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

Campbell, Alisha G.; Campbell, James H.; Schwientek, Patrick; Woyke, Tanja; Sczyrba, Alexander; Allman, Steve; Beall, Clifford J.; Griffen, Ann; Leys, Eugene; Podar, Mircea; Horn, Matthias

doi:10.1371/journal.pone.0059361

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

DOI:https://doi.org/10.1371/journal.pone.0059361· OSTI ID:1627591

Campbell, Alisha G. ^[1]; Campbell, James H. ^[2]; Schwientek, Patrick ^[3]; Woyke, Tanja ^[3]; Sczyrba, Alexander ^[3]; Allman, Steve ^[2]; Beall, Clifford J. ^[4]; Griffen, Ann ^[4]; Leys, Eugene ^[4]; Podar, Mircea ^[5]; Horn, Matthias

Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology Program; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; DOE/OSTI
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
The Ohio State Univ., Columbus, OH (United States). College of Dentistry
Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology Program; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology

Despite a long history of investigation, many bacteria associated with the human oral cavity have yet to be cultured. Studies that correlate the presence or abundance of uncultured species with oral health or disease highlight the importance of these community members. Thus, we sequenced several single-cell genomic amplicons from Desulfobulbus and Desulfovibrio (class Deltaproteobacteria) to better understand their function within the human oral community and their association with periodontitis, as well as other systemic diseases. Genomic data from oral Desulfobulbus and Desulfovibrio species were compared to other available deltaproteobacterial genomes, including from a subset of host-associated species. While both groups share a large number of genes with other environmental Deltaproteobacteria genomes, they encode a wide array of unique genes that appear to function in survival in a host environment. Many of these genes are similar to virulence and host adaptation factors of known human pathogens, suggesting that the oral Deltaproteobacteria have the potential to play a role in the etiology of periodontal disease.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231; AC05-00OR22725

OSTI ID:: 1627591

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 3 Vol. 8; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (92)

Identification of Pasteurella multocida virulence genes in a septicemic mouse model using signature-tagged mutagenesis Fuller, Troy E.; Kennedy, Michael J.; Lowery, David E. Microbial Pathogenesis, Vol. 29, Issue 1 https://doi.org/10.1006/mpat.2000.0365	journal	July 2000
Characterization of the Determinant (traB) Encoding Sex Pheromone Shutdown by the Hemolysin/Bacteriocin Plasmid pAD1 in Enterococcus faecalis An, Florence Y.; Clewell, Don B. Plasmid, Vol. 31, Issue 2 https://doi.org/10.1006/plas.1994.1023	journal	March 1994
Periodontitis and diabetes: a two-way relationship Preshaw, P. M.; Alba, A. L.; Herrera, D. Diabetologia, Vol. 55, Issue 1 https://doi.org/10.1007/s00125-011-2342-y	journal	November 2011
The Influence of Iron Availability on Human Salivary Microbial Community Composition Wang, Renke; Kaplan, Aida; Guo, Lihong Microbial Ecology, Vol. 64, Issue 1 https://doi.org/10.1007/s00248-012-0013-2	journal	February 2012
Helicobacter pylori mutants defective in the clpP ATP-dependant protease and the chaperone clpA display reduced macrophage and murine survival Loughlin, Michael F.; Arandhara, Victoria; Okolie, Charles Microbial Pathogenesis, Vol. 46, Issue 1 https://doi.org/10.1016/j.micpath.2008.10.004	journal	January 2009
