1887

Abstract

is a well characterized lactobacillus for dairy fermentations that is also found in malt whisky fermentations. The two environments contain considerable differences related to microbial growth, including the presence of different growth inhibitors and nutrients. The present study characterized strains originating from dairy fermentations (called milk strains hereafter) and malt whisky fermentations (called whisky strains hereafter) by phenotypic tests and comparative genomics. The whisky strains can tolerate ethanol more than the milk strains, whereas the milk strains can tolerate lysozyme and lactoferrin more than the whisky strains. Several plant-origin carbohydrates, including cellobiose, maltose, sucrose, fructooligosaccharide and salicin, were generally metabolized only by the whisky strains, whereas milk-derived carbohydrates, i.e. lactose and galactose, were metabolized only by the milk strains. Milk fermentation properties also distinguished the two groups. The general genomic characteristics, including genomic size, number of coding sequences and average nucleotide identity values, differentiated the two groups. The observed differences in carbohydrate metabolic properties between the two groups correlated with the presence of intact specific enzymes in glycoside hydrolase (GH) families GH1, GH4, GH13, GH32 and GH65. Several GHs in the milk strains were inactive due to the presence of stop codon(s) in genes encoding the GHs, and the inactivation patterns of the genes encoding specific enzymes assigned to GH1 in the milk strains suggested a possible diversification manner of strains. The present study has demonstrated how strains have adapted to their habitats.

Funding
This study was supported by the:
  • Tokyo University of Agriculture
    • Principle Award Recipient: NotApplicable
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2021-04-26
2022-01-21
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References

  1. Hébert EM, Raya RR, Tailliez P, de Giori GS. Characterization of natural isolates of Lactobacillus strains to be used as starter cultures in dairy fermentation. Int J Food Microbiol 2000; 59:19–27 [View Article][PubMed]
    [Google Scholar]
  2. Nalbantoglu U, Cakar A, Dogan H, Abaci N, Ustek D et al. Metagenomic analysis of the microbial community in kefir grains. Food Microbiol 2014; 41:42–51 [View Article][PubMed]
    [Google Scholar]
  3. Shangpliang HNJ, Rai R, Keisam S, Jeyaram K, Tamang JP. Bacterial community in naturally fermented milk products of Arunachal Pradesh and Sikkim of India analysed by high-throughput amplicon sequencing. Sci Rep 2018; 8:1532 [View Article][PubMed]
    [Google Scholar]
  4. Miyamoto M, Ueno HM, Watanabe M, Tatsuma Y, Seto Y et al. Distinctive proteolytic activity of cell envelope proteinase of Lactobacillus helveticus isolated from airag, a traditional Mongolian fermented mare's milk. Int J Food Microbiol 2015; 197:65–71 [View Article][PubMed]
    [Google Scholar]
  5. Oki K, Dugersuren J, Demberel S, Watanabe K. Pyrosequencing analysis of the microbial diversity of airag, khoormog and tarag, traditional fermented dairy products of Mongolia. Biosci Microbiota Food Health 2014; 33:53–64 [View Article][PubMed]
    [Google Scholar]
  6. Akabanda F, Owusu-Kwarteng J, Tano-Debrah K, Glover RL, Nielsen DS et al. Taxonomic and molecular characterization of lactic acid bacteria and yeasts in nunu, a Ghanaian fermented milk product. Food Microbiol 2013; 34:277–283 [View Article][PubMed]
    [Google Scholar]
  7. Ercolini D, Frisso G, Mauriello G, Salvatore F, Coppola S. Microbial diversity in natural whey cultures used for the production of Caciocavallo Silano PDO cheese. Int J Food Microbiol 2008; 124:164–170 [View Article][PubMed]
