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Maliibacterium massiliense gen. nov. sp. nov., Isolated from Human Feces and Proposal of Maliibacteriaceae fam. nov.

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Abstract

Bacterial strain Marseille-P3954 was isolated from a stool sample of a 35-year-old male patient living in France. It was a gram-positive, rod-shaped anaerobic, non-motile, and non-spore-forming bacterium. C16:0 and C18:1n9 were the major fatty acid, while its genome measured 2,422,126 bp with 60.8 mol% of G+C content. Phylogenetic analysis based on the 16S rRNA gene sequence showed that strain Marseille-P3954 had 85.51% of similarity with Christensenella minuta, its closest related species with standing in nomenclature. As this value is very low compared to the recommended threshold, it suggested that the Marseille-P3954 strain belongs to a new bacterial genus, classified in a new family. On the basis of these genomic, phenotypic, and phylogenetic evidences, we propose that strain Marseille-P3954 should be classified as a new genus and species, Maliibacterium massiliense gen. nov., sp. nov. The type strain of M. massiliense sp. nov. is Marseille-P3954 (CSUR P3954 = CECT 9568).

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References

  1. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023. https://doi.org/10.1038/4441022a

    Article  CAS  PubMed  Google Scholar 

  2. Jandhyala SM, Talukdar R, Subramanyam C et al (2015) Role of the normal gut microbiota. World J Gastroenterol 21:8787–8803. https://doi.org/10.3748/wjg.v21.i29.8787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ni J, Wu GD, Albenberg L, Tomov VT (2017) Gut microbiota and IBD: causation or correlation? Nat Rev Gastroenterol Hepatol 14:573–584. https://doi.org/10.1038/nrgastro.2017.88

    Article  PubMed  PubMed Central  Google Scholar 

  4. Kim D, Zeng MY, Núñez G (2017) The interplay between host immune cells and gut microbiota in chronic inflammatory diseases. Exp Mol Med 49:e339. https://doi.org/10.1038/emm.2017.24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Goodrich JK, Waters JL, Poole AC et al (2014) Human genetics shape the gut microbiome. Cell 159:789–799. https://doi.org/10.1016/j.cell.2014.09.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Shivaji S (2017) We are not alone: a case for the human microbiome in extra intestinal diseases. Gut Pathog 9:13. https://doi.org/10.1186/s13099-017-0163-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Everard A, Belzer C, Geurts L et al (2013) Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA 110:9066–9071. https://doi.org/10.1073/pnas.1219451110

    Article  PubMed  PubMed Central  Google Scholar 

  8. Ashrafian F, Shahriary A, Behrouzi A et al (2019) Akkermansia muciniphila-derived extracellular vesicles as a mucosal delivery vector for amelioration of obesity in mice. Front Microbiol 10:2155. https://doi.org/10.3389/fmicb.2019.02155

    Article  PubMed  PubMed Central  Google Scholar 

  9. Schneeberger M, Everard A, Gómez-Valadés AG et al (2015) Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci Rep 5:16643. https://doi.org/10.1038/srep16643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Mailhe M, Ricaboni D, Vitton V et al (2018) Repertoire of the gut microbiota from stomach to colon using culturomics and next-generation sequencing. BMC Microbiol 18:157. https://doi.org/10.1186/s12866-018-1304-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Lagier JC, Khelaifia S, Alou MT et al (2016) Culture of previously uncultured members of the human gut microbiota by culturomics. Nat Microbiol 1:16203. https://doi.org/10.1038/nmicrobiol.2016.203

    Article  CAS  PubMed  Google Scholar 

  12. Burcelin R (2017) Microbiote intestinal et dialogue immunitaire au cours de la maladie métabolique. Biol Aujourdhui 211:1–18. https://doi.org/10.1051/jbio/2017008

    Article  CAS  PubMed  Google Scholar 

  13. Cani PD (2018) Human gut microbiome: hopes, threats and promises. Gut 67:1716–1725. https://doi.org/10.1136/gutjnl-2018-316723