Improved 16S rRNA-targeted probe set for analysis of sulfate-reducing bacteria by fluorescence in situ hybridization Lücker, Sebastian; Steger, Doris; Kjeldsen, Kasper Urup Journal of Microbiological Methods, Vol. 69, Issue 3 https://doi.org/10.1016/j.mimet.2007.02.009	journal	June 2007
Associations between periodontal diseases and systemic diseases: A review of the inter-relationships and interactions with diabetes, respiratory diseases, cardiovascular diseases and osteoporosis Kuo, Lan-Chen; Polson, Alan M.; Kang, Taeheon Public Health, Vol. 122, Issue 4 https://doi.org/10.1016/j.puhe.2007.07.004	journal	April 2008
Characterization of the Desulfovibrio desulfuricans ATCC 27774 DsrMKJOP ComplexA Membrane-Bound Redox Complex Involved in the Sulfate Respiratory Pathway Pires, Ricardo H.; Venceslau, Sofia S.; Morais, Francisco Biochemistry, Vol. 45, Issue 1 https://doi.org/10.1021/bi0515265	journal	January 2006
The human microbiome: there is much left to do Ley, Ruth Nature, Vol. 606, Issue 7914 https://doi.org/10.1038/d41586-022-01610-5	journal	June 2022
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
Enterotypes of the human gut microbiome Arumugam, Manimozhiyan; Raes, Jeroen; Pelletier, Eric Nature, Vol. 473, Issue 7346 https://doi.org/10.1038/nature09944	journal	April 2011
Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa Mougous, Joseph D.; Gifford, Casey A.; Ramsdell, Talia L. Nature Cell Biology, Vol. 9, Issue 7 https://doi.org/10.1038/ncb1605	journal	June 2007
The versatile bacterial type IV secretion systems Cascales, Eric; Christie, Peter J. Nature Reviews Microbiology, Vol. 1, Issue 2 https://doi.org/10.1038/nrmicro753	journal	November 2003
Shifting the genomic gold standard for the prokaryotic species definition Richter, Michael; Rosselló-Móra, Ramon Proceedings of the National Academy of Sciences, Vol. 106, Issue 45 https://doi.org/10.1073/pnas.0906412106	journal	October 2009
Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen Ajdic, D.; McShan, W. M.; McLaughlin, R. E. Proceedings of the National Academy of Sciences, Vol. 99, Issue 22 https://doi.org/10.1073/pnas.172501299	journal	October 2002
Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence Winther-Larsen, H. C.; Hegge, F. T.; Wolfgang, M. Proceedings of the National Academy of Sciences, Vol. 98, Issue 26 https://doi.org/10.1073/pnas.261574998	journal	December 2001
IMG: the integrated microbial genomes database and comparative analysis system Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1044	journal	December 2011
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Systematic Biology, Vol. 59, Issue 3 https://doi.org/10.1093/sysbio/syq010	journal	March 2010
Isolation of Desulfomicrobium orale sp. nov. and Desulfovibrio strain NY682, oral sulfate-reducing bacteria involved in human periodontal disease Langendijk, P. S.; Kulik, E. M.; Sandmeier, H. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 51, Issue 3 https://doi.org/10.1099/00207713-51-3-1035	journal	May 2001
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs Zerbino, D. R.; Birney, E. Genome Research, Vol. 18, Issue 5 https://doi.org/10.1101/gr.074492.107	journal	February 2008
The Application of Ultraviolet Irradiation to Exogenous Sources of DNA in Plasticware and Water for the Amplification of Low Copy Number DNA Tamariz, Jeannie; Voynarovska, Kristina; Prinz, Mechthild Journal of Forensic Sciences, Vol. 51, Issue 4 https://doi.org/10.1111/j.1556-4029.2006.00172.x	journal	July 2006
Periodontal diseases and health: Consensus Report of the Sixth European Workshop on Periodontology Kinane, Denis; Bouchard, Phillippe Journal of Clinical Periodontology, Vol. 35 https://doi.org/10.1111/j.1600-051x.2008.01278.x	journal	September 2008
Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology Hajishengallis, G.; Lamont, R. J. Molecular Oral Microbiology, Vol. 27, Issue 6 https://doi.org/10.1111/j.2041-1014.2012.00663.x	journal	September 2012
