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INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 71, Issue 2

sp. nov., sp. nov., sp. nov., sp. nov. and sp. nov., five novel species isolated from the vertebrate gastrointestinal tract, and proposal of six subspecies of adapted to the gastrointestinal tract of specific vertebrate hosts Open Access

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).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): evolution , host adaptation , Limosilactobacillus reuteri subspecies , novel Limosilactobacillus species and phylogenetic lineages
Funding
This study was supported by the:
  • Canada Research Chairs Program
    • Principle Award Recipient: MichaelG. Gänzle
  • Alberta Innovates Postgraduate Fellowship
    • Principle Award Recipient: FuyongLi
  • Irish Government's National Development Plan (Science Foundation Ireland)
    • Principle Award Recipient: JensWalter
  • Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant
    • Principle Award Recipient: JensWalter
  • Campus Alberta Innovates Program (CAIP)
    • Principle Award Recipient: JensWalter
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2021-02-03
2024-04-24
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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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
  24. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][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 [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. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article][PubMed]
     [Google Scholar]
  28. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
  31. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article]
     [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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
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Limosilactobacillus balticus sp. nov., Limosilactobacillus agrestis sp. nov., Limosilactobacillus albertensis sp. nov., Limosilactobacillus rudii sp. nov. and Limosilactobacillus fastidiosus sp. nov., five novel Limosilactobacillus species isolated from the vertebrate gastrointestinal tract, and proposal of six subspecies of Limosilactobacillus reuteri adapted to the gastrointestinal tract of specific vertebrate hosts
Int J Syst Evol Microbiol 71, 004644 (2021); https://doi.org/10.1099/ijsem.0.004644
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