1887

Abstract

Ten strains, BG-AF3-A, pH52_RY, WF-MT5-A, BG-MG3-A, Lr3000, RRLNB_1_1, STM3_1, STM2_1, WF-MO7-1 and WF-MA3-C, were isolated from intestinal or faecal samples of rodents, pheasant and primate. 16S rRNA gene analysis identified them as . However, average nucleotide identity and digital DNA–DNA hybridization values based on whole genomes were below 95 and 70 %, respectively, and thus below the threshold levels for bacterial species delineation. Based on genomic, chemotaxonomic and morphological analyses, we propose five novel species with the names sp. nov. (type strain BG-AF3-A=DSM 110574=LMG 31633), sp. nov. (type strain WF-MT5-A=DSM 110569=LMG 31629), sp. nov. (type strain Lr3000=DSM 110573=LMG 31632), sp. nov. (type strain STM3_1=DSM 110572=LMG 31631) and sp. nov. (type strain WF-MO7-1=DSM 110576=LMG 31630). Core genome phylogeny and experimental evidence of host adaptation of strains of further provide a strong rationale to consider a number of distinct lineages within this species as subspecies. Here we propose six subspecies of : subsp. subsp. nov. (type strain AP3=DSM 110703=LMG 31724), subsp. subsp. nov. (type strain 3c6=DSM 110571=LMG 31635), subsp. subsp. nov. (type strain lpuph1=DSM 110570=LMG 31634), subsp. subsp. nov. (type strain F 275=DSM 20016=ATCC 23272), subsp. subsp. nov. (type strain 1063=ATCC 53608=LMG 31752) and subsp. subsp. nov. (type strain 100-23=DSM 17509=CIP 109821).

Funding
This study was supported by the:
  • MichaelG. Gänzle , Canada Research Chairs Program
  • FuyongLi , Alberta Innovates Postgraduate Fellowship
  • JensWalter , Irish Government's National Development Plan (Science Foundation Ireland)
  • JensWalter , Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant
  • JensWalter , Campus Alberta Innovates Program (CAIP)
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004644
2021-02-03
2021-02-26
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/10.1099/ijsem.0.004644/ijsem004644.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004644&mimeType=html&fmt=ahah

