Skip to main content

Risungbinella massiliensis sp. nov., a new member of Thermoactinomycetaceae isolated from human gut

Antonie van Leeuwenhoek volume 109, pages 773–784 (2016)Cite this article

Abstract

A novel filamentous bacterium, designated GD1T, was isolated from the gut microbiota of a 38-year-old male who suffered from a Coxiella burnetii vascular for which he received multiple a broad-spectrum antibiotic cocktail at the time of the stool collection. The strain was isolated as a part of culturomics study by cultivation on 5 % sheep blood agar in aerobic condition at 28 °C, after 14 days of incubation. Strain GD1T shows 16S rRNA gene sequence similarities of 98.01 % to the type strain of Risungbinella pyongyangensis. We describe here the features of this bacterium, together with the complete genome sequence and annotation. The G+C content of the genomic DNA was determined to be 40.1 mol %. The major fatty acids of strain GD1T were identified as iso-C15:0, iso-C17:0, anteiso-C15:0, iso-C14:0 and C16:0. The 3,440,191 bp long genome contains 3540 protein-coding and 67 RNA genes, including three rRNA genes. Strain GD1T (= DSM 46691 = CSUR P1082) sp. nov. is here classified as the type strain of a new species, Risungbinella massiliensis, within the family Thermoactinomycetaceae. To date, strain GD1T is the first member of the family Thermoactinomycetaceae isolated from human gut and the fourth from a human specimen.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Addou AN, Schumann P, Sproer C, Hacene H, Cayol JL, Fardeau ML (2012) Melghirimyces algeriensis gen. nov., sp. nov., a member of the family Thermoactinomycetaceae, isolated from a salt lake. Int J Syst Evol Microbiol 62:1491–1498

    CAS  Article  PubMed  Google Scholar 

  • Addou AN, Schumann P, Spröer C et al (2013) Melghirimyces thermohalophilus sp. nov., a thermoactinomycete isolated from an Algerian salt lake. Int J Syst Evol Microbiol 63:1717–1722

    CAS  Article  PubMed  Google Scholar 

  • Auch AF, von Jan M, Klenk HP, Göker M (2010) Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2(1):117–134

    Article  PubMed  PubMed Central  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Rapp BA, Wheeler DL (2000) GenBank. Nucleic Acids Res 28:15–18

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Buss SN, Cole JA, Hannett GE et al (2013) Hazenella coriacea gen. nov., sp. nov., isolated from clinical specimens. Int J Syst Evol Microbiol 63:4087–4093

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Chen JJ, Lin LB, Zhang LL, Zhang J, Tang SK, Wei YL, Li WJ (2012) Laceyella sediminis sp. nov., a thermophilic bacterium isolated from a hot spring. Int J Syst Evol Microbiol 62:38–42

    CAS  Article  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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Dubourg G, Lagier JC, Armougom F, Robert C, Audoly G, Papazian L, Raoult D (2013) High-level colonisation of the human gut by Verrucomicrobia following broad-spectrum antibiotic treatment. Int J Antimicrob Agents 41:149–155

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Gonzalez C, Gutierrez C, Ramirez C (1978) Halobacterium vallismortis sp. nov. An amylolytic and carbohydrate-metabolizing, extremely halophilic bacterium. Can J Microbiol 24:710–715

    CAS  Article  PubMed  Google Scholar 

  • Han SI, Lee JC, Lee HJ, Whang KS (2013) Planifilum composti sp. nov., a thermophile isolated from compost. Int J Syst Evol Microbiol 63:4557–4561

    CAS  Article  PubMed  Google Scholar 

  • Hatayama K, Shoun H, Ueda Y, Nakamura A (2005) Planifilum fimeticola gen. nov., sp. nov. and Planifilum fulgidum sp. nov., novel members of the family ‘Thermoactinomycetaceae’ isolated from compost. Int J Syst Evol Microbiol 55:2101–2104

    CAS  Article  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 Bioinformatics 11:119

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(Pt 2):346–351

    CAS  Article  PubMed  Google Scholar 

  • Kim M, Kim T, Ri S et al (2015) Risungbinella pyongyangensis gen. nov., sp. nov., a mesophilic strain of the family Thermoactinomycetaceae isolated from agricultural soil sample. Int J Syst Evol Microbiol 65(8):2726–2733

    CAS  Article  PubMed  Google Scholar 

  • Lacey J (1971) Thermoactinomyces sacchari sp. nov., a thermophilicactinomycete causing bagassosis. J Gen Microbiol 66:327–338

    CAS  Article  PubMed  Google Scholar 

  • Lacey J, Cross T (1989) Genus Thermoactinomyces Tsiklinsky 1899, 501AL. In: Williams, Sharpe, Holt (eds) Bergey’s manual of systematic bacteriology, vol 4. Williams & Wilkins, Baltimore, pp 2574–2585