Potential for Chemolithoautotrophy Among Ubiquitous Bacteria Lineages in the Dark Ocean Swan, B. K.; Martinez-Garcia, M.; Preston, C. M. Science, Vol. 333, Issue 6047 https://doi.org/10.1126/science.1203690	journal	September 2011
Double Labeling of Oligonucleotide Probes for Fluorescence In Situ Hybridization (DOPE-FISH) Improves Signal Intensity and Increases rRNA Accessibility Stoecker, K.; Dorninger, C.; Daims, H. Applied and Environmental Microbiology, Vol. 76, Issue 3 https://doi.org/10.1128/aem.02456-09	journal	December 2009
Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Amann, R. I.; Binder, B. J.; Olson, R. J. Applied and Environmental Microbiology, Vol. 56, Issue 6 https://doi.org/10.1128/aem.56.6.1919-1925.1990	journal	January 1990
Oligonucleotide Microarray for 16S rRNA Gene-Based Detection of All Recognized Lineages of Sulfate-Reducing Prokaryotes in the Environment Loy, A.; Lehner, A.; Lee, N. Applied and Environmental Microbiology, Vol. 68, Issue 10 https://doi.org/10.1128/aem.68.10.5064-5081.2002	journal	October 2002
Identification of Specific In Vivo-Induced (ivi) Genes in Yersinia ruckeri and Analysis of Ruckerbactin, a Catecholate Siderophore Iron Acquisition System Fernández, L.; Márquez, I.; Guijarro, J. A. Applied and Environmental Microbiology, Vol. 70, Issue 9 https://doi.org/10.1128/aem.70.9.5199-5207.2004	journal	September 2004
FNR Is a Global Regulator of Virulence and Anaerobic Metabolism in Salmonella enterica Serovar Typhimurium (ATCC 14028s) Fink, R. C.; Evans, M. R.; Porwollik, S. Journal of Bacteriology, Vol. 189, Issue 6 https://doi.org/10.1128/jb.00726-06	journal	January 2007
Role of FtsEX in Cell Division of Escherichia coli: Viability of ftsEX Mutants Is Dependent on Functional SufI or High Osmotic Strength Reddy, Manjula Journal of Bacteriology, Vol. 189, Issue 1 https://doi.org/10.1128/jb.01347-06	journal	October 2006
Role of the Clp System in Stress Tolerance, Biofilm Formation, and Intracellular Invasion in Porphyromonas gingivalis Capestany, Cindy A.; Tribble, Gena D.; Maeda, Kazuhiko Journal of Bacteriology, Vol. 190, Issue 4 https://doi.org/10.1128/jb.01632-07	journal	December 2007
16S ribosomal DNA amplification for phylogenetic study. Weisburg, W. G.; Barns, S. M.; Pelletier, D. A. Journal of Bacteriology, Vol. 173, Issue 2 https://doi.org/10.1128/jb.173.2.697-703.1991	journal	January 1991
Desulfovibrio fairfieldensis Bacteremia Associated with Choledocholithiasis and Endoscopic Retrograde Cholangiopancreatography Pimentel, J. D.; Chan, R. C. Journal of Clinical Microbiology, Vol. 45, Issue 8 https://doi.org/10.1128/jcm.00969-07	journal	June 2007
Identification of Candidate Periodontal Pathogens and Beneficial Species by Quantitative 16S Clonal Analysis Kumar, P. S.; Griffen, A. L.; Moeschberger, M. L. Journal of Clinical Microbiology, Vol. 43, Issue 8 https://doi.org/10.1128/jcm.43.8.3944-3955.2005	journal	August 2005
Activity of sulfate-reducing bacteria in human periodontal pocket Boopathy, R.; Robichaux, M.; LaFont, D. Canadian Journal of Microbiology, Vol. 48, Issue 12 https://doi.org/10.1139/w02-104	journal	December 2002
New Bacterial Species Associated with Chronic Periodontitis Kumar, P. S.; Griffen, A. L.; Barton, J. A. Journal of Dental Research, Vol. 82, Issue 5 https://doi.org/10.1177/154405910308200503	journal	May 2003
Detection of gene pathways with predictive power for breast cancer prognosis Ma, Shuangge; Kosorok, Michael R. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-1	journal	January 2010
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008
