain HSLZ-75T and the reference type strains Lactobacillus fructivorans DSM 20203T and Lactobacillus rossiae DSM 15814T were 66.4% and 65.7%, respectively. On the basis of phenotypic, chemotaxonomic, phylogenetic and genotypic characteristics, strain HSLZ-75T should be classified as a novel species of the genus Lactobacillus in the family Lactobacillaceae of the order Lactobacillales, for which the name Lactobacillus **shani sp. nov. is proposed. The type strain is HSLZ-75T ( = CICC 6269T = JCM 33270T).
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References
Cagno RD, Angelis MD, Cattonaro F, Gobbetti M (2015) Draft genome sequence of Lactobacillus rossiae DSM 15814T. J Bacteriol 194:5460–5461
Canchaya C, Claesson MJ, Fitzgerald GF, van Sinderen D, O’Toole PW (2006) Diversity of the genus Lactobacillus revealed by comparative genomics of five species. Microbiology 152:3185–3196
Collins MD, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycan based on 2,4-diaminobutyric acid. J Appl Bacteriol 48:459–470
Collins MD, Farrow JAE, Phillips BA, Feresu S, Jones D (1987) Classification of Lactobacillus divergens, Lactobacillus piscicola, and some catalase-negative asporogenous, rod-shaped bacteria from poultry in a new genus, Carnobacterium. Int J Syst Bacteriol 37:310–316
Corsetti A, Settanni L, van Sinderen D, Felis GE, Dellaglio F, Gobbetti M (2005) Lactobacillus rossii sp. nov., isolated from wheat sourdough. Int J Syst Evol Microbiol 55:35–40
Dellaglio F, Trovatelli LD, Sarra PG (1981) DNA–DNA homology among representative strains of the genus Pediococcus. Zbl Bakt Hyg I Abt Orig C 2:140–150
Drucker DB, Megson G, Harty DW, Riba I, Gaskell SJ (1995) Phospholipids of Lactobacillus spp. J Bacteriol 177:6304–6308
Duar RM, Lin XB, Zheng J, Martino ME, Grenier T, Pérez-Muñoz ME, Leulier F, Gänzle M, Walter J (2017) Lifestyles in transition: evolution and natural history of the genus Lactobacillus. FEMS Microbiol Rev 41:S27–S48
Ehrmann MA, Kröckel L, Lick S, Radmann P, Bantleon A, Vogel RF (2016) Lactobacillus insicii sp. nov. isolated from fermented raw meat. Int J Syst Evol Microbiol 66:236–242
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Franzmann PD, Höpfl P, Weiss N, Tindall BJ (1991) Psychrotrophic, lactic acid-producing bacteria from anoxic waters in Ace Lake, Antarctica; Carnobacterium funditum sp. nov. and Carnobacterium alterfunditum sp. nov. Arch Microbiol 156:255–262
Jöborn A, Dorsch M, Olsson JC, Westerdahl A, Kjelleberg S (1999) Carnobacterium inhibens sp. nov., isolated from the intestine of Atlantic salmon (Salmo salar). Int J Syst Bacteriol 49:1891–1898
Johnson MJ, Thatcher E, Cox ME (1995) Techniques for controlling variability in gram staining of obligate anaerobes. J Clin Microbiol 33:755–758
Kandler O (1970) Amino acid sequence of the murein and taxonomy of the genera Lactobacillus, Bifidobacterium, Leuconostoc, and Pediococcus. Int J Syst Bacteriol 20:491–507
Killer J, Pechar R, Svec P, Salmonová H, Svejstil R, Geigerová M, Rada V, Vlková E, Mekadim C (2017) Lactobacillus caviae sp. nov., an obligately heterofermentative bacterium isolated from the oral cavity of a guinea pig (Cavia aperea f. porcellus). Int J Syst Evol Microbiol 67:2903–2909
Kim J, Chun J, Han HU (2000) Leuconostoc kimchii sp. nov., a new species from kimchi. Int J Syst Evol Microbiol 50:1915–1919
Kim MS, Roh SW, Nam YD, Yoon JH, Bae JW (2009) Carnobacterium jeotgali sp. nov., isolated from a Korean traditional fermented food. Int J Syst Evol Microbiol 59:3168–3171
Kim HJ, Eom SJ, Park SJ, Cha CJ, Kim GB (2011) Lactobacillus alvi sp. nov., isolated from the intestinal tract of chicken. FEMS Microbiol Lett 323:83–87
Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721
Kim HJ, Lee HJ, Lim B, Kim E, Kim HY, Suh M, Hur M (2018) Lactobacillus terrae sp. nov., a novel species isolated from soil samples in the Republic of Korea. Int J Syst Evol Microbiol 68:2906–2911
Kozaki M, Uchimura T, Okada S (1992) Experimental manual of lactic acid bacteria. Asakurasyoten, Tokyo, pp 29–72
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Luo R, Liu B, **e Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, Tang J, Wu G, Zhang H, Shi Y, Liu Y (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18
Meucci A, Zago M, Rossetti L, Fornasari ME, Bonvini B, Tidona F, Povolo M, Contarini G, Carminati D, Giraffa G (2015) Lactococcus hircilactis sp. nov. and Lactococcus laudensis sp. nov., isolated from milk. Int J Syst Evol Microbiol 65:2091–2096
Minnikin DE, Collins MD, Goodfellow M (1979) Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 47:87–95
Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaala A, Parletta JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241
Miyashita M, Yukphan P, Chaipitakchonlatarn W, Malimas T, Sugimoto M, Yoshino M, Kamakura Y, Potacharoen W, Tanasupawat S, Tanaka N, Nakagawa Y, Suzuki K (2015) Lactobacillus plajomi sp. nov. and Lactobacillus modestisalitolerans sp. nov., isolated from traditional fermented foods. Int J Syst Evol Microbiol 65:2485–2490