    Google Scholar 

  • Lagesen K, Hallin P, Rødland EA, Staerfeldt HH, Rognes TR, Ussery DW (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acid Res 35:3100–3108

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Lagier JC, Armougom F, Million M et al (2012) Microbial culturomics: paradigm shift in the human gut microbiome study. Clin Microbiol Infect 18:1185–1193

    CAS  Article  PubMed  Google Scholar 

  • Lagier JC, Hugon P, Khelaifia S, Fournier P-E, 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 

  • Lechner M, Findeiss S, Steiner L, Marz M, Stadler PF, Prohaska SJ (2011) Proteinortho: detection of (Co-) orthologs in large-scale analysis. BMC Bioinformatics 12:124

    Article  PubMed  PubMed Central  Google Scholar 

  • Li J, Zhang GT, Yang J et al (2012) Marininema mesophilum gen. nov., sp. nov., a thermoactinomycete isolated from deep sea sediment, and emended description of the family Thermoactinomycetaceae. Int J Syst Evol Microbiol 62:1383–1388

    CAS  Article  PubMed  Google Scholar 

  • Li J, Qin S, You ZQ, Long LJ, Tian XP, Wang FZ, Zhang S (2013) Melghirimyces profundicolus sp. nov., isolated from a deep-sea sediment. Int J Syst Evol Microbiol 63:4552–4556

    CAS  Article  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 25:0955–0964

    CAS  Article  Google Scholar 

  • Matsuo Y, Katsuta A, Matsuda S, Shizuri Y, Yokota A, Kasai H (2006) Mechercharimyces mesophilus gen. nov., sp. nov. and Mechercharimyces asporophorigenens sp. nov., antitumour substance-producing marine bacteria, and description of Thermoactinomycetaceae fam. nov. Int J Syst Evol Microbiol 56:2837–2842

    CAS  Article  PubMed  Google Scholar 

  • Meier-Kolthoff JP, Göker M, Spröer C, Klenk HP (2013a) When should a DDH experiment be mandatory in microbial taxonomy? Arch Microbiol 195(6):413–418

    CAS  Article  PubMed  Google Scholar 

  • Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013b) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60

    Article  PubMed  PubMed Central  Google Scholar 

  • Moore L, Moore E, Murray R, Stackebrandt E, Starr M (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464

    Article  Google Scholar 

  • Park DJ, Dastager SG, Lee JC, Yeo SH, Yoon JH, Kim CJ (2007) Shimazuella kribbensis gen. nov., sp. nov., a mesophilic representative of the family Thermoactinomycetaceae. Int J Syst Evol Microbiol 57:2660–2664

    CAS  Article  PubMed  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    CAS  Article  PubMed  Google Scholar 

  • Rosselló-Mora R (2006) DNA-DNA reassociation methods applied to microbial taxonomy and their critical evaluation. In: Stackebrandt E (ed) Molecular identification, systematics, and population structure of prokaryotes. Springer, Berlin, pp 23–50

    Chapter  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Sasser M (2006) Bacterial Identification by gas chromatographic analysis of fatty acids methyl esters (GC-FAME). Technical Note 101

  • Server T v. 2.0. http://www.cbs.dtu.dk/services/TMHMM/

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

    Google Scholar 

  • Tindall BJ, Rosselló-Mora R, Busse HJ, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266

    CAS  Article  PubMed  Google Scholar 

  • Tsubouchi T, Shimane Y, Mori K et al (2013) Polycladomyces abyssicola gen. nov., sp. nov., a thermophilic filamentous bacterium isolated from hemipelagic sediment. Int J Syst Evol Microbiol 63:1972–1981

    CAS  Article  PubMed  Google Scholar 

  • von Jan M, Riegger N, Pötter G et al (2011) Kroppenstedtia eburnea gen. nov., sp. nov., a thermoactinomycete isolated by environmental screening, and emended description of the family Thermoactinomycetaceae Matsuo et al. 2006 emend. Yassin et al. 2009. Int J Syst Evol Microbiol 61:2304–2310

    Article  Google Scholar 

  • Wu H, Liu B, Pan S (2015) Thermoactinomyces guangxiensis sp. nov., a thermophilic actinomycetes isolated from mushroom compost. Int J Syst Evol Microbiol 65(9):2859–2864

    CAS  Article  PubMed  Google Scholar 

  • Yang G, Qin D, Wu C, Yuan Y, Zhou S, Cai Y (2013) Kroppenstedtia guangzhouensis sp. nov., a thermoactinomycete isolated from soil. Int J Syst Evol Microbiol 63:4077–4080

