1887

Abstract

The human gastrointestinal tract is inhabited by various microorganisms, including thousands of bacterial taxa that have yet to be cultured and characterized. In this report, we describe the isolation, cultivation, genotypic and phenotypic characterization and taxonomy of five novel anaerobic bacterial strains that were recovered during the massive cultivation and isolation of gut microbes from human faecal samples. On the basis of the polyphasic taxonomic results, we propose two novel genera and five novel species. They are sp. nov. (type strain NSJ-142=CGMCC 1.17903=KCTC 25346), sp. nov. (type strain NSJ-176=CGMCC 1.17933=KCTC 25355), gen. nov. sp. nov. (type strain NSJ-141=CGMCC 1.17902=KCTC 25345), gen. nov. sp. nov. (type strain NSJ-153=CGMCC 1.17915=KCTC 25350) and sp. nov. (type strain NSJ-152=CGMCC 1.17914=KCTC 25349).

Funding
This study was supported by the:
  • the Strategic Priority Research Program of Chinese Academy of Sciences (Award Grant No. XDB38020300)
    • Principle Award Recipient: Shuang-JiangLiu
  • National Key Research and Development Program of China (Award No.2019YFA0905601)
    • Principle Award Recipient: Shuang-JiangLiu
  • 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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2023-02-03
2024-05-07
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References

  1. Lloyd-Price J, Abu-Ali G, Huttenhower C. The healthy human microbiome. Genome Med 2016; 8:51 [View Article]
    [Google Scholar]
  2. Rajilić-Stojanović M, Heilig HGHJ, Tims S, Zoetendal EG, de Vos WM. Long-term monitoring of the human intestinal microbiota composition. Environ Microbiol 2012 [View Article] [PubMed]
    [Google Scholar]
  3. 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]
  4. Qin J, Li Y, Cai Z, Li S, Zhu J et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012; 490:55–60 [View Article] [PubMed]
    [Google Scholar]
  5. Truong DT, Tett A, Pasolli E, Huttenhower C, Segata N. Microbial strain-level population structure and genetic diversity from metagenomes. Genome Res 2017; 27:626–638 [View Article] [PubMed]
    [Google Scholar]
  6. Wang W-L, Xu S-Y, Ren Z-G, Tao L, Jiang J-W et al. Application of metagenomics in the human gut microbiome. World J Gastroenterol 2015; 21:803–814 [View Article] [PubMed]
    [Google Scholar]
  7. Oren A, Garrity GM. Valid publication of the names of forty-two phyla of prokaryotes. Int J Syst Evol Microbiol 2021; 71:10 [View Article] [PubMed]
    [Google Scholar]
  8. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T et al. Enterotypes of the human gut microbiome. Nature 2011; 473:174–180 [View Article] [PubMed]
    [Google Scholar]
  9. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. The influence of diet on the gut microbiota. Pharmacol Res 2013; 69:52–60 [View Article] [PubMed]
    [Google Scholar]
  10. Rinninella E, Raoul P, Cintoni M, Franceschi F, Miggiano GAD et al. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms 2019; 7:E14 [View Article]
    [Google Scholar]
  11. Chen W, Liu F, Ling Z, Tong X, Xiang C. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One 2012; 7:e39743 [View Article]
    [Google Scholar]
  12. Wang Z, Lai Z, Zhang X, Huang P, Xie J et al. Altered gut microbiome compositions are associated with the severity of asthma. J Thorac Dis 2021; 13:4322–4338 [View Article]
    [Google Scholar]
  13. Aparicio M, Alba C, Cam Public Health Area P, Rodríguez JM, Fernández L. Microbiological and immunological markers in milk and infant feces for common gastrointestinal disorders: a pilot study. Nutrients 2020; 12:E634 [View Article]
    [Google Scholar]
  14. Sakamoto M, Ikeyama N, Toyoda A, Murakami T, Mori H et al. Coprobacter secundus subsp. similis subsp. nov. and Solibaculum mannosilyticum gen. nov., sp. nov., isolated from human feces. Microbiol Immunol 2021; 65:245–256 [View Article]
    [Google Scholar]
  15. Gaffney J, Embree J, Gilmore S, Embree M. Ruminococcus bovis sp. nov., a novel species of amylolytic Ruminococcus isolated from the rumen of a dairy cow. Int J Syst Evol Microbiol 2021; 71: [View Article] [PubMed]
