Genomics of the Uncultivated, Periodontitis-Associated Bacterium Tannerella sp. BU045 (Oral Taxon 808)

Beall, Clifford J.; Campbell, Alisha G.; Griffen, Ann L.; Podar, Mircea; Leys, Eugene J.

doi:10.1128/mSystems.00018-18

Genomics of the Uncultivated, Periodontitis-Associated Bacterium Tannerella sp. BU045 (Oral Taxon 808)

Journal Article · Tue Jun 05 00:00:00 EDT 2018 · mSystems

DOI:https://doi.org/10.1128/mSystems.00018-18· OSTI ID:1468065

^[1]; Campbell, Alisha G. ^[2]; Griffen, Ann L. ^[3]; ^[2]; Leys, Eugene J. ^[1]

The Ohio State Univ., Columbus, OH (United States). Division of Biosciences, College of Dentistry
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology
The Ohio State Univ., Columbus, OH (United States). Division of Pediatric Dentistry, College of Dentistry

Despite decades of research into the human oral microbiome, many species remain uncultivated. The technique of single-cell whole-genome amplification and sequencing provides a means of deriving genome sequences for species that can be informative on biological function and suggest pathways to cultivation. Tannerella forsythia has long been known to be highly associated with chronic periodontitis and to cause periodontitis-like symptoms in experimental animals, and Tannerella sp. BU045 (human oral taxon 808) is an uncultivated relative of this organism. Here, in this study, we extend our previous sequencing of the Tannerella sp. BU063 (human oral taxon 286) genome by sequencing amplified genomes from 11 cells of Tannerella sp. BU045, including 3 genomes that are at least 90% complete. Tannerella sp. BU045 is more closely related to Tannerella sp. BU063 than to T. forsythia by gene content and average nucleotide identity. However, two independent data sets of association with periodontitis, one based on 16S rRNA gene abundance and the other based on gene expression in a metatranscriptomic data set, show that Tannerella sp. BU045 is more highly associated with disease than Tannerella sp. BU063. Finally, comparative genomics shows genes and functions that are shared or unique to the different species, which may direct further research of the pathogenesis of chronic periodontitis.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1468065

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 3 Vol. 3; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (54)

Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Role of a Tannerella forsythia exopolysaccharide synthesis operon in biofilm development Honma, Kiyonobu; Inagaki, Satoru; Okuda, Katsuji Microbial Pathogenesis, Vol. 42, Issue 4 https://doi.org/10.1016/j.micpath.2007.01.003	journal	April 2007
In-depth snapshot of the equine subgingival microbiome Gao, Wenling; Chan, Yuki; You, Meng Microbial Pathogenesis, Vol. 94 https://doi.org/10.1016/j.micpath.2015.11.002	journal	May 2016
Comparison of periodontal pathogens between cats and their owners Booij-Vrieling, H. E.; van der Reijden, W. A.; Houwers, D. J. Veterinary Microbiology, Vol. 144, Issue 1-2 https://doi.org/10.1016/j.vetmic.2009.12.046	journal	July 2010
Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing Griffen, Ann L.; Beall, Clifford J.; Campbell, James H. The ISME Journal, Vol. 6, Issue 6 https://doi.org/10.1038/ismej.2011.191	journal	December 2011
A bacterial glycan core linked to surface (S)-layer proteins modulates host immunity through Th17 suppression Settem, R. P.; Honma, K.; Nakajima, T. Mucosal Immunology, Vol. 6, Issue 2 https://doi.org/10.1038/mi.2012.85	journal	September 2012
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
Functional biomarkers for chronic periodontitis and insights into the roles of Prevotella nigrescens and Fusobacterium nucleatum; a metatranscriptome analysis Szafrański, Szymon P.; Deng, Zhi-Luo; Tomasch, Jürgen npj Biofilms and Microbiomes, Vol. 1, Issue 1 https://doi.org/10.1038/npjbiofilms.2015.17	journal	September 2015
Mutations in virus-derived small RNAs Nigam, Deepti; LaTourrette, Katherine; Garcia-Ruiz, Hernan Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-66374-2	journal	June 2020
UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota Campbell, J. H.; O'Donoghue, P.; Campbell, A. G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 14, p. 5540-5545 https://doi.org/10.1073/pnas.1303090110	journal	March 2013
Characterization and Scope of S-layer Protein O -Glycosylation in Tannerella forsythia Posch, Gerald; Pabst, Martin; Brecker, Lothar Journal of Biological Chemistry, Vol. 286, Issue 44 https://doi.org/10.1074/jbc.M111.284893	journal	September 2011
A Rapid Bootstrap Algorithm for the RAxML Web Servers Stamatakis, Alexandros; Hoover, Paul; Rougemont, Jacques Systematic Biology, Vol. 57, Issue 5 https://doi.org/10.1080/10635150802429642	journal	October 2008
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
Biopython: freely available Python tools for computational molecular biology and bioinformatics Cock, P. J. A.; Antao, T.; Chang, J. T. Bioinformatics, Vol. 25, Issue 11 https://doi.org/10.1093/bioinformatics/btp163	journal	March 2009
IMG ER: a system for microbial genome annotation expert review and curation Markowitz, Victor M.; Mavromatis, Konstantinos; Ivanova, Natalia N. Bioinformatics, Vol. 25, Issue 17 https://doi.org/10.1093/bioinformatics/btp393	journal	June 2009
QUAST: quality assessment tool for genome assemblies Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay Bioinformatics, Vol. 29, Issue 8 https://doi.org/10.1093/bioinformatics/btt086	journal	February 2013
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
RNAmmer: consistent and rapid annotation of ribosomal RNA genes Lagesen, Karin; Hallin, Peter; Rødland, Einar Andreas Nucleic Acids Research, Vol. 35, Issue 9 https://doi.org/10.1093/nar/gkm160	journal	April 2007
Microbial species delineation using whole genome sequences Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia Nucleic Acids Research, Vol. 43, Issue 14 https://doi.org/10.1093/nar/gkv657	journal	July 2015
Reclassification of Bacteroides forsythus (Tanner et al. 1986) as Tannerella forsythensis corrig., gen. nov., comb. nov. Suzuki, Masahito; Benno, Yoshimi; Umeda, Makoto International Journal of Systematic and Evolutionary Microbiology, Vol. 52, Issue 3 https://doi.org/10.1099/00207713-52-3-841	journal	May 2002
Proposal to conserve the adjectival form of the specific epithet in the reclassification of Bacteroides forsythus Tanner et al. 1986 to the genus Tannerella Sakamoto et al. 2002 as Tannerella forsythia corrig., gen. nov., comb. nov. Request for an Opinion Maiden, M. F. J. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 53, Issue 6 https://doi.org/10.1099/ijs.0.02641-0	journal	November 2003
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Genus Enhydrobacter Staley et al. 1987 should be recognized as a member of the family Rhodospirillaceae within the class Alphaproteobacteria: Taxonomic position of genus Enhydrobacter Kawamura, Yoshiaki; Fujiwara, Nagatoshi; Naka, Takashi Microbiology and Immunology, Vol. 56, Issue 1 https://doi.org/10.1111/j.1348-0421.2011.00401.x	journal	January 2012
Microbial complexes in subgingival plaque Socransky, S. S.; Haffajee, A. D.; Cugini, M. A. Journal of Clinical Periodontology, Vol. 25, Issue 2, p. 134-144 https://doi.org/10.1111/j.1600-051X.1998.tb02419.x	journal	February 1998
Rat Model of Polymicrobial Infection, Immunity, and Alveolar Bone Resorption in Periodontal Disease Kesavalu, L.; Sathishkumar, S.; Bakthavatchalu, V. Infection and Immunity, Vol. 75, Issue 4 https://doi.org/10.1128/IAI.00733-06	journal	January 2007
Dependence of proliferation of Bacteroides forsythus on exogenous N-acetylmuramic acid. Wyss, C. Infection and Immunity, Vol. 57, Issue 6 https://doi.org/10.1128/IAI.57.6.1757-1759.1989	journal	January 1989
The Human Oral Microbiome Dewhirst, F. E.; Chen, T.; Izard, J. Journal of Bacteriology, Vol. 192, Issue 19 https://doi.org/10.1128/JB.00542-10	journal	July 2010
Association of Bacteroides forsythus and a Novel Bacteroides Phylotype with Periodontitis Leys, E. J.; Lyons, S. R.; Moeschberger, M. L. Journal of Clinical Microbiology, Vol. 40, Issue 3 https://doi.org/10.1128/JCM.40.3.821-825.2002	journal	March 2002
