Isolation and Description of Catonella massiliensis sp. nov., a Novel Catonella Species, Isolated from a Stable Periodontitis Subject
Abstract
:1. Introduction
2. Results
2.1. Strain Isolation and Phenotypic Characteristics
2.2. Genome Sequencing Information and Genome Properties
2.3. Comparison with Closely Related Bacterial Strains
2.4. Description of Catonella Massiliensis sp. nov.
3. Discussion
4. Materials and Methods
4.1. Strain Isolation and Phenotypic Tests
4.2. Extraction and Genome Sequencing
4.3. Assembly and Annotation of the Genome Sequence
4.4. Phylogenetic Analysis and Genome Comparison
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Deo, P.N.; Deshmukh, R. Oral microbiome: Unveiling the fundamentals. J. Oral Maxillofac. Pathol. 2019, 23, 122–128. [Google Scholar] [CrossRef]
- Socransky, S.S.; Haffajee, A.D. Periodontal microbial ecology. Periodontol. 2000 2005, 38, 135–187. [Google Scholar] [CrossRef]
- Curtis, M.A.; Diaz, P.I.; Van Dyke, T.E. The role of the microbiota in periodontal disease. Periodontol. 2000 2020, 83, 14–25. [Google Scholar] [CrossRef]
- Nyvad, B.; Takahashi, N. Integrated hypothesis of dental caries and periodontal diseases. J. Oral Microbiol. 2020, 12, 1710953. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ye, S.H.; Siddle, K.J.; Park, D.J.; Sabeti, P.C. Benchmarking Metagenomics Tools for Taxonomic Classification. Cell 2019, 178, 779–794. [Google Scholar] [CrossRef]
- Baker, J.L.; Morton, J.T.; Dinis, M.; Alvarez, R.; Tran, N.C.; Knight, R.; Edlund, A. Deep metagenomics examines the oral microbiome during dental caries, revealing novel taxa and co-occurrences with host molecules. Genome Res. 2021, 31, 64–74. [Google Scholar] [CrossRef] [PubMed]
- Qi, Y.; Zang, S.-Q.; Wei, J.; Yu, H.-C.; Yang, Z.; Wu, H.-M.; Kang, Y.; Tao, H.; Yang, M.-F.; Jin, L.; et al. High-throughput sequencing provides insights into oral microbiota dysbiosis in association with inflammatory bowel disease. Genomics 2021, 113, 664–676. [Google Scholar] [CrossRef]
- Chen, T.; Yu, W.-H.; Izard, J.; Baranova, O.V.; Lakshmanan, A.; Dewhirst, F.E. The Human Oral Microbiome Database: A web accessible resource for investigating oral microbe taxonomic and genomic information. Database 2010, 2010, baq013. [Google Scholar] [CrossRef] [PubMed]
- Wade, W.; Thompson, H.; Rybalka, A.; Vartoukian, S. Uncultured Members of the Oral Microbiome. J. Calif. Dent. Assoc. 2016, 44, 447–456. [Google Scholar] [PubMed]
- Vartoukian, S.R.; Palmer, R.M.; Wade, W.G. Strategies for culture of ‘unculturable’ bacteria: Culturing the unculturable. FEMS Microbiol. Lett. 2010, 309, 1–7. [Google Scholar] [CrossRef] [Green Version]
- Papapanou, P.N.; Sanz, M.; Buduneli, N.; Dietrich, T.; Feres, M.; Fine, D.H.; Flemmig, T.F.; Garcia, R.; Giannobile, W.V.; Graziani, F.; et al. Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J. Clin. Periodontol. 2018, 45, S162–S170. [Google Scholar] [CrossRef]
