Antonie van Leeuwenhoek

, Volume 110, Issue 6, pp 737–750 | Cite as

Inediibacterium massiliense gen. nov., sp. nov., a new bacterial species isolated from the gut microbiota of a severely malnourished infant

  • Maryam Tidjani Alou
  • Jaishriram Rathored
  • Caroline Michelle
  • Gregory Dubourg
  • Claudia Andrieu
  • Nicholas Armstrong
  • Cheikh Sokhna
  • Aldiouma Diallo
  • Didier Raoult
  • Pierre-Edouard Fournier
Original Article

Abstract

A novel strain, Mt12T (=CSUR P1907 = DSM 100590), was isolated from the fecal sample of a 7-month-old girl from Senegal afflicted with severe acute malnutrition. This bacterium is a strictly anaerobic, spore-forming Gram-stain positive bacillus. The major cellular fatty acid was identified as tetradecanoic acid. Its 16S rRNA gene sequence exhibited 94.9% similarity with that of Crassaminicella profunda strain Ra1766HT, currently the closest species with a validly published name. The draft genome of strain Mt12T is 3,497,275-bp long with a 30.45% of G+C content. 3397 genes were predicted, including 3268 protein-coding genes and 129 RNAs, including eight 16S rRNAs. Genomic comparison with closely related species with an available genome showed a lower quantitative genomic content. The phylogenetic analysis alongside the dDDH values under 30% and phenotypic characteristics suggest that strain Mt12T represents a new genus within the family Clostridiaceae, for which the name Inediibacterium massiliense gen. nov., sp. nov. is proposed.

Keywords

Inediibacterium massiliense Gut microbiota Taxonogenomics Culturomics Genome 

Abbreviations

AGIOS

Average of genomic identity of orthologous gene sequences

bp

Base pairs

COG

Clusters of orthologous groups

CSUR

Collection de souches de l’Unité des Rickettsies

DDH

DNA–DNA hybridization

DSM

Deutsche Sammlung von Mikroorganismen

FAME

Fatty acid methyl ester

GC/MS

Gas chromatography/mass spectrometry

kb

Kilobases

MALDI-TOF MS

Matrix-assisted laser-desorption/ionization time-of-flight mass spectrometry

ORF

Open reading frame

TE buffer

Tris-EDTA buffer

SDS

Sodium dodecyl sulfate

URMITE

Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergent

Supplementary material

10482_2017_843_MOESM1_ESM.tif (4.2 mb)
Supplementary Fig. 1Gram staining of Inediibacterium massiliense strain Mt12T (TIFF 4273 kb)
10482_2017_843_MOESM2_ESM.docx (12 kb)
Supplementary Table 1 (DOCX 12 kb)