Bacterial Toxin–Antitoxin Systems: More Than Selfish Entities? Van Melderen, Laurence; Saavedra De Bast, Manuel PLoS Genetics, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pgen.1000437	journal	March 2009
Assembling the Marine Metagenome, One Cell at a Time Woyke, Tanja; Xie, Gary; Copeland, Alex PLoS ONE, Vol. 4, Issue 4 https://doi.org/10.1371/journal.pone.0005299	journal	April 2009
Whole Genome Amplification and De novo Assembly of Single Bacterial Cells Rodrigue, Sébastien; Malmstrom, Rex R.; Berlin, Aaron M. PLoS ONE, Vol. 4, Issue 9 https://doi.org/10.1371/journal.pone.0006864	journal	September 2009
Oxidation of H2, organic compounds and inorganic sulfur compounds coupled to reduction of O2 or nitrate by sulfate-reducing bacteria Dannenberg, Simone; Kroder, Michael; Dilling, Waltraud Archives of Microbiology, Vol. 158, Issue 2 https://doi.org/10.1007/BF00245211	journal	July 1992
Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids II. Incomplete oxidation of propionate by Desulfobulbus propionicus gen. nov., sp. nov. Widdel, Friedrich; Pfennig, Norbert Archives of Microbiology, Vol. 131, Issue 4 https://doi.org/10.1007/BF00411187	journal	June 1982
Periodontal Disease and Coronary Heart Disease Incidence: A Systematic Review and Meta-analysis Humphrey, Linda L.; Fu, Rongwei; Buckley, David I. Journal of General Internal Medicine, Vol. 23, Issue 12 https://doi.org/10.1007/s11606-008-0787-6	journal	September 2008
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
Specificity of the oral microflora in dentinal caries, endodontic infections and periodontitis Wade, W. G.; Munson, M. A.; de Lillo, A. International Congress Series, Vol. 1284 https://doi.org/10.1016/j.ics.2005.06.097	journal	September 2005
Periodontitis is associated with altered plasma fatty acids and cardiovascular risk markers Ramirez-Tortosa, M. C.; Quiles, J. L.; Battino, M. Nutrition, Metabolism and Cardiovascular Diseases, Vol. 20, Issue 2 https://doi.org/10.1016/j.numecd.2009.03.003	journal	February 2010
The oral microbiome in health and disease Wade, William G. Pharmacological Research, Vol. 69, Issue 1 https://doi.org/10.1016/j.phrs.2012.11.006	journal	March 2013
Isolation of the provisionally named Desulfovibrio fairfieldensis from human periodontal pockets Loubinoux, J.; Bisson-Boutelliez, C.; Miller, N. Oral Microbiology and Immunology, Vol. 17, Issue 5 https://doi.org/10.1034/j.1399-302X.2002.170510.x	journal	October 2002
Sulfate-reducing bacteria in association with human periodontitis Langendijk, P. S.; Hanssen, J. T. J.; Van der Hoeven, J. S. Journal of Clinical Periodontology, Vol. 27, Issue 12 https://doi.org/10.1034/j.1600-051x.2000.027012943.x	journal	December 2000
Crystal structure of the Haemophilus influenzae Hap adhesin reveals an intercellular oligomerization mechanism for bacterial aggregation: Structural framework for bacterial aggregation Meng, Guoyu; Spahich, Nicole; Kenjale, Roma The EMBO Journal, Vol. 30, Issue 18 https://doi.org/10.1038/emboj.2011.279	journal	August 2011
The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation Abusleme, Loreto; Dupuy, Amanda K.; Dutzan, Nicolás The ISME Journal, Vol. 7, Issue 5 https://doi.org/10.1038/ismej.2012.174	journal	January 2013
Crystal structure of bacterial multidrug efflux transporter AcrB Murakami, Satoshi; Nakashima, Ryosuke; Yamashita, Eiki Nature, Vol. 419, Issue 6907 https://doi.org/10.1038/nature01050	journal	October 2002
Structure, function and diversity of the healthy human microbiome No authors listed Nature, Vol. 486, Issue 7402, p. 207-214 https://doi.org/10.1038/nature11234	journal	June 2012
Periodontitis: a polymicrobial disruption of host homeostasis Darveau, Richard P. Nature Reviews Microbiology, Vol. 8, Issue 7 https://doi.org/10.1038/nrmicro2337	journal	June 2010
