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

Journal Article · · PLoS ONE
 [1];  [2];  [3];  [3];  [2];  [3]
  1. The Ohio State University, Columbus, OH (United States); DOE/OSTI
  2. Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); University of Tennessee, Knoxville, TN (United States)
  3. The Ohio State University, Columbus, OH (United States)

The uncultivated bacterium Tannerella BU063 (oral taxon 286) is the closest relative to the periodontal pathogen Tannerella forsythia, but is not disease-associated itself. Using a single cell genomics approach, we isolated 12 individual BU063 cells by flow cytometry, and we amplified and sequenced their genomes. Comparative analyses of the assembled genomic scaffolds and their gene contents allowed us to study the diversity of this taxon within the oral community of a single human donor that provided the sample. Eight different BU063 genotypes were represented, all about 5% divergent at the nucleotide level. There were 2 pairs of cells and one group of three that were more highly identical, and may represent clonal populations. We did pooled assemblies on the nearly identical genomes to increase the assembled genomic coverage. The presence of a set of 66 ‘‘core’’ housekeeping genes showed that two of the single cell assemblies and the assembly derived from the three putatively identical cells were essentially complete. As expected, the genome of BU063 is more similar to Tannerella forsythia than any other known genome, although there are significant differences, including a 44% difference in gene content, changes in metabolic pathways, loss of synteny, and an 8–9% difference in GC content. Several identified virulence genes of T. forsythia are not found in BU063 including karilysin, prtH, and bspA. The absence of these genes may explain the lack of periodontal pathogenesis by this species and provides a new foundation to further understand the genome evolution and mechanisms of bacterial-host interaction in closely related oral microbes with different pathogenicity potential.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institute of Dental and Craniofacial Research (NIDCR); National Human Genome Research Institute
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1627681
Journal Information:
PLoS ONE, Journal Name: PLoS ONE Journal Issue: 2 Vol. 9; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (69)