References

  1. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature 2011; 474: 327 336 [CrossRef] [PubMed]
    [Google Scholar]
  2. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010; 464: 59 65 [CrossRef] [PubMed]
    [Google Scholar]
  3. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009; 9: 313 323 [CrossRef] [PubMed]
    [Google Scholar]
  4. Zheng J, Wittouck S, Salvetti E, Franz CMAP, Harris HMB et al. A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae . Int J Syst Evol Microbiol 2020; 70: 2782 2858 [CrossRef] [PubMed]
    [Google Scholar]
  5. Duar RM, Frese SA, Lin XB, Fernando SC, Burkey TE et al. Experimental evaluation of host adaptation of Lactobacillus reuteri to different vertebrate species. Appl Environ Microbiol 2017; 83: e00132 17 [CrossRef] [PubMed]
    [Google Scholar]
  6. Frese SA, Benson AK, Tannock GW, Loach DM, Kim J et al. The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri . PLoS Genet 2011; 7: e1001314 [CrossRef] [PubMed]
    [Google Scholar]
  7. Oh PL, Benson AK, Peterson DA, Patil PB, Moriyama EN et al. Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. Isme J 2010; 4: 377 387 [CrossRef] [PubMed]
    [Google Scholar]
  8. Walter J, Britton RA, Roos S. Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc Natl Acad Sci U S A 2011; 108 Suppl 1: 4645 4652 [CrossRef] [PubMed]
    [Google Scholar]
  9. Duar RM, Lin XB, Zheng J, Martino ME, Grenier T et al. Lifestyles in transition: evolution and natural history of the genus Lactobacillus. FEMS Microbiol Rev 2017; 41: S27 S48 [CrossRef] [PubMed]
    [Google Scholar]
  10. Zheng J, Ruan L, Sun M, Ganzle M. A genomic view of Lactobacilli and Pediococci demonstrates that phylogeny matches ecology and physiology. Appl Environ Microbiol 2015; 81: 7233 7243 [CrossRef] [PubMed]
    [Google Scholar]
  11. Frese SA, Mackenzie DA, Peterson DA, Schmaltz R, Fangman T et al. Molecular characterization of host-specific biofilm formation in a vertebrate gut symbiont. PLoS Genet 2013; 9: e1004057 [CrossRef] [PubMed]
    [Google Scholar]
  12. Krumbeck JA, Marsteller NL, Frese SA, Peterson DA, Ramer-Tait AE et al. Characterization of the ecological role of genes mediating acid resistance in Lactobacillus reuteri during colonization of the gastrointestinal tract. Environ Microbiol 2016; 18: 2172 2184 [CrossRef] [PubMed]
    [Google Scholar]
  13. Lin XB, Wang T, Stothard P, Corander J, Wang J et al. The evolution of ecological facilitation within mixed-species biofilms in the mouse gastrointestinal tract. Isme J 2018; 12: 2770 2784 [CrossRef] [PubMed]
    [Google Scholar]
  14. Walter J, Chagnaud P, Tannock GW, Loach DM, Dal Bello F et al. A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl Environ Microbiol 2005; 71: 979 986 [CrossRef] [PubMed]
    [Google Scholar]
  15. Walter J, Loach DM, Alqumber M, Rockel C, Hermann C et al. D-alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100-23 results in impaired colonization of the mouse gastrointestinal tract. Environ Microbiol 2007; 9: 1750 1760 [CrossRef] [PubMed]
    [Google Scholar]
  16. Cheng CC, Duar RM, Lin X, Perez-Munoz ME, Tollenaar S et al. Ecological importance of cross-feeding of the intermediate metabolite 1,2-propanediol between bacterial gut symbionts. Appl Environ Microbiol 2020; 86: e00190 20 [CrossRef] [PubMed]
    [Google Scholar]
  17. Ganzle MG, Zheng J. Lifestyles of sourdough lactobacilli - Do they matter for microbial ecology and bread quality?. Int J Food Microbiol 2019; 302: 15 23 [CrossRef] [PubMed]
    [Google Scholar]
  18. Zheng J, Zhao X, Lin XB, Ganzle M. Comparative genomics Lactobacillus reuteri from sourdough reveals adaptation of an intestinal symbiont to food fermentations. Sci Rep 2015; 5: 18234 [CrossRef] [PubMed]
    [Google Scholar]
  19. Kim M, Oh H-S, Park S-C, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64: 346 351 [CrossRef] [PubMed]
    [Google Scholar]
  20. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57: 81 91 [CrossRef] [PubMed]
    [Google Scholar]
  21. Richter M, Rossello-Mora R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106: 19126 19131 [CrossRef] [PubMed]
    [Google Scholar]
  22. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14: 60 [CrossRef] [PubMed]
    [Google Scholar]
  23. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68: 461 466 [CrossRef] [PubMed]
    [Google Scholar]
  24. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 2014; 30: 2114 2120 [CrossRef] [PubMed]
    [Google Scholar]
  25. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ et al. ABySS: a parallel assembler for short read sequence data. Genome Res 2009; 19: 1117 1123 [CrossRef] [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 [CrossRef] [PubMed]
    [Google Scholar]
  27. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215: 403 410 [CrossRef] [PubMed]
    [Google Scholar]
  28. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32: 1792 1797 [CrossRef] [PubMed]
    [Google Scholar]
  29. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30: 1312 1313 [CrossRef] [PubMed]
    [Google Scholar]