    [Google Scholar]
  16. Parte AC. LPSN—list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 2014; 42:D613–6 [View Article]
    [Google Scholar]
  17. Vacca M, Celano G, Calabrese FM, Portincasa P, Gobbetti M et al. The controversial role of human gut Lachnospiraceae. Microorganisms 2020; 8:E573 [View Article]
    [Google Scholar]
  18. Meehan CJ, Beiko RG. A phylogenomic view of ecological specialization in the Lachnospiraceae, A family of digestive tract-associated bacteria. Genome Biol Evol 2014; 6:703–713 [View Article] [PubMed]
    [Google Scholar]
  19. Zhang J, Song L, Wang Y, Liu C, Zhang L et al. Beneficial effect of butyrate-producing Lachnospiraceae on stress-induced visceral hypersensitivity in rats. J Gastroenterol Hepatol 2019; 34:1368–1376 [View Article] [PubMed]
    [Google Scholar]
  20. Jumas-Bilak E, Carlier J-P, Jean-Pierre H, Mory F, Teyssier C et al. Acidaminococcus intestini sp. nov., isolated from human clinical samples. Int J Syst Evol Microbiol 2007; 57:2314–2319 [View Article]
    [Google Scholar]
  21. Rogosa M. Acidaminococcus gen. n., Acidaminococcus fermentans sp. n., anaerobic Gram-negative diplococci using amino acids as the sole energy source for growth. J Bacteriol 1969; 98:756–766 [View Article]
    [Google Scholar]
  22. Würdemann D, Tindall BJ, Pukall R, Lünsdorf H, Strömpl C et al. Gordonibacter pamelaeae gen. nov., sp. nov., a new member of the Coriobacteriaceae isolated from a patient with Crohn’s disease, and reclassification of Eggerthella hongkongensis Lau et al. 2006 as Paraeggerthella hongkongensis gen. nov., comb. nov. Int J Syst Evol Microbiol 2009; 59:1405–1415 [View Article]
    [Google Scholar]
  23. Lau SKP, Woo PCY, Woo GKS, Fung AMY, Wong MKM et al. Eggerthella hongkongensis sp. nov. and Eggerthella sinensis sp. nov., two novel Eggerthella species, account for half of the cases of Eggerthella bacteremia. Diagn Microbiol Infect Dis 2004; 49:255–263 [View Article]
    [Google Scholar]
  24. Ikeyama N, Toyoda A, Morohoshi S, Kunihiro T, Murakami T et al. Amedibacterium intestinale gen. nov., sp. nov., isolated from human faeces, and reclassification of Eubacterium dolichum Moore et al. 1976 (Approved Lists 1980) as Amedibacillus dolichus gen. nov., comb. nov. Int J Syst Evol Microbiol 2020; 70:3656–3664 [View Article]
    [Google Scholar]
  25. Ganguli LA, Turton LJ, Tillotson GS. Evaluation of fastidious anaerobe broth as a blood culture medium. J Clin Pathol 1982; 35:458–461 [View Article] [PubMed]
    [Google Scholar]
  26. Lopez-Siles M, Khan TM, Duncan SH, Harmsen HJM, Garcia-Gil LJ et al. Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrates for growth. Appl Environ Microbiol 2012; 78:420–428 [View Article]
    [Google Scholar]
  27. Liu C, Du M-X, Abuduaini R, Yu H-Y, Li D-H et al. Enlightening the taxonomy darkness of human gut microbiomes with a cultured biobank. Microbiome 2021; 9:119 [View Article]
    [Google Scholar]
  28. Wikins TD, Holdeman LV, Abramson IJ, Moore WE. Standardized single-disc method for antibiotic susceptibility testing of anaerobic bacteria. Antimicrob Agents Chemother 1972; 1:451–459 [View Article]
    [Google Scholar]
  29. Preston-Mafham J, Boddy L, Randerson PF. Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles – a critique. FEMS Microbiol Ecol 2002; 42:1–14 [View Article]
    [Google Scholar]
  30. Wang Y-J, Xu X-J, Zhou N, Sun Y, Liu C et al. Parabacteroides acidifaciens sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 2019; 69:761–766 [View Article]
    [Google Scholar]
  31. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article]
    [Google Scholar]
  32. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 1994; 22:4673–4680 [View Article]
    [Google Scholar]
  33. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article]
    [Google Scholar]
  34. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article] [PubMed]
    [Google Scholar]
  35. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  36. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
    [Google Scholar]