References

  1. Alain K, Pignet P, Zbinden M, Quillevere M, Duchiron F, Donval JP, Lesongeur F, Raguenes G, Crassous P, Querellou J, Cambon-Bonavita MA (2002) Caminicella sporogenes gen. nov., sp. nov., a novel thermophilic spore-forming bacterium isolated from an East-Pacific Rise hydrothermal vent. Int J Syst Evol Microbiol 52:1621–1628PubMedGoogle Scholar
  2. Auch AF, von Jan M, Klenk H-P, Göker M (2010) Digital DNA–DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genom Sci 2:117–134CrossRefGoogle Scholar
  3. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genom 9:75CrossRefGoogle Scholar
  4. Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, Sayers EW (2012) GenBank. Nucleic Acids Res 40:D48–D53CrossRefPubMedGoogle Scholar
  5. Brisbarre N, Fardeau ML, Cueff V, Cayol JL, Barbier G, Cilia V, Ravot G, Thomas P, Garcia JL, Ollivier B (2003) Clostridium caminithermale sp. nov., a slightly halophilic and moderately thermophilic bacterium isolated from an Atlantic deep-sea hydrothermal chimney. Int J Syst Evol Microbiol 53:1043–1049CrossRefPubMedGoogle Scholar
  6. Buck JD (1982) Nonstaining (KOH) method for determination of gram reactions of marine bacteria. Appl Environ Microbiol 44:992–993PubMedPubMedCentralGoogle Scholar
  7. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J (2009) DNAPlotter: circular and linear interactive genome visualization. Bioinformatics (Oxf Engl) 25:119–120CrossRefGoogle Scholar
  8. Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J, Garcia P, Cai J, Hippe H, Farrow JAE (1994) The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44:812–826CrossRefPubMedGoogle Scholar
  9. Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dione N, Sankar SA, Lagier JC, Khelaifia S, Michele C, Armstrong N, Richez M, Abrahão J, Raoult D, Fournier PE (2016) Genome sequence and description of Anaerosalibacter massiliensis sp. nov. New Microbes New Infect 10:66–76CrossRefPubMedPubMedCentralGoogle Scholar
  11. Drancourt M, Bollet C, Carlioz A, Martelin R, Gayral JP, Raoult D (2000) 16S ribosomal DNA sequence analysis of a large collection of environmental and clinical unidentifiable bacterial isolates. J Clin Microbiol 38:3623–3630PubMedPubMedCentralGoogle Scholar
  12. Fendrich C, Hippe H, Gottschalk G (1990) Clostridium halophilium sp. nov. and C. litorale sp. nov., an obligate halophilic and a marine species degrading betaine in the Stickland reaction. Arch Microbiol 154:127–132CrossRefGoogle Scholar
  13. Fournier P-E, Lagier J-C, Dubourg G, Raoult D (2015) From culturomics to taxonomogenomics: a need to change the taxonomy of prokaryotes in clinical microbiology. Anaerobe 36:73–78CrossRefPubMedGoogle Scholar
  14. Gouret P, Vitiello V, Balandraud N, Gilles A, Pontarotti P, Danchin EG (2005) FIGENIX: intelligent automation of genomic annotation: expertise integration in a new software platform. BMC Bioinform 6:198CrossRefGoogle Scholar
  15. Gouret P, Thompson JD, Pontarotti P (2009) PhyloPattern: regular expressions to identify complex patterns in phylogenetic trees. BMC Bioinform 10:298CrossRefGoogle Scholar
  16. Gouret P, Paganini J, Dainat J, Louati D, Darbo E, Pontarotti P, Levasseur A (2011) Integration of evolutionary biology concepts for functional annotation and automation of complex research in evolution: the multi-agent software system DAGOBAH. In: Pontarotti P (ed) Evolutionary biology—concepts, biodiversity, macroevolution and genome evolution. Springer, Berlin, pp 71–87CrossRefGoogle Scholar
  17. Graf D, Di Cagno R, Fåk F, Flint HJ, Nyman M, Saarela M, Watzl B (2015) Contribution of diet to the composition of the human gut microbiota. Microb Ecol Health Dis 26:26164PubMedGoogle Scholar
  18. Hong H, Kim SJ, Min UG, Lee YJ, Kim SG, Roh SW, Kim JG, Na JG, Rhee SK (2015) Anaerosolibacter carboniphilus gen. nov., sp. nov., a strictly anaerobic iron-reducing bacterium isolated from coal-contaminated soil. Int J Syst Evol Microbiol 65:1480–1485CrossRefPubMedGoogle Scholar
  19. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform 11:119CrossRefGoogle Scholar
  20. Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D (2015) Role of the normal gut microbiota. World J Gastroenterol 21:8787–8803CrossRefPubMedPubMedCentralGoogle Scholar
  21. Johnson MJ, Thatcher E, Cox ME (1995) Techniques for controlling variability in gram staining of obligate anaerobes. J Clin Microbiol 33:755–758PubMedPubMedCentralGoogle Scholar
  22. Käll L, Krogh A, Sonnhammer ELL (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338:1027–1036CrossRefPubMedGoogle Scholar
  23. Kim M, Oh H-S, Park S-C, 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 64:346–351CrossRefPubMedGoogle Scholar
  24. Klouche N, Fardeau ML, Lascourrèges JF, Cayol JL, Hacene H, Thomas P, Magot M (2007) Geosporobacter subterraneus gen. nov., sp. nov., a spore-forming bacterium isolated from a deep subsurface aquifer. Int J Syst Evol Microbiol 57:1757–1761CrossRefPubMedGoogle Scholar