Draft Genome Sequence of Tannerella forsythia Type Strain ATCC 43037 Friedrich, Valentin; Pabinger, Stephan; Chen, Tsute Genome Announcements, Vol. 3, Issue 3 https://doi.org/10.1128/genomeA.00660-15	journal	June 2015
Dependence of proliferation of Bacteroides forsythus on exogenous N-acetylmuramic acid. Wyss, C. Infection and Immunity, Vol. 57, Issue 6 https://doi.org/10.1128/iai.57.6.1757-1759.1989	journal	January 1989
A Commensal Bacterium Promotes Virulence of an Opportunistic Pathogen via Cross-Respiration Stacy, Apollo; Fleming, Derek; Lamont, Richard J. mBio, Vol. 7, Issue 3 https://doi.org/10.1128/mBio.00782-16	journal	June 2016
Draft Genome Sequence of Medusavirus Stheno, Isolated from the Tatakai River of Uji, Japan Yoshida, Koki; Zhang, Ruixuan; Garcia, Kimberly G. Microbiology Resource Announcements, Vol. 10, Issue 1 https://doi.org/10.1128/mra.01323-20	journal	January 2021
First Cultivation of Health-Associated Tannerella sp. HOT-286 (BU063) Vartoukian, S. R.; Moazzez, R. V.; Paster, B. J. Journal of Dental Research, Vol. 95, Issue 11 https://doi.org/10.1177/0022034516651078	journal	July 2016
Tannerella forsythia -induced Alveolar Bone Loss in Mice Involves Leucine-rich-repeat BspA Protein Sharma, A.; Inagaki, S.; Honma, K. Journal of Dental Research, Vol. 84, Issue 5 https://doi.org/10.1177/154405910508400512	journal	May 2005
Versatile and open software for comparing large genomes Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L. Genome Biology, Vol. 5, Issue 2, R12 https://doi.org/10.1186/gb-2004-5-2-r12	journal	January 2004
Characterization and functional analysis of phytoene synthase gene family in tobacco Wang, Zhaojun; Zhang, Lin; Dong, Chen BMC Plant Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s12870-020-02816-3	journal	January 2021
Polinton-like viruses are abundant in aquatic ecosystems Bellas, Christopher M.; Sommaruga, Ruben Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-020-00956-0	journal	January 2021
A RESTful API for Accessing Microbial Community Data for MG-RAST Wilke, Andreas; Bischof, Jared; Harrison, Travis PLoS Computational Biology, Vol. 11, Issue 1 https://doi.org/10.1371/journal.pcbi.1004008	journal	January 2015
MEGAN Community Edition - Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data Huson, Daniel H.; Beier, Sina; Flade, Isabell PLOS Computational Biology, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pcbi.1004957	journal	June 2016
Multiple Single-Cell Genomes Provide Insight into Functions of Uncultured Deltaproteobacteria in the Human Oral Cavity Campbell, Alisha G.; Campbell, James H.; Schwientek, Patrick PLoS ONE, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pone.0059361	journal	March 2013
Bacterial Community Development in Experimental Gingivitis Kistler, James O.; Booth, Veronica; Bradshaw, David J. PLoS ONE, Vol. 8, Issue 8 https://doi.org/10.1371/journal.pone.0071227	journal	August 2013
Single Cell Genomics of Uncultured, Health-Associated Tannerella BU063 (Oral Taxon 286) and Comparison to the Closely Related Pathogen Tannerella forsythia Beall, Clifford J.; Campbell, Alisha G.; Dayeh, Daniel M. PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0089398	journal	February 2014
Neutrophil Mobilization by Surface-Glycan Altered Th17-Skewing Bacteria Mitigates Periodontal Pathogen Persistence and Associated Alveolar Bone Loss Settem, Rajendra P.; Honma, Kiyonobu; Sharma, Ashu PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0108030	journal	September 2014
Comparison of the Oral Microbiomes of Canines and Their Owners Using Next-Generation Sequencing Oh, Changin; Lee, Kunkyu; Cheong, Yeotaek PLOS ONE, Vol. 10, Issue 7 https://doi.org/10.1371/journal.pone.0131468	journal	July 2015
A Pyrosequencing Investigation of Differences in the Feline Subgingival Microbiota in Health, Gingivitis and Mild Periodontitis Harris, Stephen; Croft, Julie; O’Flynn, Ciaran PLOS ONE, Vol. 10, Issue 11 https://doi.org/10.1371/journal.pone.0136986	journal	November 2015
A novel matrix metalloprotease-like enzyme (karilysin) of the periodontal pathogen Tannerella forsythia ATCC 43037 Karim, Abdulkarim Y.; Kulczycka, Magdalena; Kantyka, Tomasz Biological Chemistry, Vol. 391, Issue 1 https://doi.org/10.1515/BC.2010.009	journal	January 2010
KLIKK proteases of Tannerella forsythia: putative virulence factors with a unique domain structure Ksiazek, Miroslaw; Mizgalska, Danuta; Eick, Sigrum Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00312	journal	April 2015
A Metalloproteinase Mirolysin of Tannerella forsythia Inhibits All Pathways of the Complement System Jusko, Monika; Potempa, Jan; Mizgalska, Danuta The Journal of Immunology, Vol. 195, Issue 5 https://doi.org/10.4049/jimmunol.1402892	journal	July 2015
PhyloSift: Phylogenetic analysis of genomes and metagenomes Bik, Holly; Matsen, Erick; Lowe, Eric Figshare https://doi.org/10.6084/m9.figshare.706369	dataset	January 2013
PhyloSift: Phylogenetic analysis of genomes and metagenomes Bik, Holly; Matsen, Erick; Lowe, Eric figshare https://doi.org/10.6084/m9.figshare.706369.v1	dataset	January 2013
PhyloSift: phylogenetic analysis of genomes and metagenomes Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric PeerJ, Vol. 2 https://doi.org/10.7717/peerj.243	journal	January 2014
KLIKK proteases of Tannerella forsythia: putative virulence factors with a unique domain structure. Thøgersen, Ida B.; Eick, Sigrun; Potempa, Jan Frontiers https://doi.org/10.7892/boris.72322	text	January 2015
A Metalloproteinase Mirolysin of Tannerella forsythia Inhibits All Pathways of the Complement System Jusko, Monika; Riesbeck, Kristian; Blom, Anna M. American Association of Immunologists https://doi.org/10.7892/boris.75637	text	January 2015