    [Google Scholar]
  8. Slattery L, O'Callaghan J, Fitzgerald GF, Beresford T, Ross RP. Invited review: Lactobacillus helveticus – a thermophilic dairy starter related to gut bacteria. J Dairy Sci 2010; 93:4435–4454 [View Article][PubMed]
    [Google Scholar]
  9. Burns P, Molinari F, Beccaria A, Páez R, Meinardi C et al. Suitability of buttermilk for fermentation with Lactobacillus helveticus and production of a functional peptide-enriched powder by spray-drying. J Appl Microbiol 2010; 109:1370–1378 [View Article][PubMed]
    [Google Scholar]
  10. Azagra-Boronat I, Massot-Cladera M, Knipping K, Garssen J, Ben Amor K et al. Strain-specific probiotic properties of bifidobacteria and lactobacilli for the prevention of diarrhea caused by rotavirus in a preclinical model. Nutrients 2020; 12:498 [View Article]
    [Google Scholar]
  11. De Andrés J, Manzano S, García C, Rodríguez JM, Espinosa-Martos I et al. Modulatory effect of three probiotic strains on infants' gut microbial composition and immunological parameters on a placebo-controlled, double-blind, randomised study. Benef Microbes 2018; 9:573–584 [View Article][PubMed]
    [Google Scholar]
  12. Vinderola G, Matar C, Perdigón G. Milk fermented by Lactobacillus helveticus R389 and its non-bacterial fraction confer enhanced protection against Salmonella enteritidis serovar Typhimurium infection in mice. Immunobiology 2007; 212:107–118 [View Article][PubMed]
    [Google Scholar]
  13. Cachat E, Priest FG. Lactobacillus suntoryeus sp. nov., isolated from malt whisky distilleries. Int J Syst Evol Microbiol 2005; 55:31–34 [View Article][PubMed]
    [Google Scholar]
  14. van Beek S, Priest FG. Evolution of the lactic acid bacterial community during malt whisky fermentation: a polyphasic study. Appl Environ Microbiol 2002; 68:297–305 [View Article][PubMed]
    [Google Scholar]
  15. van Beek S, Priest FG. Decarboxylation of substituted cinnamic acids by lactic acid bacteria isolated during malt whisky fermentation. Appl Environ Microbiol 2000; 66:5322–5328 [View Article][PubMed]
    [Google Scholar]
  16. Naser SM, Hagen KE, Vancanneyt M, Cleenwerck I, Swings J et al. Lactobacillus suntoryeus Cachat and Priest 2005 is a later synonym of Lactobacillus helveticus (Orla-Jensen 1919) Bergey et al. 1925 (Approved Lists 1980). Int J Syst Evol Microbiol 2006; 56:355–360 [View Article][PubMed]
    [Google Scholar]
  17. Nsogning SD, Fischer S, Becker T. Investigating on the fermentation behavior of six lactic acid bacteria strains in barley malt wort reveals limitation in key amino acids and buffer capacity. Food Microbiol 2018; 73:245–253 [View Article][PubMed]
    [Google Scholar]
  18. Kunji ER, Mierau I, Hagting A, Poolman B, Konings WN. The proteolytic systems of lactic acid bacteria. Antonie van Leeuwenhoek 1996; 70:187–221 [View Article][PubMed]
    [Google Scholar]
  19. Minami J, Odamaki T, Hashikura N, Abe F, Xiao JZ. Lysozyme in breast milk is a selection factor for bifidobacterial colonisation in the infant intestine. Benef Microbes 2016; 7:53–60 [View Article][PubMed]
    [Google Scholar]
  20. Endo A, Tanizawa Y, Tanaka N, Maeno S, Kumar H et al. Comparative genomics of Fructobacillus spp. and Leuconostoc spp. reveals niche-specific evolution of Fructobacillus spp. BMC Genomics 2015; 16:1117 [View Article][PubMed]
    [Google Scholar]
  21. van de Guchte M, Penaud S, Grimaldi C, Barbe V, Bryson K et al. The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proc Natl Acad Sci USA 2006; 103:9274–9279 [View Article][PubMed]
    [Google Scholar]