Salmonella SsrB activates a global regulon of horizontally acquired genes: Salmonella SsrB activates a global regulon of horizontally acquired genes Worley, Micah J.; Ching, Katherine H. L.; Heffron, Fred Molecular Microbiology, Vol. 36, Issue 3 https://doi.org/10.1046/j.1365-2958.2000.01902.x	journal	May 2000
Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes Seshadri, R.; Myers, G. S. A.; Tettelin, H. Proceedings of the National Academy of Sciences, Vol. 101, Issue 15 https://doi.org/10.1073/pnas.0307639101	journal	April 2004
Matching phylogeny and metabolism in the uncultured marine bacteria, one cell at a time Stepanauskas, R.; Sieracki, M. E. Proceedings of the National Academy of Sciences, Vol. 104, Issue 21 https://doi.org/10.1073/pnas.0700496104	journal	May 2007
Digital MDA for enumeration of total nucleic acid contamination Blainey, P. C.; Quake, S. R. Nucleic Acids Research, Vol. 39, Issue 4 https://doi.org/10.1093/nar/gkq1074	journal	November 2010
The Pfam protein families database Punta, M.; Coggill, P. C.; Eberhardt, R. Y. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1065	journal	November 2011
clpB, a class III heat-shock gene regulated by CtsR, is involved in thermotolerance and virulence of Enterococcus faecalis de Oliveira, Naira Elane Moreira; Abranches, Jaqueline; Gaca, Anthony O. Microbiology, Vol. 157, Issue 3 https://doi.org/10.1099/mic.0.041897-0	journal	March 2011
Type I and type IV pili of Xylella fastidiosa affect twitching motility, biofilm formation and cell–cell aggregation Li, Yaxin.; Hao, Guixia.; Galvani, Cheryl D. Microbiology, Vol. 153, Issue 3 https://doi.org/10.1099/mic.0.2006/002311-0	journal	March 2007
Mauve: Multiple Alignment of Conserved Genomic Sequence With Rearrangements Darling, A. C. E. Genome Research, Vol. 14, Issue 7 https://doi.org/10.1101/gr.2289704	journal	June 2004
An ABC transporter and an outer membrane lipoprotein participate in posttranslational activation of type VI secretion in Pseudomonas aeruginosa: Trans-membrane activation of T6S Casabona, Maria G.; Silverman, Julie M.; Sall, Khady M. Environmental Microbiology, Vol. 15, Issue 2 https://doi.org/10.1111/j.1462-2920.2012.02816.x	journal	July 2012
Acetogenesis from pyruvate by Desulfotomaculum thermobenzoicum and differences in pyruvate metabolism among three sulfate-reducing bacteria in the absence of sulfate Tasaki, Masaharu; Kamagata, Yoichi; Nakamura, Kazunori FEMS Microbiology Letters, Vol. 106, Issue 3 https://doi.org/10.1111/j.1574-6968.1993.tb05973.x	journal	February 1993
Periodontal diseases and health: Consensus Report of the Sixth European Workshop on Periodontology Kinane, Denis; Bouchard, Phillippe Journal of Clinical Periodontology, Vol. 35 https://doi.org/10.1111/j.1600-051X.2008.01278.x	journal	September 2008
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Double Labeling of Oligonucleotide Probes for Fluorescence In Situ Hybridization (DOPE-FISH) Improves Signal Intensity and Increases rRNA Accessibility Stoecker, K.; Dorninger, C.; Daims, H. Applied and Environmental Microbiology, Vol. 76, Issue 3 https://doi.org/10.1128/AEM.02456-09	journal	December 2009
Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Amann, R. I.; Binder, B. J.; Olson, R. J. Applied and Environmental Microbiology, Vol. 56, Issue 6 https://doi.org/10.1128/AEM.56.6.1919-1925.1990	journal	January 1990
Oligonucleotide Microarray for 16S rRNA Gene-Based Detection of All Recognized Lineages of Sulfate-Reducing Prokaryotes in the Environment Loy, A.; Lehner, A.; Lee, N. Applied and Environmental Microbiology, Vol. 68, Issue 10 https://doi.org/10.1128/AEM.68.10.5064-5081.2002	journal	October 2002