    CAS  Article  PubMed  Google Scholar 

  • Yang G, Chen J, Zhou S (2015) Novibacillus thermophilus gen. nov., sp. nov., a Gram-staining-negative and moderately thermophilic species within the family Thermoactinomycetaceae. Int J Syst Evol Microbiol 65(8):2591–2597

    CAS  Article  PubMed  Google Scholar 

  • Yao S, Liu Y, Zhang M et al (2014) Thermoactinomyces daqus sp. nov., a thermophilic bacterium isolated from high-temperature Daqu. Int J Syst Evol Microbiol 64:206–210

    CAS  Article  PubMed  Google Scholar 

  • Yassin AF, Hupfer H, Klenk HP, Siering C (2009) Desmospora activa gen. nov., sp. nov., a thermoactinomycete isolated from sputum of a patient with suspected pulmonary tuberculosis, and emended description of the family Thermoactinomycetaceae Matsuo et al. 2006. Int J Syst Evol Microbiol 59:454–459

    CAS  Article  PubMed  Google Scholar 

  • Yoon JH, Kim IG, Shin YK, Park YH (2005) Proposal of the genus Thermoactinomyces sensu stricto and three new genera, Laceyella, Thermoflavimicrobium and Seinonella, on the basis of phenotypic, phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 55:395–400

    CAS  Article  PubMed  Google Scholar 

  • Yu TT, Zhang BH, Yao JC et al (2012) Lihuaxuella thermophila gen. nov., sp. nov., isolated from a geothermal soil sample in Tengchong, Yunnan, south-west China. Antonie Van Leeuwenhoek 102:711–718

    CAS  Article  PubMed  Google Scholar 

  • Zarparvar P, Amoozegar MA, Nikou MM, Schumann P, Ventosa A (2014) Salinithrix halophila gen. nov., sp. nov., a halophilic bacterium in the family Thermoactinomycetaceae. Int J Syst Evol Microbiol 64:4115–4119

    Article  PubMed  Google Scholar 

  • Zhang YX, Dong C, Biao S (2007) Planifilum yunnanense sp. nov., a thermophilic thermoactinomycete isolated from a hot spring. Int J Syst Evol Microbiol 57:1851–1854

    Article  PubMed  Google Scholar 

  • Zhang XM, He J, Zhang DF et al (2013) Marininema halotolerans sp. nov., a novel thermoactinomycete isolated from a sediment sample, and emended description of the genus Marininema Li et al. 2012. Int J Syst Evol Microbiol 63:4562–4567

    CAS  Article  PubMed  Google Scholar 

  • Zhang Y, Li J, Tian X, Zhang S (2015) Marinithermofilum abyssi gen. nov., sp. nov. and Desmospora profundinema sp. nov. isolated from a deep-sea sediment, and emended description of the genus Desmospora Yassin et al 2009. Int J Syst Evol Microbiol 65(8):2622–2629

    CAS  Article  PubMed  Google Scholar 

  • Zhou EM, Yu TT, Liu L et al (2014) Geothermomicrobium terrae gen. nov., sp. nov., a novel member of the family Thermoactinomycetaceae. Int J Syst Evol Microbiol 64:2998–3004

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the Xegen Company (www.xegen.fr) for automating the genomic annotation process. This study was funded by the Mediterranée-Infection Foundation.

Author information

Authors and Affiliations

  1. Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UM 63, CNRS 7278, IRD 198, Inserm 1095, Institut Hospitalo-Universitaire Méditerranée-Infection, Faculté de médecine, Aix-Marseille Université, 27 Boulevard Jean Moulin, 13385, Marseille Cedex 05, France

    Grégory Dubourg, Jean-Christophe Lagier, Catherine Robert, Nicholas Armstrong, Pierre-Edouard Fournier & Didier Raoult

  2. Pôle des Maladies Infectieuses et Tropicales Clinique et Biologique, Fédération de Bactériologie–Hygiène–Virologie, University, Hospital Centre Timone, Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, Assistance Publique–Hôpitaux de Marseille, Marseille, France

    Grégory Dubourg, Carine Couderc, Pierre-Edouard Fournier & Didier Raoult

  3. Special Infectious Agents Unit, King Fahd Medical Research Center, King Abdul Aziz University, Jeddah, Saudi Arabia

    Didier Raoult

Authors
  1. Grégory Dubourg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jean-Christophe Lagier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catherine Robert
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicholas Armstrong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carine Couderc
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pierre-Edouard Fournier
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Didier Raoult
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Didier Raoult.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dubourg, G., Lagier, JC., Robert, C. et al. Risungbinella massiliensis sp. nov., a new member of Thermoactinomycetaceae isolated from human gut. Antonie van Leeuwenhoek 109, 773–784 (2016). https://doi.org/10.1007/s10482-016-0677-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-016-0677-6

Keywords

  • Genome
  • Culturomics
  • Taxono-genomics