Purinergic signaling during Porphyromonas gingivalis infection journal August 2016
Mining metagenomic data for novel domains: BACON, a new carbohydrate-binding module journal April 2010
Identification and characterization of the genes encoding a unique surface (S-) layer of Tannerella forsythia journal April 2006
Role of a Tannerella forsythia exopolysaccharide synthesis operon in biofilm development journal April 2007
Basic local alignment search tool journal October 1990
Structural divergence of the rotary ATPases journal March 2011
A framework for human microbiome research journal June 2012
Genomic sequencing of uncultured microorganisms from single cells journal August 2012
Phase-variable expression of a family of glycoproteins imparts a dynamic surface to a symbiont in its human intestinal ecosystem journal February 2007
UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota journal March 2013
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing journal May 2012
IMG ER: a system for microbial genome annotation expert review and curation journal June 2009
The COG database: a tool for genome-scale analysis of protein functions and evolution journal January 2000
RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics journal June 2012
Uncultivated Tannerella BU045 and BU063 are slim segmented filamentous rods of high prevalence but low abundance in inflammatory disease-associated dental plaques journal November 2007
Loss of adherence ability to human gingival epithelial cells in S-layer protein-deficient mutants of Tannerella forsythensis journal March 2007
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs journal February 2008
BLAT---The BLAST-Like Alignment Tool journal March 2002
Porphyromonas gingivalis Vesicles Enhance Attachment, and the Leucine-Rich Repeat BspA Protein Is Required for Invasion of Epithelial Cells by "Tannerella forsythia" journal August 2006
Role of Tannerella forsythia NanH Sialidase in Epithelial Cell Attachment journal November 2010
Antivirulence Genes: Insights into Pathogen Evolution through Gene Loss journal October 2012
Toll-Like Receptor 2-Mediated Interleukin-8 Expression in Gingival Epithelial Cells by the Tannerella forsythia Leucine-Rich Repeat Protein BspA journal October 2007
Cloning, expression, and sequencing of a protease gene from Bacteroides forsythus ATCC 43037 in Escherichia coli. journal January 1997
Cloning, Expression, and Sequencing of a Cell Surface Antigen Containing a Leucine-Rich Repeat Motif from Bacteroides forsythus ATCC 43037 journal December 1998
Culture-Independent Identification of Periodontitis-Associated Porphyromonas and Tannerella Populations by Targeted Molecular Analysis journal December 2004
SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler journal December 2012
CORE: A Phylogenetically-Curated 16S rDNA Database of the Core Oral Microbiome journal April 2011
Correlation Network Analysis Applied to Complex Biofilm Communities journal December 2011
The “Most Wanted” Taxa from the Human Microbiome for Whole Genome Sequencing journal July 2012
A novel matrix metalloprotease-like enzyme (karilysin) of the periodontal pathogen Tannerella forsythia ATCC 43037 journal January 2010
A Metalloproteinase Karilysin Present in the Majority of Tannerella forsythia Isolates Inhibits All Pathways of the Complement System journal January 2012
Mesobacillus aurantius sp. nov., isolated from an orange-colored pond near a solar saltern journal January 2021
Basic local alignment search tool journal October 1990
Pathogenicity islands: the tip of the iceberg journal June 2001
Glucose toxicity effect and accumulation of methylglyoxal by the periodontal anaerobe Bacteroides forsythus journal February 2004
Isolation and identification of a cytopathic activity in Tannerella forsythia journal December 2006
Structural divergence of the rotary ATPases journal March 2011
Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing journal December 2011
The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation journal January 2013
A bacterial glycan core linked to surface (S)-layer proteins modulates host immunity through Th17 suppression journal September 2012
Efficient de novo assembly of single-cell bacterial genomes from short-read data sets journal September 2011
Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth journal July 2007
Characterization and Scope of S-layer Protein O -Glycosylation in Tannerella forsythia journal September 2011
Artemis: sequence visualization and annotation journal October 2000
Description of Alloprevotella rava gen. nov., sp. nov., isolated from the human oral cavity, and reclassification of Prevotella tannerae Moore et al. 1994 as Alloprevotella tannerae gen. nov., comb. nov. journal June 2012
Role of sialidase in glycoprotein utilization by Tannerella forsythia journal November 2011
BLAT---The BLAST-Like Alignment Tool journal March 2002
Microbial complexes in subgingival plaque journal February 1998
Virulence mechanisms of Tannerella forsythia: Virulence mechanisms of Tannerella forsythia journal August 2010
Pro-inflammatory cytokine production from normal human fibroblasts is induced by Tannerella forsythia detaching factor journal April 2008
Porphyromonas gingivalis Vesicles Enhance Attachment, and the Leucine-Rich Repeat BspA Protein Is Required for Invasion of Epithelial Cells by "Tannerella forsythia" journal August 2006
Role of Tannerella forsythia NanH Sialidase in Epithelial Cell Attachment journal November 2010
Rat Model of Polymicrobial Infection, Immunity, and Alveolar Bone Resorption in Periodontal Disease journal January 2007
Antivirulence Genes: Insights into Pathogen Evolution through Gene Loss journal October 2012
The Surface Layer of Tannerella forsythia Contributes to Serum Resistance and Oral Bacterial Coaggregation journal January 2013
Toll-Like Receptor 2-Mediated Interleukin-8 Expression in Gingival Epithelial Cells by the Tannerella forsythia Leucine-Rich Repeat Protein BspA journal October 2007
Cloning, expression, and sequencing of a protease gene from Bacteroides forsythus ATCC 43037 in Escherichia coli. journal January 1997
Cloning, Expression, and Sequencing of a Cell Surface Antigen Containing a Leucine-Rich Repeat Motif from Bacteroides forsythus ATCC 43037 journal December 1998
A Novel Sialic Acid Utilization and Uptake System in the Periodontal Pathogen Tannerella forsythia journal February 2010
The Human Oral Microbiome journal July 2010
Association of Bacteroides forsythus and a Novel Bacteroides Phylotype with Periodontitis journal March 2002
Culture-Independent Identification of Periodontitis-Associated Porphyromonas and Tannerella Populations by Targeted Molecular Analysis journal December 2004
Bacterial Persistence and Toxin-Antitoxin Loci journal October 2012
Tannerella forsythia -induced Alveolar Bone Loss in Mice Involves Leucine-rich-repeat BspA Protein journal May 2005
SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler journal December 2012
Evidence of Selection upon Genomic GC-Content in Bacteria journal September 2010
Multiple Single-Cell Genomes Provide Insight into Functions of Uncultured Deltaproteobacteria in the Human Oral Cavity journal March 2013
Prediction of a caspase-like fold in Tannerella forsythia virulence factor PrtH journal May 2009
Uncultivated Tannerella BU045 and BU063 are slim segmented filamentous rods of high prevalence but low abundance in inflammatory disease-associated dental plaques text January 2007

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Metabolic network percolation quantifies biosynthetic capabilities across the human oral microbiome journal June 2019
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High-Resolution Taxonomic Profiling of the Subgingival Microbiome for Biomarker Discovery and Periodontitis Diagnosis journal December 2014
Genomics of the Uncultivated, Periodontitis-Associated Bacterium Tannerella sp. BU045 (Oral Taxon 808) journal June 2018
First Cultivation of Health-Associated Tannerella sp. HOT-286 (BU063) journal July 2016
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A General Protein O-Glycosylation Gene Cluster Encodes the Species-Specific Glycan of the Oral Pathogen Tannerella forsythia: O-Glycan Biosynthesis and Immunological Implications journal August 2018