Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Article
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Article 31 May 2018

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

References

  • 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 52:1621–1628

    CAS  PubMed  Google Scholar 

  • 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 2:117–134

    Article  Google Scholar 

  • 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 9:75

    Article  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, Sayers EW (2012) GenBank. Nucleic Acids Res 40:D48–D53

    Article  CAS  PubMed  Google Scholar 

  • 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 53:1043–1049

    Article  CAS  PubMed  Google Scholar 

  • Buck JD (1982) Nonstaining (KOH) method for determination of gram reactions of marine bacteria. Appl Environ Microbiol 44:992–993

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J (2009) DNAPlotter: circular and linear interactive genome visualization. Bioinformatics (Oxf Engl) 25:119–120

    Article  CAS  Google Scholar 

  • 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 44:812–826

    Article  CAS  PubMed  Google Scholar 

  • Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 10:66–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 38:3623–3630

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 154:127–132

    Article  CAS  Google Scholar 

  • 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 36:73–78

    Article  PubMed  Google Scholar 

  • 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 6:198

    Article  Google Scholar 

  • Gouret P, Thompson JD, Pontarotti P (2009) PhyloPattern: regular expressions to identify complex patterns in phylogenetic trees. BMC Bioinform 10:298

    Article  Google Scholar 

  • 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 71–87

    Chapter  Google Scholar 

  • 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 26:26164

    PubMed  Google Scholar 

  • 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 65:1480–1485

    Article  CAS  PubMed  Google Scholar 

  • Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform 11:119

    Article  Google Scholar 

  • Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D (2015) Role of the normal gut microbiota. World J Gastroenterol 21:8787–8803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson MJ, Thatcher E, Cox ME (1995) Techniques for controlling variability in gram staining of obligate anaerobes. J Clin Microbiol 33:755–758

    CAS  PubMed  PubMed Central  Google Scholar 

  • Käll L, Krogh A, Sonnhammer ELL (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338:1027–1036

    Article  PubMed  Google Scholar 

  • 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 64:346–351

    Article  CAS  PubMed  Google Scholar 

  • 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 57:1757–1761

    Article  PubMed  Google Scholar 

  • 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 35:3100–3108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 18:1185–1193

    Article  CAS  PubMed  Google Scholar 

  • Lagier JC, Million M, Hugon P, Armougom F, Raoult D (2012b) Human gut microbiota: repertoire and variations. Front Cell Infect Microbiol 2:136

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 28:237–264

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 65:3097–3102

    Article  CAS  PubMed  Google Scholar 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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–O266

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Million M, Diallo A, Raoult D (2016) Gut microbiota and malnutrition. Microb Pathog. doi:10.1016/j.micpath.2016.02.003

    Google Scholar 

  • 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 59:964–971

    Article  CAS  PubMed  Google Scholar 

  • Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5:e177

    Article  PubMed  PubMed Central  Google Scholar 

  • Parte AC (2014) LPSN—list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42:D613–D616

    Article  CAS  PubMed  Google Scholar 

  • 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 64:384–391

    Article  PubMed  Google Scholar 

  • Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics (Oxf Engl) 16:944–945

    Article  CAS  Google Scholar 

  • Sankar SA, Lagier JC, Pontarotti P, Raoult D, Fournier PE (2015) The human gut microbiome, a taxonomic conundrum. Syst Appl Microbiol 38:276–286

    Article  CAS  PubMed  Google Scholar 

  • Sasser M (2006) Bacterial identification by gas chromatographic analysis of fatty acids methyl esters (GC-FAME). Microbial ID Inc., Newark

    Google Scholar 

  • 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 49:543–551

    Article  CAS  PubMed  Google Scholar 

  • 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 51:2182–2194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152

    Google Scholar 

  • 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 62:66–70

    Article  CAS  PubMed  Google Scholar 

  • Tidjani Alou M, Lagier J-C, Raoult D (2016) Diet influence on the gut microbiota and dysbiosis related to nutritional disorders. Hum Microbiome J 1:3–11

    Article  Google Scholar 

  • 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 12:635–645

    Article  CAS  PubMed  Google Scholar 

  • 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 63:1317–1322

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39:W347–W352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank the Xegen Company (www.xegen.fr) for automating the genomic annotation process. This study was funded by the “Fondation Méditerranée Infection”. We thank TradOnline for English reviewing.

Author information

Authors and Affiliations

  1. URMITE, Aix Marseille Université, UM63, CNRS 7278, IRD 198, INSERM 1095, IHU - Méditerranée Infection, 19-21 Boulevard Jean Moulin, 13005, Marseille, France

    Maryam Tidjani Alou, Jaishriram Rathored, Caroline Michelle, Gregory Dubourg, Claudia Andrieu, Nicholas Armstrong, Didier Raoult & Pierre-Edouard Fournier

  2. Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes IRD 198, CNRS 7278, Aix-Marseille Université, Marseille, France

    Cheikh Sokhna & Aldiouma Diallo

  3. Campus Commun UCAD-IRD of Hann, Route des pères Maristes, Hann Maristes, BP 1386, CP 18524, Dakar, Senegal

    Cheikh Sokhna & Aldiouma Diallo

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

    Didier Raoult

Authors
  1. Maryam Tidjani Alou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jaishriram Rathored
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Caroline Michelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gregory Dubourg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Claudia Andrieu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nicholas Armstrong
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cheikh Sokhna
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Aldiouma Diallo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Didier Raoult
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Pierre-Edouard Fournier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pierre-Edouard Fournier.

Ethics declarations

Compliance with ethical standards

See Methods

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

Gram staining of Inediibacterium massiliense strain Mt12T (TIFF 4273 kb)

Supplementary Table 1 (DOCX 12 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alou, M.T., Rathored, J., Michelle, C. et al. Inediibacterium massiliense gen. nov., sp. nov., a new bacterial species isolated from the gut microbiota of a severely malnourished infant. Antonie van Leeuwenhoek 110, 737–750 (2017). https://doi.org/10.1007/s10482-017-0843-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-017-0843-5

Keywords

Search

Navigation