  30. Chen IA, Chu K, Palaniappan K, Pillay M, Ratner A et al. IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res 2019; 47: D666 D677 [CrossRef] [PubMed]
    [Google Scholar]
  31. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30: 2068 2069 [CrossRef] [PubMed]
    [Google Scholar]
  32. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31: 3691 3693 [CrossRef] [PubMed]
    [Google Scholar]
  33. Richter M, Rossello-Mora R, Oliver Glockner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32: 929 931 [CrossRef] [PubMed]
    [Google Scholar]
  34. Spinler JK, Sontakke A, Hollister EB, Venable SF, Oh PL et al. From prediction to function using evolutionary genomics: human-specific ecotypes of Lactobacillus reuteri have diverse probiotic functions. Genome Biol Evol 2014; 6: 1772 1789 [CrossRef] [PubMed]
    [Google Scholar]
  35. Gregersen T. Rapid method for distinction of gram-negative from gram-positive bacteria. Eur J Appl Microbiol Biotechnol 1978; 5: 123 127 [CrossRef]
    [Google Scholar]
  36. Gerhardt P. American Society for M Manual of methods for general bacteriology. In Gerhardt Philipp, Murray RGE. (editors) Morphology American Society for Microbiology; 1981
    [Google Scholar]
  37. McFrederick QS, Vuong HQ, Rothman JA. Lactobacillus micheneri sp. nov., Lactobacillus timberlakei sp. nov. and Lactobacillus quenuiae sp. nov., lactic acid bacteria isolated from wild bees and flowers. Int J Syst Evol Microbiol 2018; 68: 1879 1884 [CrossRef] [PubMed]
    [Google Scholar]
  38. Schumann P. Peptidoglycan structure. In Rainey F, Oren A. (editors) Methods in Microbiology Academic Press; 2011 pp 101 129
    [Google Scholar]
  39. Lüthi-Peng Q, Dileme FB, Puhan Z. Effect of glucose on glycerol bioconversion by Lactobacillus reuteri . Appl Microbiol Biotechnol 2002; 59: 289 296 [CrossRef] [PubMed]
    [Google Scholar]
  40. Dishisha T, Pereyra LP, Pyo SH, Britton RA, Hatti-Kaul R. Flux analysis of the Lactobacillus reuteri propanediol-utilization pathway for production of 3-hydroxypropionaldehyde, 3-hydroxypropionic acid and 1,3-propanediol from glycerol. Microb Cell Fact 2014; 13: 76 [CrossRef] [PubMed]
    [Google Scholar]
  41. Roos S, Jonsson H. A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 2002; 148: 433 442 [CrossRef] [PubMed]
    [Google Scholar]
  42. MacKenzie DA, Tailford LE, Hemmings AM, Juge N. Crystal structure of a mucus-binding protein repeat reveals an unexpected functional immunoglobulin binding activity. J Biol Chem 2009; 284: 32444 32453 [CrossRef] [PubMed]
    [Google Scholar]
  43. Yu J, Zhao J, Song Y, Zhang J, Yu Z et al. Comparative genomics of the herbivore gut symbiont Lactobacillus reuteri reveals genetic diversity and lifestyle adaptation. Front Microbiol 2018; 9: 1151 [CrossRef] [PubMed]
    [Google Scholar]
  44. Morita H, Toh H, Fukuda S, Horikawa H, Oshima K et al. Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobalamin production. DNA Res 2008; 15: 151 161 [CrossRef] [PubMed]
    [Google Scholar]
  45. Kandler O, Stetter K-O, Köhl R, sp Lreuteri. Lactobacillus reuteri sp. nov., a new species of heterofermentative lactobacilli . Zentralbl Bakteriol Hyg Abt IOrig C 1980; 1: 264 269
    [Google Scholar]
  46. Wegmann U, MacKenzie DA, Zheng J, Goesmann A, Roos S et al. The pan-genome of Lactobacillus reuteri strains originating from the pig gastrointestinal tract. BMC Genomics 2015; 16: 1023 [CrossRef] [PubMed]
    [Google Scholar]
  47. Lee JY, Han GG, Choi J, Jin GD, Kang SK et al. Pan-genomic approaches in Lactobacillus reuteri as a porcine probiotic: investigation of host adaptation and antipathogenic activity. Microb Ecol 2017; 74: 709 721 [CrossRef] [PubMed]
    [Google Scholar]
  48. Hou C, Zeng X, Yang F, Liu H, Qiao S. Study and use of the probiotic Lactobacillus reuteri in pigs: a review. J Anim Sci Biotechnol 2015; 6: 14 [CrossRef] [PubMed]
    [Google Scholar]
  49. MacKenzie DA, Jeffers F, Parker ML, Vibert-Vallet A, Bongaerts RJ et al. Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillus reuteri . Microbiology 2010; 156: 3368 3378 [CrossRef] [PubMed]
    [Google Scholar]
  50. Axelsson L, Lindgren S. Characterization and DNA homology of Lactobacillus strains isolated from pig intestine. J Appl Bacteriol 1987; 62: 433 440 [CrossRef] [PubMed]
    [Google Scholar]
  51. Zhao X, Gänzle MG. Genetic and phenotypic analysis of carbohydrate metabolism and transport in Lactobacillus reuteri . Int J Food Microbiol 2018; 272: 12 21 [CrossRef] [PubMed]
    [Google Scholar]
  52. Gänzle MG, Vogel RF. Contribution of reutericyclin production to the stable persistence of Lactobacillus reuteri in an industrial sourdough fermentation. Int J Food Microbiol 2003; 80: 31 45 [CrossRef] [PubMed]
    [Google Scholar]
  53. Wesney E, Tannock GW. Association of rat, pig, and fowl biotypes of Lactobacilli with the stomach of gnotobiotic mice. Microb Ecol 1979; 5: 35 42 [CrossRef] [PubMed]
    [Google Scholar]
  54. Letunic I, Bork P. Interactive Tree of Life (iTOL) V4: recent updates and new developments. Nucleic Acids Res 2019; 47: W256 W259 [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004644
Loading
/content/journal/ijsem/10.1099/ijsem.0.004644
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error