  22. Vogel RF, Pavlovic M, Ehrmann MA, Wiezer A, Liesegang H et al. Genomic analysis reveals Lactobacillus sanfranciscensis as stable element in traditional sourdoughs. Microb Cell Fact 2011; 10:S6 [View Article][PubMed]
    [Google Scholar]
  23. Endo A, Nakamura S, Konishi K, Nakagawa J, Tochio T. Variations in prebiotic oligosaccharide fermentation by intestinal lactic acid bacteria. Int J Food Sci Nutr 2016; 67:125–132 [View Article]
    [Google Scholar]
  24. Kajitani R, Yoshimura D, Ogura Y, Gotoh Y, Hayashi T. Platanus_B: an accurate de novo assembler for bacterial genomes using an iterative error-removal process. DNA Res 2020; 27:dsaa014 [View Article][PubMed]
    [Google Scholar]
  25. Tanizawa Y, Fujisawa T, Kaminuma E, Nakamura Y, Arita M. DFAST and DAGA: web-based integrated genome annotation tools and resources. Biosci Microbiota Food Health 2016; 35:173–184 [View Article][PubMed]
    [Google Scholar]
  26. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article][PubMed]
    [Google Scholar]
  27. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article][PubMed]
    [Google Scholar]
  28. Tanizawa Y, Tada I, Kobayashi H, Endo A, Maeno S et al. Lactobacillus paragasseri sp. nov., a sister taxon of Lactobacillus gasseri, based on whole-genome sequence analyses. Int J Syst Evol Microbiol 2018; 68:3512–3517 [View Article][PubMed]
    [Google Scholar]
  29. Maeno S, Tanizawa Y, Kanesaki Y, Kubota E, Kumar H et al. Genomic characterization of a fructophilic bee symbiont Lactobacillus kunkeei reveals its niche-specific adaptation. Syst Appl Microbiol 2016; 39:516–526 [View Article][PubMed]
    [Google Scholar]
  30. Contreras-Moreira B, Vinuesa P. GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl Environ Microbiol 2013; 79:7696–7701 [View Article][PubMed]
    [Google Scholar]
  31. Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 2000; 28:33–36 [View Article][PubMed]
    [Google Scholar]
  32. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 2007; 35:W182–W185 [View Article][PubMed]
    [Google Scholar]
  33. Zhang H, Yohe T, Huang L, Entwistle S, Wu P et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 2018; 46:W95–W101 [View Article][PubMed]
    [Google Scholar]
  34. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article][PubMed]
    [Google Scholar]
  35. Andersen S, Møller MS, Poulsen J-CN, Pichler MJ, Svensson B et al. An 1,4-α-glucosyltransferase defines a new maltodextrin catabolism scheme in Lactobacillus acidophilus . Appl Environ Microbiol 2020; 86:e00661-20 [View Article][PubMed]
    [Google Scholar]
  36. Møller MS, Fredslund F, Majumder A, Nakai H, Poulsen JC et al. Enzymology and structure of the GH13_31 glucan 1,6-α-glucosidase that confers isomaltooligosaccharide utilization in the probiotic Lactobacillus acidophilus NCFM. J Bacteriol 2012; 194:4249–4259 [View Article][PubMed]
    [Google Scholar]
  37. Møller MS, Goh YJ, Rasmussen KB, Cypryk W, Celebioglu HU et al. An extracellular cell-attached pullulanase confers branched α-glucan utilization in human gut Lactobacillus acidophilus . Appl Environ Microbiol 2017; 83:e00402-17 [View Article][PubMed]
    [Google Scholar]
  38. Nakai H, Baumann MJ, Petersen BO, Westphal Y, Schols H et al. The maltodextrin transport system and metabolism in Lactobacillus acidophilus NCFM and production of novel alpha-glucosides through reverse phosphorolysis by maltose phosphorylase. FEBS J 2009; 276:7353–7365 [View Article][PubMed]
    [Google Scholar]
  39. Barrangou R, Altermann E, Hutkins R, Cano R, Klaenhammer TR. Functional and comparative genomic analyses of an operon involved in fructooligosaccharide utilization by Lactobacillus acidophilus . Proc Natl Acad Sci USA 2003; 100:8957–8962 [View Article][PubMed]
    [Google Scholar]