Identification of Specific In Vivo-Induced (ivi) Genes in Yersinia ruckeri and Analysis of Ruckerbactin, a Catecholate Siderophore Iron Acquisition System Fernández, L.; Márquez, I.; Guijarro, J. A. Applied and Environmental Microbiology, Vol. 70, Issue 9 https://doi.org/10.1128/AEM.70.9.5199-5207.2004	journal	September 2004
Inactivation of clpB in the Pathogen Leptospira interrogans Reduces Virulence and Resistance to Stress Conditions Lourdault, Kristel; Cerqueira, Gustavo M.; Wunder, Elsio A. Infection and Immunity, Vol. 79, Issue 9 https://doi.org/10.1128/IAI.05168-11	journal	July 2011
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
Rcs and PhoPQ Regulatory Overlap in the Control of Salmonella enterica Virulence García-Calderón, Clara B.; Casadesús, Josep; Ramos-Morales, Francisco Journal of Bacteriology, Vol. 189, Issue 18 https://doi.org/10.1128/JB.00640-07	journal	July 2007
FNR Is a Global Regulator of Virulence and Anaerobic Metabolism in Salmonella enterica Serovar Typhimurium (ATCC 14028s) Fink, R. C.; Evans, M. R.; Porwollik, S. Journal of Bacteriology, Vol. 189, Issue 6 https://doi.org/10.1128/JB.00726-06	journal	January 2007
Role of FtsEX in Cell Division of Escherichia coli: Viability of ftsEX Mutants Is Dependent on Functional SufI or High Osmotic Strength Reddy, Manjula Journal of Bacteriology, Vol. 189, Issue 1 https://doi.org/10.1128/JB.01347-06	journal	October 2006
Outer Membrane Components of the Tad (Tight Adherence) Secreton of Aggregatibacter actinomycetemcomitans Clock, Sarah A.; Planet, Paul J.; Perez, Brenda A. Journal of Bacteriology, Vol. 190, Issue 3 https://doi.org/10.1128/JB.01347-07	journal	November 2007
Role of the Clp System in Stress Tolerance, Biofilm Formation, and Intracellular Invasion in Porphyromonas gingivalis Capestany, Cindy A.; Tribble, Gena D.; Maeda, Kazuhiko Journal of Bacteriology, Vol. 190, Issue 4 https://doi.org/10.1128/JB.01632-07	journal	December 2007
Quantitative Analysis of Three Hydrogenotrophic Microbial Groups, Methanogenic Archaea, Sulfate-Reducing Bacteria, and Acetogenic Bacteria, within Plaque Biofilms Associated with Human Periodontal Disease Vianna, M. E.; Holtgraewe, S.; Seyfarth, I. Journal of Bacteriology, Vol. 190, Issue 10 https://doi.org/10.1128/JB.01861-07	journal	March 2008
Genome Sequence and Analysis of the Oral Bacterium Fusobacterium nucleatum Strain ATCC 25586 Kapatral, Vinayak; Anderson, Iain; Ivanova, Natalia Journal of Bacteriology, Vol. 184, Issue 7 https://doi.org/10.1128/JB.184.7.2005-2018.2002	journal	April 2002
Complete Genome Sequence of the Oral Pathogenic Bacterium Porphyromonas gingivalis Strain W83 Nelson, Karen E.; Fleischmann, Robert D.; DeBoy, Robert T. Journal of Bacteriology, Vol. 185, Issue 18 https://doi.org/10.1128/JB.185.18.5591-5601.2003	journal	September 2003
Identification of New Flagellar Genes of Salmonella enterica Serovar Typhimurium Frye, Jonathan; Karlinsey, Joyce E.; Felise, Heather R. Journal of Bacteriology, Vol. 188, Issue 6 https://doi.org/10.1128/JB.188.6.2233-2243.2006	journal	March 2006
Desulfovibrio fairfieldensis Bacteremia Associated with Choledocholithiasis and Endoscopic Retrograde Cholangiopancreatography Pimentel, J. D.; Chan, R. C. Journal of Clinical Microbiology, Vol. 45, Issue 8 https://doi.org/10.1128/JCM.00969-07	journal	June 2007
Bacteremia Caused by a Strain ofDesulfovibrio Related to the Provisionally NamedDesulfovibrio fairfieldensis Loubinoux, Julien; Mory, Francine; Pereira, Ines A. C. Journal of Clinical Microbiology, Vol. 38, Issue 2 https://doi.org/10.1128/JCM.38.2.931-934.2000	journal	January 2000
Identification of Candidate Periodontal Pathogens and Beneficial Species by Quantitative 16S Clonal Analysis Kumar, P. S.; Griffen, A. L.; Moeschberger, M. L. Journal of Clinical Microbiology, Vol. 43, Issue 8 https://doi.org/10.1128/JCM.43.8.3944-3955.2005	journal	August 2005