- Chapple, I.L.C.; Mealey, B.L.; Van Dyke, T.E.; Bartold, P.M.; Dommisch, H.; Eickholz, P.; Geisinger, M.L.; Genco, R.J.; Glogauer, M.; Goldstein, M.; et al. Periodontal health and gingival diseases and conditions on an intact and a reduced periodontium: Consensus report of workgroup 1 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J. Periodontol. 2018, 89, S74–S84. [Google Scholar] [CrossRef] [PubMed]
- Moore, L.V.; Moore, W.E. Oribaculum catoniae gen. nov., sp. nov.; Catonella morbi gen. nov., sp. nov.; Hallella seregens gen. nov., sp. nov.; Johnsonella ignava gen. nov., sp. nov.; and Dialister pneumosintes gen. nov., comb. nov., nom. rev., Anaerobic Gram-Negative Bacilli from the Human Gingival Crevice. Int. J. Syst. Bacteriol. 1994, 44, 187–192. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, X.; Chen, J.; Xu, W.; Zhu, D.; Wang, X.; Chen, Y.; Wu, J.; Cui, C.; Zhang, W.; Yu, L. 16S rDNA analysis of periodontal plaque in chronic obstructive pulmonary disease and periodontitis patients. J. Oral Microbiol. 2017, 9, 1324725. [Google Scholar] [CrossRef] [PubMed]
- Colombo, A.P.V.; Bennet, S.; Cotton, S.L.; Goodson, J.M.; Kent, R.; Haffajee, A.D.; Socransky, S.S.; Hasturk, H.; Van Dyke, T.E.; Dewhirst, F.E.; et al. Impact of Periodontal Therapy on the Subgingival Microbiota of Severe Periodontitis: Comparison Between Good Responders and Individuals With Refractory Periodontitis Using the Human Oral Microbe Identification Microarray. J Periodontol. 2012, 83, 1279–1287. [Google Scholar] [CrossRef] [PubMed]
- Siqueira, J.F.; Rôças, I.N. Catonella morbi and Granulicatella adiacens: New species in endodontic infections. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endodontol. 2006, 102, 259–264. [Google Scholar] [CrossRef] [PubMed]
- Lagkouvardos, I.; Pukall, R.; Abt, B.; Foesel, B.U.; Meier-Kolthoff, J.P.; Kumar, N.; Bresciani, A.; Martínez, I.; Just, S.; Ziegler, C.; et al. The Mouse Intestinal Bacterial Collection (miBC) provides host-specific insight into cultured diversity and functional potential of the gut microbiota. Nat. Microbiol. 2016, 1, 16131. [Google Scholar] [CrossRef] [Green Version]
- Sakamoto, M.; Iino, T.; Ohkuma, M. Faecalimonas umbilicata gen. nov., sp. nov., isolated from human faeces, and reclassification of Eubacterium contortum, Eubacterium fissicatena and Clostridium oroticum as Faecalicatena contorta gen. nov., comb. nov., Faecalicatena fissicatena comb. nov. and Faecalicatena orotica comb. nov. Int. J. Syst. Evol. Microbiol. 2017, 67, 1219–1227. [Google Scholar] [CrossRef]
- Ueki, A.; Ohtaki, Y.; Kaku, N.; Ueki, K. Descriptions of Anaerotaenia torta gen. nov., sp. nov. and Anaerocolumna cellulosilytica gen. nov., sp. nov. isolated from a methanogenic reactor of cattle waste and reclassification of Clostridium aminovalericum, Clostridium jejuense and Clostridium xylanovorans as Anaerocolumna species. Int. J. Syst. Evol. Microbiol. 2016, 66, 2936–2943. [Google Scholar] [CrossRef] [Green Version]