  25. Lagesen K, Hallin P, Rødland EA, Staerfeldt HH, Rognes T, Ussery DW (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lagier JC, Armougom F, Million M, Hugon P, Pagnier I, Robert C, Bittar F, Fournous G, Gimenez G, Maraninchi M, Trape JF, Koonin EV, La Scola B, Raoult D (2012a) Microbial culturomics: paradigm shift in the human gut microbiome study. Clin Microbiol Infect 18:1185–1193CrossRefPubMedGoogle Scholar
  27. Lagier JC, Million M, Hugon P, Armougom F, Raoult D (2012b) Human gut microbiota: repertoire and variations. Front Cell Infect Microbiol 2:136CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lagier JC, Hugon P, Khelaifia S, Fournier PE, La Scola B, Raoult D (2015) The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clin Microbiol Rev 28:237–264CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lakhal R, Pradel N, Postec A, Ollivier B, Cayol J-L, Godfroy A, Fardeau M-L, Galès G (2015) Crassaminicella profunda gen. nov., sp. nov., an anaerobic marine bacterium isolated from deep-sea sediments. Int J Syst Evol Microbiol 65:3097–3102CrossRefPubMedGoogle Scholar
  30. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964CrossRefPubMedPubMedCentralGoogle Scholar
  31. Matuschek E, Brown DFJ, Kahlmeter G (2014) Development of the EUCAST disk diffusion antimicrobial susceptibility testing method and its implementation in routine microbiology laboratories. Clin Microbiol Infect 20:O255–O266CrossRefPubMedGoogle Scholar
  32. 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 14:60CrossRefGoogle Scholar
  33. Million M, Diallo A, Raoult D (2016) Gut microbiota and malnutrition. Microb Pathog. doi:10.1016/j.micpath.2016.02.003 Google Scholar
  34. Ogg CD, Patel BKC (2009) Thermotalea metallivorans gen. nov., sp. nov., a thermophilic, anaerobic bacterium from the Great Artesian Basin of Australia aquifer. Int J Syst Evol Microbiol 59:964–971CrossRefPubMedGoogle Scholar
  35. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5:e177CrossRefPubMedPubMedCentralGoogle Scholar
  36. Parte AC (2014) LPSN—list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42:D613–D616CrossRefPubMedGoogle Scholar
  37. Ramasamy D, Mishra AK, Lagier JC, Padhmanabhan R, Rossi M, Sentausa E, Raoult D, Fournier PE (2014) A polyphasic strategy incorporating genomic data for the taxonomic description of novel bacterial species. Int J Syst Evol Microbiol 64:384–391CrossRefPubMedGoogle Scholar
  38. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics (Oxf Engl) 16:944–945CrossRefGoogle Scholar
  39. Sankar SA, Lagier JC, Pontarotti P, Raoult D, Fournier PE (2015) The human gut microbiome, a taxonomic conundrum. Syst Appl Microbiol 38:276–286CrossRefPubMedGoogle Scholar
  40. Sasser M (2006) Bacterial identification by gas chromatographic analysis of fatty acids methyl esters (GC-FAME). Microbial ID Inc., NewarkGoogle Scholar
  41. Seng P, Drancourt M, Gouriet F, La Scola B, Fournier PE, Rolain JM, Raoult D (2009) Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clin Infect Dis 49:543–551CrossRefPubMedGoogle Scholar
  42. Seng P, Abat C, Rolain JM, Colson P, Lagier JC, Gouriet F, Fournier PE, Drancourt M, La Scola B, Raoult D (2013) Identification of rare pathogenic bacteria in a clinical microbiology laboratory: impact of matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol 51:2182–2194CrossRefPubMedPubMedCentralGoogle Scholar
  43. Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152Google Scholar
  44. Tan HQ, Wu XY, Zhang XQ, Wu M, Zhu XF (2012) Tepidibacter mesophilus sp. nov., a mesophilic fermentative anaerobe isolated from soil polluted by crude oil, and emended description of the genus Tepidibacter. Int J Syst Evol Microbiol 62:66–70CrossRefPubMedGoogle Scholar
  45. Tidjani Alou M, Lagier J-C, Raoult D (2016) Diet influence on the gut microbiota and dysbiosis related to nutritional disorders. Hum Microbiome J 1:3–11CrossRefGoogle Scholar
  46. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer K-H, Whitman WB, Euzéby J, Amann R, Rosselló-Móra R (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645CrossRefPubMedGoogle Scholar
  47. Zhang YZ, Fang MX, Zhang WW, Li TT, Wu M, Zhu XF (2013) Salimesophilobacter vulgaris gen. nov., sp. nov., an anaerobic bacterium isolated from paper-mill wastewater. Int J Syst Evol Microbiol 63:1317–1322CrossRefPubMedGoogle Scholar
  48. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39:W347–W352CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Maryam Tidjani Alou
    • 1
  • Jaishriram Rathored
    • 1
  • Caroline Michelle
    • 1
  • Gregory Dubourg
    • 1
  • Claudia Andrieu
    • 1
  • Nicholas Armstrong
    • 1
  • Cheikh Sokhna
    • 2
    • 3
  • Aldiouma Diallo
    • 2
    • 3
  • Didier Raoult
    • 1
    • 4
  • Pierre-Edouard Fournier
    • 1
  1. 1.URMITE, Aix Marseille Université, UM63, CNRS 7278, IRD 198, INSERM 1095, IHU - Méditerranée InfectionMarseilleFrance
  2. 2.Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes IRD 198, CNRS 7278, Aix-Marseille UniversitéMarseilleFrance
  3. 3.Campus Commun UCAD-IRD of HannDakarSenegal
  4. 4.Special Infectious Agents Unit, King Fahd Medical Research CenterKing Abdulaziz UniversityJeddahSaudi Arabia

Personalised recommendations