    Article  CAS  PubMed  Google Scholar 

  14. Federico A, Dallio M, Di Sarno R et al (2017) Gut microbiota, obesity and metabolic disorders. Minerva Gastroenterol Dietol 63:337–344. https://doi.org/10.23736/S1121-421X.17.02376-5

    Article  PubMed  Google Scholar 

  15. Diakite A, Dubourg G, Dione N et al (2019) Extensive culturomics of 8 healthy samples enhances metagenomics efficiency. PLoS ONE 14:e0223543. https://doi.org/10.1371/journal.pone.0223543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Dubourg G, Lagier JC, Armougom F et al (2013) The gut microbiota of a patient with resistant tuberculosis is more comprehensively studied by culturomics than by metagenomics. Eur J Clin Microbiol Infect Dis 32:637–645. https://doi.org/10.1007/s10096-012-1787-3

    Article  CAS  PubMed  Google Scholar 

  17. Lagier JC, Dubourg G, Million M et al (2018) Culturing the human microbiota and culturomics. Nat Rev Microbiol 16:540–550. https://doi.org/10.1038/s41579-018-0041-0

    Article  CAS  PubMed  Google Scholar 

  18. Lagier JC, Hugon P, Khelaifia S et al (2015) The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clin Microbiol Rev 28:237–264. https://doi.org/10.1128/CMR.00014-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Dubourg G, Lagier JC, Robert C et al (2014) Culturomics and pyrosequencing evidence of the reduction in gut microbiota diversity in patients with broad-spectrum antibiotics. Int J Antimicrob Agents 44:117–124. https://doi.org/10.1016/j.ijantimicag.2014.04.020

    Article  CAS  PubMed  Google Scholar 

  20. Martellacci L, Quaranta G, Patini R et al (2019) A literature review of metagenomics and culturomics of the peri-implant microbiome: current evidence and future perspectives. Mater Basel Switz. https://doi.org/10.3390/ma12183010

    Article  Google Scholar 

  21. Fournier PE, Drancourt M (2015) New microbes new infections promotes modern prokaryotic taxonomy: a new section “TaxonoGenomics: new genomes of microorganisms in humans.” New Microbes New Infect 7:48–49. https://doi.org/10.1016/j.nmni.2015.06.001

    Article  PubMed  PubMed Central  Google Scholar 

  22. Lo CI, Fall B, Sambe-Ba B et al (2015) MALDI-TOF mass spectrometry: a powerful tool for clinical microbiology at Hôpital Principal de Dakar, Senegal (West Africa). PLoS ONE 10:e0145889. https://doi.org/10.1371/journal.pone.0145889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lo CI, Padhmanabhan R, Mediannikov O et al (2015) Genome sequence and description of Pantoea septica strain FF5. Stand Genomic Sci 10:103. https://doi.org/10.1186/s40793-015-0083-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Morel AS, Dubourg G, Prudent E et al (2015) Complementarity between targeted real-time specific PCR and conventional broad-range 16S rDNA PCR in the syndrome-driven diagnosis of infectious diseases. Eur J Clin Microbiol Infect Dis 34:561–570. https://doi.org/10.1007/s10096-014-2263-z

    Article  CAS  PubMed  Google Scholar 

  25. Sayers EW, Cavanaugh M, Clark K et al (2019) GenBank. Nucleic Acids Res 47:D94–D99. https://doi.org/10.1093/nar/gky989

    Article  CAS  PubMed  Google Scholar 

  26. Yarza P, Yilmaz P, Pruesse E et al (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645. https://doi.org/10.1038/nrmicro3330

    Article  CAS  PubMed  Google Scholar 

  27. Kim M, Oh HS, Park SC, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351. https://doi.org/10.1099/ijs.0.059774-0