- Koeck, D.E.; Hahnke, S.; Zverlov, V.V. Herbinix luporum sp. nov., a thermophilic cellulose-degrading bacterium isolated from a thermophilic biogas reactor. Int. J. Syst. Evol. Microbiol. 2016, 66, 4132–4137. [Google Scholar] [CrossRef]
- Stothard, P.; Wishart, D.S. Circular genome visualization and exploration using CGView. Bioinformatics 2004, 21, 537–539. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
- Seng, P.; Drancourt, M.; Gouriet, F.; La Scola, B.; Fournier, P.; Rolain, J.M.; Raoult, D. Ongoing Revolution in Bacteriology: Routine Identification of Bacteria by Matrix-Assisted Laser Desorption Ionization Time-of-Flight Mass Spectrometry. Clin. Infect. Dis. 2009, 49, 543–551. [Google Scholar] [CrossRef]
- Seng, P.; Abat, C.; Rolain, J.M.; Colson, P.; Lagier, J.-C.; Gouriet, F.; Fournier, P.E.; Drancourt, M.; La Scola, B.; Raoult, D. 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. 2013, 51, 2182–2194. [Google Scholar] [CrossRef] [Green Version]
- Sasser, M. Bacterial Identification by Gas Chromatographic Analysis of Fatty Acid Methyl Esters (GC-FAME); Microbial ID: Newark, NJ, USA, 2006. [Google Scholar]
- Dione, N.; Sankar, S.; Lagier, J.-C.; Khelaifia, S.; Michele, C.; Armstrong, N.; Richez, M.; Abrahão, J.; Raoult, D.; Fournier, P.-E. Genome sequence and description of Anaerosalibacter massiliensis sp. nov. New Microbes New Infect. 2016, 10, 66–76. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zerbino, D.R.; Birney, E. Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008, 18, 821–829. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bankevich, A.; Nurk, S.; Antipov, D.; Gurevich, A.A.; Dvorkin, M.; Kulikov, A.S.; Lesin, V.M.; Nikolenko, S.I.; Pham, S.; Prjibelski, A.D.; et al. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J. Comput. Biol. 2012, 19, 455–477. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, R.; Liu, B.; Xie, Y.; Li, Z.; Huang, W.; Yuan, J.; He, G.; Chen, Y.; Pan, Q.; Liu, Y.; et al. SOAPdenovo2: An empirically improved memory-efficient short-read de novo assembler. GigaScience 2012, 1, 18. [Google Scholar] [CrossRef] [PubMed]
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef] [Green Version]
- Hyatt, D.; Chen, G.-L.; LoCascio, P.F.; Land, M.L.; Larimer, F.W.; Hauser, L.J. Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010, 11, 119. [Google Scholar] [CrossRef] [Green Version]
- Clark, K.; Karsch-Mizrachi, I.; Lipman, D.J.; Ostell, J.; Sayers, E.W. GenBank. Nucleic Acids Res. 2016, 44, D67–D72. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seemann, T. Prokka: Rapid Prokaryotic Genome Annotation. Bioinformatics 2014, 30, 2068–2069. [Google Scholar] [CrossRef]
- Cuccuru, G.; Orsini, M.; Pinna, A.; Sbardellati, A.; Soranzo, N.; Travaglione, A.; Uva, P.; Zanetti, G.; Fotia, G. Orione, a web-based framework for NGS analysis in microbiology. Bioinformatics 2014, 30, 1928–1929. [Google Scholar] [CrossRef] [Green Version]
- Seemann, T. ABRicate: Mass Screening of Contigs for Antiobiotic Resistance Genes. Available online: https://github.com/tseemann/abricate (accessed on 10 January 2021).
- Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980, 16, 111–120. [Google Scholar] [CrossRef]
- Meier-Kolthoff, J.P.; Auch, A.F.; Klenk, H.-P.; Göker, M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013, 14, 60. [Google Scholar] [CrossRef] [Green Version]
- Lee, I.; Kim, Y.O.; Park, S.-C.; Chun, J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evol. Microbiol. 2016, 66, 1100–1103. [Google Scholar] [CrossRef]
- Page, A.J.; Cummins, C.A.; Hunt, M.; Wong, V.K.; Reuter, S.; Holden, M.T.; Fookes, M.; Falush, D.; Keane, J.A.; Parkhill, J. Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015, 31, 3691–3693. [Google Scholar] [CrossRef]
Characteristic | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 |
---|---|---|---|---|---|---|---|---|
Gram stain | - | + | + | + | + | + | - | + |
Spore formation | - | - | + | - | - | + | - | - |
Temperature (°C) | 28–41.5 | 37 | 20–40 | 20–40 | 20–40 | 15–40 | 37 | 40–65 |
pH | 6.5–8.5 | 7.0 | 6.0–8.0 | 6.0–8.0 | 6.0–8.0 | 6.2–8.5 | 5.0–5.6 | 6.5–8.5 |
Catalase activity | - | ND | ND | ND | - | - | - | - |
Oxidase activity | - | ND | ND | ND | ND | - | ND | ND |
Acid produced from: | ||||||||
L-Arabinose | + | + | + | + | + | + | - | + |
Cellobiose | + | - | + | + | - | + | + | + |
Lactose | + | - | + | + | - | + | + | - |
Maltose | + | - | + | + | + | + | + | ND |
D-Mannitol | + | - | + | - | - | - | - | ND |
D-Mannose | + | - | + | + | + | + | - | + |
Raffinose | + | - | + | + | - | - | + | ND |
L-Rhamnose | + | + | + | + | + | - | + | ND |
D-Sorbitol | + | - | + | - | - | - | - | - |
Enzyme activity: | ||||||||
Alkaline phosphatase | + | - | - | - | - | ND | ND | ND |
C4 esterase | - | ND | w | w | w | ND | ND | ND |
C8 esterase lipase | - | ND | w | w | - | ND | ND | ND |
C14 lipase | - | ND | - | - | - | - | ND | ND |
Leucine arylamidase | + | - | - | - | - | ND | ND | ND |
Valine arylamidase | - | ND | - | - | - | ND | ND | ND |
Cystine arylamidase | - | ND | - | - | - | ND | ND | ND |
Trypsin | - | ND | - | - | - | ND | ND | ND |
α-Chymotrypsin | - | ND | - | - | - | ND | ND | ND |
Acid phosphatase | + | ND | + | + | w | ND | ND | ND |
Naphthol-AS-BI-phosphohydrolase | + | ND | w | w | w | ND | ND | ND |
α-Galactosidase | + | + | + | + | + | ND | ND | ND |
β-Galactosidase | + | + | + | + | - | ND | ND | ND |
β-Glucuronidase | - | + | + | - | - | ND | ND | ND |
α-Glucosidase | + | + | + | w | + | ND | ND | ND |
β-Glucosidase | + | + | + | - | - | ND | ND | ND |
N-Acetyl-β-glucosaminidase | + | - | - | - | - | ND | ND | ND |
α-Mannosidase | - | ND | - | - | - | ND | ND | ND |
α-Fucosidase | - | - | + | - | - | ND | ND | ND |
Fatty Acid | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 |
---|---|---|---|---|---|---|---|---|
C12:0 | TR | ND | 1.6 | 3.3 | 2.6 | ND | ND | ND |
C13:0 | TR | ND | - | - | - | ND | ND | ND |
C14:0 | 6.4 | 6.2 | 6.0 | 9.3 | 9.2 | 0.6 | 42 | 14.0 |
C14:0 DMA | ND | ND | - | - | - | 1.5 | 14 | 9.1 |
C15:0 | TR | ND | - | - | - | ND | ND | ND |
