Abstract
The novel strain AM35T was isolated from the faeces of C57BL/6 mice. These cells are strictly anaerobic, gram negative, oxidase negative, catalase positive, rod-shaped and non-motile. The strain produced creamy yellowish colonies on brain heart infusion (BHI) agar with hemin. Growth was investigated at 30–41 °C in the presence of 0.5–1.5% (w/v) NaCl at pH 6.5–8.5. Taxonomic analysis based on 16S rRNA gene sequencing revealed that strain AM35T is affiliated with the family Muribaculaceae and closely related to the genus Muribaculum. The genomic DNA G + C content of strain AM35T was 47.8 mol%. We detected the whole-cell sugars ribose and galactose; meso-2,6-diaminopimelic acid was absent. The major fatty acids (> 10%) were anteiso-C15:0 and iso-C15:0; the major polar lipid was phosphatidylethanolamine. The major respiratory quinones were MK-10 and MK-11. Based on our phylogenetic, phenotypic and chemotaxonomic analyses, strain AM35T represents a novel genus within the family Muribaculaceae, for which we propose the name Heminiphilus faecis gen. nov., sp. nov. The type strain of Heminiphilus faecis gen. nov., sp. nov. is AM35T (= KCTC 15907 T = DSM 110151 T).
Similar content being viewed by others
Abbreviations
- isDDH:
-
In silico DNA–DNA hybridization
- ANI:
-
Average nucleotide identity.
- RAST:
-
Rapid Annotation using Subsystem Technology
References
Bankevich A et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Bauerl C, Collado MC, Diaz Cuevas A, Vina J, Perez Martinez G (2018) Shifts in gut microbiota composition in an APP/PSS1 transgenic mouse model of Alzheimer’s disease during lifespan. Lett Appl Microbiol. 66:464–471. https://doi.org/10.1111/lam.12882
Brettin T et al (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep. 5:8365. https://doi.org/10.1038/srep08365
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973
Chang D-H et al (2016) Pseudomonas kribbensis sp. nov., isolated from garden soils in Daejeon. Korea Antonie Van Leeuwenhoek 109:1433–1446
Chaplin A, Efimov B, Khokhlova E, Kafarskaia L, Tupikin A, Kabilov M, Shkoporov A (2014) Draft genome sequence of Coprobacter fastidiosus NSB1T Genome announcements. 2
Darling AE, Jospin G, Lowe E, Matsen FA IV, Bik HM, Eisen JA (2014) PhyloSift: phylogenetic analysis of genomes and metagenomes. PeerJ. 2:e243
Evans CC et al (2014) Exercise prevents weight gain and alters the gut microbiota in a mouse model of high fat diet-induced obesity. PLoS ONE 9:e92193. https://doi.org/10.1371/journal.pone.0092193
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach Journal of molecular evolution 17:368–376
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 20:406–416
Fujimoto S, Nakagami Y, Kojima F (2004) Optimal bacterial DNA isolation method using bead-beating technique Memoirs Kyushu Univ Dep Of Health Scis Of Medical Sch 3:33–38
Garzetti D, Brugiroux S, Bunk B, Pukall R, McCoy KD, Macpherson AJ, Stecher B (2017) High-quality whole-genome sequences of the oligo-mouse-microbiota bacterial community Genome announcements. 5
Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91
Hall TA BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In: Nucleic acids symposium series, 1999. vol 41. [London]: Information Retrieval Ltd., c1979-c2000; 95–98
Hoang DT, Chernomor O, Von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522
Kalyaanamoorthy S, Minh BQ, Wong TK, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences Journal of molecular evolution 16:111–120
Knowles SCL, Eccles RM, Baltrunaite L (2019) Species identity dominates over environment in shaping the microbiota of small mammals. Ecol Lett 22:826–837. https://doi.org/10.1111/ele.13240
Krych L, Nielsen DS, Hansen AK, Hansen CH (2015) Gut microbial markers are associated with diabetes onset, regulatory imbalance and IFN-gamma level in NOD mice. Gut Microbes. 6:101–109. https://doi.org/10.1080/19490976.2015.1011876
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lagkouvardos I et al (2019) Sequence and cultivation study of Muribaculaceae reveals novel species, host preference and functional potential of this yet undescribed family. Microbiome 7:28. https://doi.org/10.1186/s40168-019-0637-2
Lagkouvardos I et al (2016) The Mouse Intestinal Bacterial Collection (miBC) provides host-specific insight into cultured diversity and functional potential of the gut microbiota. Nat Microbiol. 1:16131. https://doi.org/10.1038/nmicrobiol.2016.131
Lee G-H, Rhee M-S, Chang D-H, Kwon KK, Bae KS, Yang S-H, Kim B-C (2014) Bacillus solimangrovi sp. nov., isolated from mangrove soil. Int J Syst Evol Microbiol 64:1622–1628
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
Liu C et al (2020) The Mouse Gut Microbial Biobank expands the coverage of cultured bacteria Nature communications 11:1–12
Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions BMC bioinformatics 14:60