  37. Nei M. Phylogenetic inference: maximum parsimony methods. In Nei M, Kumar S. eds Molecular Evolution and Phylogenetics Oxford: Oxford University Press; 2000 pp 115–146
    [Google Scholar]
  38. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  39. 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]
  40. Na S-I, Kim YO, Yoon S-H, Ha S-M, Baek I et al. UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 2018; 56:280–285 [View Article]
    [Google Scholar]
  41. Lee I, Ouk Kim Y, Park SC, Chun J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article]
    [Google Scholar]
  42. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article]
    [Google Scholar]
  43. Kim D, Park S, Chun J. Introducing EzAAI: a pipeline for high throughput calculations of prokaryotic average amino acid identity. J Microbiol 2021; 59:476–480 [View Article] [PubMed]
    [Google Scholar]
  44. Ndongo S, Lagier JC, Fournier PE, Raoult D, Khelaifia S. Phocea massiliensis” a new bacterial species isolated from the human gut. New Microbes New Infect 2016; 13:67–68 [View Article]
    [Google Scholar]
  45. Parker CT, Tindall BJ, Garrity GM. International Code of Nomenclature of Prokaryotes. Prokaryotic code (2008 revision). Int J Syst Evol Microbiol 2019; 69:S1–S111
    [Google Scholar]
  46. Stackebrandt E. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 2006; 33:152–155
    [Google Scholar]
  47. 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]
    [Google Scholar]
  48. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article]
    [Google Scholar]
  49. Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196:2210–2215 [View Article] [PubMed]
    [Google Scholar]
  50. Luo C, Rodriguez-R LM, Konstantinidis KT. MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 2014; 42:e73 [View Article]
    [Google Scholar]
  51. Liu C, Du M-X, Abuduaini R, Yu H-Y, Li D-H et al. Enlightening the taxonomy darkness of human gut microbiomes with a cultured biobank. Microbiome 2021; 9:119 [View Article]
    [Google Scholar]
  52. Petzoldt D, Breves G, Rautenschlein S, Taras D. Harryflintia acetispora gen. nov., sp. nov., isolated from chicken caecum. Int J Syst Evol Microbiol 2016; 66:4099–4104 [View Article]
    [Google Scholar]
  53. Lawson PA, Song Y, Liu C, Molitoris DR, Vaisanen M-L et al. Anaerotruncus colihominis gen. nov., sp. nov., from human faeces. Int J Syst Evol Microbiol 2004; 54:413–417 [View Article]
    [Google Scholar]
  54. Chen S, Dong X. Acetanaerobacterium elongatum gen. nov., sp. nov., from paper mill waste water. Int J Syst Evol Microbiol 2004; 54:2257–2262 [View Article]
    [Google Scholar]
  55. Song L, Dong X. Hydrogenoanaerobacterium saccharovorans gen. nov., sp. nov., isolated from H2-producing UASB granules. Int J Syst Evol Microbiol 2009; 59:295–299 [View Article]
    [Google Scholar]
  56. Haas KN, Blanchard JL. Reclassification of the Clostridium clostridioforme and Clostridium sphenoides clades as Enterocloster gen. nov. and Lacrimispora gen. nov., including reclassification of 15 taxa. Int J Syst Evol Microbiol 2020; 70:23–34 [View Article]
    [Google Scholar]
  57. Broda DM, Saul DJ, Bell RG, Musgrave DR. Clostridium algidixylanolyticum sp. nov., a psychrotolerant, xylan-degrading, spore-forming bacterium. Int J Syst Evol Microbiol 2000; 50 Pt 2:623–631 [View Article]
    [Google Scholar]
  58. Mechichi T, Labat M, Patel BK, Woo TH, Thomas P et al. Clostridium methoxybenzovorans sp. nov., a new aromatic o-demethylating homoacetogen from an olive mill wastewater treatment digester. Int J Syst Bacteriol 1999; 49 Pt 3:1201–1209 [View Article] [PubMed]
    [Google Scholar]
  59. Palop ML, Valles S, Pinaga F, Flors A. Isolation and characterization of an anaerobic, cellulolytic bacterium, Clostridium celerecrescens sp. nov. Int J Syst Bacteriol 1989; 39:68–71 [View Article]
    [Google Scholar]
  60. Chamkha M, Garcia JL, Labat M. Metabolism of cinnamic acids by some Clostridiales and emendation of the descriptions of Clostridium aerotolerans, Clostridium celerecrescens and Clostridium xylanolyticum. Int J Syst Evol Microbiol 2001; 51:2105–2111 [View Article]
    [Google Scholar]
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