C16:0 | 64.2 | 43.4 | 12.0 | 15.6 | 15.6 | 5.5 | 12 | 19.9 |
C16:0 ALDE | - | ND | - | - | - | 20.6 | ND | 2.9 |
C16:0 DMA | ND | ND | 2.0 | 3.4 | 3.4 | 17.4 | ND | 5.3 |
C16:0 3-OH | - | ND | ND | ND | ND | 1.2 | ND | ND |
C16:1ω9c DMA | ND | ND | ND | ND | ND | 3.8 | ND | ND |
C16:1n9 | - | ND | ND | ND | ND | ND | 2 | 1.2 |
C17:0 | TR | ND | - | - | - | ND | ND | ND |
C17:1 ω8c | ND | 8.3 | ND | ND | ND | ND | ND | ND |
C18:0 | 6.6 | ND | 1.4 | - | 3.9 | ND | 4 | 1.2 |
C18:1n7 | 1.3 | ND | ND | ND | ND | ND | ND | ND |
C18:1n9 | 12.5 | ND | 25.9 | 21.9 | 22.9 | ND | 5 | ND |
C18:1ω9C DMA | ND | ND | 37.0 | 36.3 | 28.6 | 3.1 | ND | ND |
C18:1ω7C DMA | ND | ND | 2.4 | - | 4.0 | 9.0 | ND | ND |
C18:2n6 | 7.8 | ND | ND | ND | ND | ND | ND | ND |
C19:0 cyclo 9,10 DMA | ND | ND | ND | ND | ND | ND | ND | 38.3 |
C19:0 cyclo 11,12 DMA | ND | ND | ND | ND | ND | 1.4 | ND | ND |
Code | Strain Marseille-Q4567 T | Description |
---|---|---|
[J] | 145 | Translation, ribosomal structure, and biogenesis |
[A] | 0 | RNA processing and modification |
[K] | 150 | Transcription |
[L] | 137 | Replication, recombination, and repair |
[B] | 0 | Chromatin structure and dynamics |
[D] | 29 | Cell cycle control, cell division, chromosome partitioning |
[Y] | 0 | Nuclear structure |
[V] | 76 | Defense mechanisms |
[T] | 82 | Signal transduction mechanisms |
[M] | 64 | Cell wall/membrane/envelope biogenesis |
[N] | 49 | Cell motility |
[Z] | 0 | Cytoskeleton |
[W] | 0 | Extracellular structures |
[U] | 38 | Intracellular trafficking, secretion, and vesicular transport |
[O] | 60 | Posttranslational modification, protein turnover, chaperones |
[X] | 0 | Mobilome: Prophages, transposons |
[C] | 74 | Energy production and conversion |
[G] | 183 | Carbohydrate transport and metabolism |
[E] | 141 | Amino acid transport and metabolism |
[F] | 51 | Nucleotide transport and metabolism |
[H] | 31 | Coenzyme transport and metabolism |
[I] | 47 | Lipid transport and metabolism |
[P] | 86 | Inorganic ion transport and metabolism |
[Q] | 21 | Secondary metabolites biosynthesis, transport, and catabolism |
[R] | 214 | General function prediction only |
[S] | 134 | Function unknown |
Species | Genome Size (bp) | Number of Contigs | G+C Content (%) | Gene Content |
---|---|---|---|---|
Catonella massiliensis Marseille-Q4567T | 3,122,925 | 3 | 38.8 | 2849 |
Cuneatibacter caecimuris DSM 29486T (NZ_SGXF01000001.1) | 3,462,725 | 16 | 49.1 | 3268 |
Eubacterium oxidoreducens DSM 3217T (NZ_FMXR01000031.1) | 2,912,287 | 33 | 39.8 | 2700 |
Faecalicatena orotica strain NLAE-zl-C242 (NZ_QGDL01000001.1) | 5,717,637 | 33 | 44.7 | 5174 |
Roseburia hominis A2-183T (NC_015977.1) | 3,592,125 | 1 | 48.5 | 3349 |
Faecalicatena contorta 2789STDY5834876 (NZ_CYZU01000001.1) | 5,545,490 | 139 | 45.9 | 5148 |
Faecalicatena fissicatena KCTC 15010 (NZ_LDAQ01000001.1) | 5,014,239 | 184 | 45.6 | 4411 |
Anaerocolumna cellulosilytica strain SN021T (NZ_AP023367.1) | 5,430,627 | 1 | 36.7 | 4545 |