Na SI, Kim YO, Yoon SH, Ha SM, Baek I, Chun J (2018) UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 56:280–285
Nam SH, Choi SH, Kang A, Li KS, Kim DW, Kim RN, Kim DS, Park HS (2012) Genome sequence of Lactobacillus fructivorans KCTC 3543. J Bacteriol 194:2111–2112
Praet J, Meeus I, Cnockaert M, Houf K, Smagghe G, Vandamme P (2015) Novel lactic acid bacteria isolated from the bumble bee gut: Convivina intestini gen. nov., sp. nov., Lactobacillus bombicola sp. nov., and Weissella bombi sp. nov. Antonie van leeuwenhoke 107:1337–1349
Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131
Rzhetsky A, Nei M (1992) A simple method for evaluating and testing minimum-evolution trees. Mol Biol Evol 9:945–967
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. Technical Note 101. Microbial ID, Newark, DE
Schumann P (2011) Peptidoglycan structure. Methods Microbiol 38:101–129
Sorokin DY (2005) Is there a limit for high-pH life? Int J Syst Evol Microbiol 55:1405–1406
Sukontasing S, Tanasupawat S, Moonmangmee S, Lee JS, Suzuki K (2007) Enterococcus camelliae sp. nov. isolated from fermented tea leaves in Thailand. Int J Syst Evol Microbiol 57:2151–2154
Tanasupawat S, Shida O, Okada S, Komagata K (2000) Lactobacillus acidipiscis sp. nov. and Weissella thailandensis sp. nov. isolated from fermented fish in Thailand. Int J Syst Evol Microbiol 50:1479–1485
Tanasupawat S, Thongsanit J, Okada S, Komagata K (2002) Lactic acid bacteria isolated from soy sauce mash in Thailand. J Gen Appl Microbiol 48:201–209
Tanasupawat S, Pakdeeto A, Thawai C, Yukphan P, Okada S (2007) Identification of lactic acid bacteria from fermented tea leaves (miang) in Thailand and proposals of Lactobacillus thailandensis sp. nov. Lactobacillus camelliae sp. nov., and Pediococcus siamensis sp. nov. J Gen Appl Microbiol 53:7–15
Tanasupawat S, Sukontasing S, Lee JS (2008) Enterococcus thailandicus sp. nov. isolated from fermented sausage (‘mum’) in Thailand. Int J Syst Evol Microbiol 58:1630–1634
Tohno M, Kitahara M, Uegaki R, Lrisawa T, Ohkuma M, Tajima K (2013) Lactobacillus hokkaidonensis sp. nov. isolated from subarctic timothy grass (Phleum pratense L.) silage. Int J Syst Evol Microbiol 63:2526–2531
Wade ME, Strickland MT, Osborne JP, Edwards CG (2019) Role of Pediococcus in winemaking. Aust J Grape Wine R 25:7–24
Wang ZM, Lu ZM, Yu YJ, Li GQ, Shi JS, Xu ZH (2015) Batch-to-batch uniformity of bacterial community succession and flavor formation in the fermentation of Zhenjiang aromatic vinegar. Food Microbiol 50:64–69
Wang ZM, Lu ZM, Shi JS, Xu ZH (2016) Exploring flavour-producing core microbiota in multispecies solid-state fermentation of traditional Chinese vinegar. Sci Rep 6:26818
Weiss N, Schillinger U, Laternser M, Kandler O (1981) Lactobacillus sharpeae sp. nov. and Lactobacillus agilis sp. nov., two new species of homofermentative, meso-diaminopimelic acid containing lactobacilli isolated from sewage. Zbl Bakt Hyg I Abt Orig C 2:242–253
Weiss N, Schillinger U, Kandler O (1983) Lactobacillus trichodes, and Lactobacillus heterohiochii, subjective synonyms of Lactobacillus fructivorans. Syst Appl Microbiol 4:507–511
Wu LH, Lu ZM, Zhang XJ, Wang ZM, Yu YJ, Shi JS, Xu ZH (2017) Metagenomics reveals flavour metabolic network of cereal vinegar microbiota. Food Microbiol 62:23–31
Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer KH, Whitman WB, Euzéby J, Amann R, Rosselló-Móra R (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617
Zanoni P, Farrow JAE, Phillips BA, Collins MD (1987) Lactobacillus pentosus (Fred, Peterson and Anderson) sp. nov., nom. rev. Int J Syst Bacteriol 37:339–341
Zhang J, Fang F, Chen J, Du G (2014) The arginine deiminase pathway of koji bacteria is involved in ethyl carbamate precursor production in soy sauce. FEMS Microbiol Lett 358:91–97
Acknowledgements
We would like to express our gratitude to Prof. Henglin Cui for helpful discussions, are grateful to Prof. Aharon Oren (the Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem) for the suggestions for the nomination in this study. This study was financially supported by the National key research and development program of China (No. 2018YFD0400401) and the Key research and development program of Zhenjiang (No. Y2017011).
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YY, ZML and ZHX designed the experiments. XL, JZ and LJC conducted the experiments. XL, JZ, LJC and ZML analysed the results. YY, XL, JZ, LJC, ZML and ZHX prepared the manuscript. All authors read and approved the final manuscript.
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Yu, Y., Li, X., Zhang, J. et al. Lactobacillus **shani sp. nov., isolated from solid-state vinegar culture of Zhenjiang aromatic vinegar. Antonie van Leeuwenhoek 113, 43–54 (2020). https://doi.org/10.1007/s10482-019-01316-1
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DOI: https://doi.org/10.1007/s10482-019-01316-1