    Article  PubMed  Google Scholar 

  28. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Belkacemi S, Bou Khalil J, Ominami Y et al (2019) Passive filtration, rapid scanning electron microscopy, and matrix-assisted laser desorption ionization-time of flight mass spectrometry for Treponema culture and identification from the oral cavity. J Clin Microbiol 57:e00517-e519. https://doi.org/10.1128/JCM.00517-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Dione N, Sankar SA, Lagier JC et al (2016) Genome sequence and description of Anaerosalibacter massiliensis sp. nov. New Microbes New Infect 10:66–76. https://doi.org/10.1016/j.nmni.2016.01.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Su G, Morris JH, Demchak B, Bader GD (2014) Biological network exploration with Cytoscape 3. Curr Protoc Bioinform. https://doi.org/10.1002/0471250953.bi0813s47

    Article  Google Scholar 

  33. Lee I, Ouk Kim Y, Park SC, Chun J (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103. https://doi.org/10.1099/ijsem.0.000760

    Article  CAS  PubMed  Google Scholar 

  34. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60. https://doi.org/10.1186/1471-2105-14-60

    Article  Google Scholar 

  35. Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol 9:678–687. https://doi.org/10.1093/oxfordjournals.molbev.a040752

    Article  CAS  PubMed  Google Scholar 

  36. Morotomi M, Nagai F, Watanabe Y (2012) Description of Christensenella minuta gen. nov., sp. nov., isolated from human faeces, which forms a distinct branch in the order Clostridiales, and proposal of Christensenellaceae fam. nov. Int J Syst Evol Microbiol 62:144–149. https://doi.org/10.1099/ijs.0.026989-0

    Article  CAS  PubMed  Google Scholar 

  37. Lau SKP, McNabb A, Woo GKS et al (2007) Catabacter hongkongensis gen. nov., sp. nov., isolated from blood cultures of patients from Hong Kong and Canada. J Clin Microbiol 45:395–401. https://doi.org/10.1128/JCM.01831-06

    Article  CAS  PubMed  Google Scholar 

  38. Bouanane-Darenfed A, Ben Hania W, Cayol JL et al (2015) Reclassification of Acetomicrobium faecale as Caldicoprobacter faecalis comb. nov. Int J Syst Evol Microbiol 65:3286–3288. https://doi.org/10.1099/ijsem.0.000409

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Amael Fadlane for culturing the strains, Aurelia Caputo for submitting the genomic sequence to GenBank, and Marion Giansy for improving the quality of English grammar.

Funding

This study was supported by the Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, the National Research Agency under the program « Investissements d’avenir», reference ANR-10-IAHU-03, the Région Provence-Alpes-Côte d’Azur and European funding FEDER PRIMI.

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Authors and Affiliations

  1. Aix Marseille University, IRD, AP-HM, MEPHII, Marseille, France

    Sory Ibrahima Traore, Guillaume Durand & Jean Christophe Lagier

  2. IHU-Méditerranée Infection, 19-21 Boulevard Jean Moulin, 13385, Marseille Cedex 05, France

    Sory Ibrahima Traore, Cheikh Ibrahima Lo, Maaloum Mossaab, Guillaume Durand, Jean Christophe Lagier, Didier Raoult, Pierre-Edouard Fournier & Florence Fenollar

  3. Aix Marseille University, IRD, AP-HM, SSA, VITROME, Marseille, France

    Cheikh Ibrahima Lo, Pierre-Edouard Fournier & Florence Fenollar

  4. Laboratory of Biology and Health, Faculty of Sciences Ben M’sik, Hassan II University, Casablanca, Morocco

    Maaloum Mossaab

  5. Special Infectious Agents Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia

    Didier Raoult

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  1. Sory Ibrahima Traore
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Contributions

Conceptualization, FF and DR; methodology, PEF, JCL and FF; validation, PEF, and FF; formal analysis, CIL, RS, GD, and MM; investigation, SIT; writing—original draft preparation, SIT and CIL; writing—review and editing, CIL; supervision, FF; funding acquisition, DR. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Florence Fenollar.

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Traore, S.I., Lo, C.I., Mossaab, M. et al. Maliibacterium massiliense gen. nov. sp. nov., Isolated from Human Feces and Proposal of Maliibacteriaceae fam. nov.. Curr Microbiol 80, 211 (2023). https://doi.org/10.1007/s00284-023-03301-4

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