Catonella morbi ATCC 51271T (NZ_KI535366.1) | 3,479,204 | 8 | 37.1 | 3155 |
Herbinix luporum strain SD1DT (NZ_LN879430.1) | 2,609,352 | 1 | 35.3 | 2430 |
Species | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 |
---|---|---|---|---|---|---|---|---|---|---|
1 Catonella massiliensis Marseille-Q4567T | 100.00 | 28.4 [26.1–30.9] | 27.0 [24.6–29.5] | 26.0 [23.7–28.5] | 24.8 [22.5–27.3 | 24.7 [22.3–27.1] | 24.60 [22.3–27.1] | 24.5 [22.2–27] | 23.80 [21.5–26.2] | 22.9 [20.6–25.3] |
2 Cuneatibacter caecimuris DSM 29486T (NZ_SGXF01000001.1) | 100.00 | 25.7 [23.3–28.1] | 23.0 [20.7–25.4] | 25.8 [23.5–28.3] | 19.2 [17–21.6] | 19.0 [16.8–21.4] | 25.4 [23.1–27.9] | 23.1 [20.8–25.5] | 30.1 [27.7–32.6] | |
3 Eubacterium oxidoreducens DSM 3217T (NZ_FMXR01000031.1) | 100.00 | 22.6 [20.3–25] | 23.2 [20.9–25.7] | 26.1 [23.8–28.6] | 22.9 [20.6–25.3] | 28.8 [26.4–31.3] | 29.3 [26.9–31.8] | 20.7 [18.4–23.1] | ||
4 Faecalicatena orotica strain NLAE-zl-C242 (NZ_QGDL01000001.1) | 100.00 | 22.0 [19.7–24.4] | 21.6 [19.4–24.1] | 21.7 [19.4–24.1 | 22.2 [20–24.7] | 22.2 [19.9–24.6] | 25.5 [23.2–28] | |||
5 Roseburia hominis A2-183T (NC_015977.1) | 100.00 | 24.0 [21.7–26.5] | 24.6 [22.3–27.1] | 32.9 [30.5–35.4] | 23.70 [21.4–26.1] | 29.2 [26.9–31.7] | ||||
6 Faecalicatena contorta 2789STDY5834876 (NZ_CYZU01000001.1) | 100.00 | 28.5 [26.2–31] | 28.5 [26.1–31] | 26.4 [24–28.8] | 25.8 [23.5–28.3] | |||||
7 Faecalicatena fissicatena KCTC 15010 (NZ_LDAQ01000001.1) | 100.00 | 26.4 [24.1–28.9] | 25.3 [22.9–27.8] | 23.1 [20.9–25.6] | ||||||
8 Anaerocolumna cellulosilytica strain SN021T (NZ_AP023367.1) | 100.00 | 24.1 [21.8–26.5] | 26.5 [24.1–29] | |||||||
9 Catonella morbi ATCC 51271T (NZ_KI535366.1) | 100.00 | 21.0 [18.8–23.4] | ||||||||
10 Herbinix luporum strain SD1DT (NZ_LN879430.1) | 100.00 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Antezack, A.; Boxberger, M.; La Scola, B.; Monnet-Corti, V. Isolation and Description of Catonella massiliensis sp. nov., a Novel Catonella Species, Isolated from a Stable Periodontitis Subject. Pathogens 2021, 10, 367. https://doi.org/10.3390/pathogens10030367
Antezack A, Boxberger M, La Scola B, Monnet-Corti V. Isolation and Description of Catonella massiliensis sp. nov., a Novel Catonella Species, Isolated from a Stable Periodontitis Subject. Pathogens. 2021; 10(3):367. https://doi.org/10.3390/pathogens10030367
Chicago/Turabian StyleAntezack, Angéline, Manon Boxberger, Bernard La Scola, and Virginie Monnet-Corti. 2021. "Isolation and Description of Catonella massiliensis sp. nov., a Novel Catonella Species, Isolated from a Stable Periodontitis Subject" Pathogens 10, no. 3: 367. https://doi.org/10.3390/pathogens10030367
APA StyleAntezack, A., Boxberger, M., La Scola, B., & Monnet-Corti, V. (2021). Isolation and Description of Catonella massiliensis sp. nov., a Novel Catonella Species, Isolated from a Stable Periodontitis Subject. Pathogens, 10(3), 367. https://doi.org/10.3390/pathogens10030367