Cited By (2)

Oral microbial biofilms: an update Mosaddad, Seyed Ali; Tahmasebi, Elahe; Yazdanian, Alireza European Journal of Clinical Microbiology & Infectious Diseases, Vol. 38, Issue 11 https://doi.org/10.1007/s10096-019-03641-9	journal	August 2019
Comparative genome characterization of the periodontal pathogen Tannerella forsythia Zwickl, Nikolaus F.; Stralis-Pavese, Nancy; Schäffer, Christina BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-6535-y	journal	February 2020

Similar Records

Single Cell Genomics of Uncultured, Health-Associated Tannerella BU063 (Oral Taxon 286) and Comparison to the Closely Related Pathogen Tannerella forsythia

Journal Article · Thu Feb 13 23:00:00 EST 2014 · PLoS ONE · OSTI ID:1627681

Multiple Single-Cell Genomes Provide Insight into Functions of Uncultured Deltaproteobacteria in the Human Oral Cavity

Journal Article · Tue Mar 26 00:00:00 EDT 2013 · PLoS ONE · OSTI ID:1627591

Non-contiguous finished genome sequence of the opportunistic oral pathogen Prevotella multisaccharivorax type strain (PPPA20^T)

Journal Article · Sat Oct 15 00:00:00 EDT 2011 · Standards in Genomic Sciences · OSTI ID:1630576

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Genomics of the Uncultivated, Periodontitis-Associated Bacterium Tannerella sp. BU045 (Oral Taxon 808)

Citation Formats

References (54)

Cited By (2)

Similar Records

Related Subjects