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, Von Haeseler A, Lanfear R (2020) IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era Molecular. Biology and Evolution. 37:1530–1534
Miyake S, Ding Y, Soh M, Low A, Seedorf H (2020a) Cultivation and description of Duncaniella dubosii sp. nov., Duncaniella freteri sp. nov. and emended description of the species Duncaniella muris. Int J Syst Evol Microbiol. 70:3105–3110. https://doi.org/10.1099/ijsem.0.004137
Miyake S, Ding Y, Soh M, Low A, Seedorf H (2020b) Muribaculum gordoncarteri sp. nov., an anaerobic bacterium from the faeces of C57BL/6J mice. Int J Syst Evol Microbiol. 70:4725–4729. https://doi.org/10.1099/ijsem.0.004338
Miyake S, Ding Y, Soh M, Seedorf H (2019) Complete genome sequence of Duncaniella muris Strain B8, isolated from the feces of C57/BL6 Mice. Microbiology resource announcements. 8:e00566-e519
Morotomi M, Nagai F, Sakon H, Tanaka R (2008) Dialister succinatiphilus sp. nov and Barnesiella intestinihominis sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 58:2716–2720
Nakajima M et al (2015) Oral administration of P. gingivalis induces dysbiosis of gut microbiota and impaired barrier function leading to dissemination of enterobacteria to the liver. PLoS One 10:e0134234. https://doi.org/10.1371/journal.pone.0134234
Ormerod KL et al. (2016) Genomic characterization of the uncultured Bacteroidales family S24–7 inhabiting the guts of homeothermic animals Microbiome. 4; 36 doi:https://doi.org/10.1186/s40168-016-0181-2
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates. single cells and metagenomes Genome research. 25; 1043–1055
Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 106:19126–19131
Rogier R et al (2017) Alteration of the intestinal microbiome characterizes preclinical inflammatory arthritis in mice and its modulation attenuates established arthritis Sci Rep 7:15613. https://doi.org/10.1038/s41598-017-15802-x
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sakamoto M, Lan PTN, Benno Y (2007) Barnesiella viscericola gen. nov., sp. nov., a novel member of the family Porphyromonadaceae isolated from chicken caecum. Int J Syst Evol Microbiol 57:342–346
Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications Bacteriological reviews 36:407
Seedorf H et al (2014) Bacteria from diverse habitats colonize and compete in the mouse gut. Cell 159:253–266. https://doi.org/10.1016/j.cell.2014.09.008
Shkoporov AN et al (2015) Alistipes inops sp. nov. and Coprobacter secundus sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 65:4580–4588
Shkoporov AN et al (2013) Coprobacter fastidiosus gen. nov., sp. nov., a novel member of the family Porphyromonadaceae isolated from infant faeces. Int J Syst Evol Microbiol 63:4181–4188
Smith BJ, Miller RA, Ericsson AC, Harrison DE, Strong R, Schmidt TM (2018) Changes in the gut microbiota and fermentation products associated with enhanced longevity in acarbose-treated mice. BioRxiv. 311456
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic acids research. 22; 4673–4680
Tindall B (1990a) A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 13:128–130
Tindall B (1990b) Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 66:199–202
Tropini C et al (2018) Transient Osmotic Perturbation Causes Long-Term Alteration to the Gut Microbiota. Cell 173(1742–1754):e1717. https://doi.org/10.1016/j.cell.2018.05.008
Wayne L et al (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 37:463–464
Yarza P 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
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol. 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Acknowledgements
This study was supported by grants from the National Research Foundation of Korea (NRF) (2015M3C9A4053394) and the KRIBB Research Initiative Program of the Republic of Korea.
Author information
Authors and Affiliations
Contributions
BCK and ML established the main idea of the manuscript. JKP, MSR and DHC designed the experiments and performed data analysis. JKP and BCK wrote the manuscript. The review has been checked and revised by HJ, JS, BJK and SBK.
Corresponding authors
Ethics declarations
Conflicts of interest
The authors declare that there are no conflicts of interest.
Ethical statement
All animal experiments were approved by the Institutional Animal Use and Care Committee of the Korea Research Institute of Bioscience and Biotechnology (KRIBB-AEC-18114).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Park, J.K., Chang, DH., Rhee, MS. et al. Heminiphilus faecis gen. nov., sp. nov., a member of the family Muribaculaceae, isolated from mouse faeces and emended description of the genus Muribaculum. Antonie van Leeuwenhoek 114, 275–286 (2021). https://doi.org/10.1007/s10482-021-01521-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-021-01521-x