  40. Fredslund F, Hachem MA, Larsen RJ, Sørensen PG, Coutinho PM et al. Crystal structure of α-galactosidase from Lactobacillus acidophilus NCFM: insight into tetramer formation and substrate binding. J Mol Biol 2011; 412:466–480 [View Article][PubMed]
    [Google Scholar]
  41. Sheridan PO, Martin JC, Lawley TD, Browne HP, Harris HMB et al. Polysaccharide utilization loci and nutritional specialization in a dominant group of butyrate-producing human colonic Firmicutes . Microb Genom 2016; 2:e000043 [View Article][PubMed]
    [Google Scholar]
  42. Sakurai T, Hashikura N, Minami J, Yamada A, Odamaki T et al. Tolerance mechanisms of human-residential bifidobacteria against lysozyme. Anaerobe 2017; 47:104–110 [View Article][PubMed]
    [Google Scholar]
  43. Schuster JA, Vogel RF, Ehrmann MA. Biodiversity of Lactobacillus helveticus isolates from dairy and cereal fermentations reveals habitat-adapted biotypes. FEMS Microbiol Lett 2020; 367:fnaa058 [View Article][PubMed]
    [Google Scholar]
  44. Viiard E, Mihhalevski A, Rühka T, Paalme T, Sarand I. Evaluation of the microbial community in industrial rye sourdough upon continuous back-slopping propagation revealed Lactobacillus helveticus as the dominant species. J Appl Microbiol 2013; 114:404–412 [View Article][PubMed]
    [Google Scholar]
  45. Callanan M, Kaleta P, O'Callaghan J, O'Sullivan O, Jordan K et al. Genome sequence of Lactobacillus helveticus, an organism distinguished by selective gene loss and insertion sequence element expansion. J Bacteriol 2008; 190:727–735 [View Article][PubMed]
    [Google Scholar]
  46. Broadbent JR, Hughes JE, Welker DL, Tompkins TA, Steele JL. Complete genome sequence for Lactobacillus helveticus CNRZ 32, an industrial cheese starter and cheese flavor adjunct. Genome Announc 2013; 1:e00590-13 [View Article][PubMed]
    [Google Scholar]
  47. Schmid M, Muri J, Melidis D, Varadarajan AR, Somerville V et al. Comparative genomics of completely sequenced Lactobacillus helveticus genomes provides insights into strain-specific genes and resolves metagenomics data down to the strain level. Front Microbiol 2018; 9:63 [View Article][PubMed]
    [Google Scholar]
  48. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B et al. Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 2006; 103:15611–15616 [View Article][PubMed]
    [Google Scholar]
  49. Cai H, Thompson R, Budinich MF, Broadbent JR, Steele JL. Genome sequence and comparative genome analysis of Lactobacillus casei: insights into their niche-associated evolution. Genome Biol Evol 2009; 1:239–257 [View Article][PubMed]
    [Google Scholar]
  50. Trollope KM, van Wyk N, Kotjomela MA, Volschenk H. Sequence and structure-based prediction of fructosyltransferase activity for functional subclassification of fungal GH32 enzymes. FEBS J 2015; 282:4782–4796 [View Article][PubMed]
    [Google Scholar]
  51. Tanno H, Fujii T, Hirano K, Maeno S, Tonozuka T et al. Characterization of fructooligosaccharide metabolism and fructooligosaccharide-degrading enzymes in human commensal butyrate producers. Gut Microbes 2021; 13:1–20 [View Article][PubMed]
    [Google Scholar]
  52. Menéndez C, Martínez D, Pérez ER, Musacchio A, Ramírez R et al. Engineered thermostable β-fructosidase from Thermotoga maritima with enhanced fructooligosaccharides synthesis. Enzyme Microb Technol 2019; 125:53–62 [View Article][PubMed]
    [Google Scholar]
  53. Schwab C, Sørensen KI, Gänzle MG. Heterologous expression of glycoside hydrolase family 2 and 42 β-galactosidases of lactic acid bacteria in Lactococcus lactis . Syst Appl Microbiol 2010; 33:300–307 [View Article][PubMed]
    [Google Scholar]
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