The Biochemistry and Genetics of Capsular Polysaccharide Production in Bacteria Roberts, Ian S. Annual Review of Microbiology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.micro.50.1.285	journal	October 1996
Oxygen Respiration by Desulfovibrio Species Cypionka, Heribert Annual Review of Microbiology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.micro.54.1.827	journal	October 2000
Type IV Pili and Twitching Motility Mattick, John S. Annual Review of Microbiology, Vol. 56, Issue 1 https://doi.org/10.1146/annurev.micro.56.012302.160938	journal	October 2002
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Complete genome sequence of Desulfarculus baarsii type strain (2st14T) Sun, Hui; Spring, Stefan; Lapidus, Alla Standards in Genomic Sciences, Vol. 3, Issue 3 https://doi.org/10.4056/sigs.1243258	journal	January 2010
Complete genome sequence of Desulfobulbus propionicus type strain (1pr3T) Pagani, Ioanna; Lapidus, Alla; Nolan, Matt Standards in Genomic Sciences, Vol. 4, Issue 1 https://doi.org/10.4056/sigs.1613929	journal	February 2011

Cited By (13)

RiboFR-Seq: a novel approach to linking 16S rRNA amplicon profiles to metagenomes Zhang, Yanming; Ji, Peifeng; Wang, Jinfeng Nucleic Acids Research, Vol. 44, Issue 10 https://doi.org/10.1093/nar/gkw165	journal	March 2016
Enrichment of Root Endophytic Bacteria from Populus deltoides and Single-Cell-Genomics Analysis Utturkar, Sagar M.; Cude, W. Nathan; Robeson, Michael S. Applied and Environmental Microbiology, Vol. 82, Issue 18 https://doi.org/10.1128/aem.01285-16	journal	July 2016
Insights into the Evolution of Host Association through the Isolation and Characterization of a Novel Human Periodontal Pathobiont, Desulfobulbus oralis Cross, Karissa L.; Chirania, Payal; Xiong, Weili mBio, Vol. 9, Issue 2 https://doi.org/10.1128/mbio.02061-17	journal	March 2018
Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments Bird, Jordan T.; Tague, Eric D.; Zinke, Laura mBio, Vol. 10, Issue 2 https://doi.org/10.1128/mbio.02376-18	journal	April 2019
Genomics of the Uncultivated, Periodontitis-Associated Bacterium Tannerella sp. BU045 (Oral Taxon 808) Beall, Clifford J.; Campbell, Alisha G.; Griffen, Ann L. mSystems, Vol. 3, Issue 3 https://doi.org/10.1128/msystems.00018-18	journal	June 2018
Hidden Diversity in Honey Bee Gut Symbionts Detected by Single-Cell Genomics Engel, Philipp; Stepanauskas, Ramunas; Moran, Nancy A. PLoS Genetics, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pgen.1004596	journal	September 2014
In vitro Increased Respiratory Activity of Selected Oral Bacteria May Explain Competitive and Collaborative Interactions in the Oral Microbiome Hernandez-Sanabria, Emma; Slomka, Vera; Herrero, Esteban R. Frontiers in Cellular and Infection Microbiology, Vol. 7 https://doi.org/10.3389/fcimb.2017.00235	journal	June 2017
The Role of Oral Cavity Biofilm on Metallic Biomaterial Surface Destruction–Corrosion and Friction Aspects Mystkowska, Joanna; Niemirowicz-Laskowska, Katarzyna; Łysik, Dawid International Journal of Molecular Sciences, Vol. 19, Issue 3 https://doi.org/10.3390/ijms19030743	journal	March 2018
Metabolic network percolation quantifies biosynthetic capabilities across the human oral microbiome Bernstein, David B.; Dewhirst, Floyd E.; Segrè, Daniel eLife, Vol. 8 https://doi.org/10.7554/elife.39733	journal	June 2019
Targeted isolation and cultivation of uncultivated bacteria by reverse genomics Cross, Karissa L.; Campbell, James H.; Balachandran, Manasi Nature Biotechnology, Vol. 37, Issue 11 https://doi.org/10.1038/s41587-019-0260-6	journal	September 2019
A Phase II Study of Neoadjuvant Stereotactic Radiosurgery for Large Brain Metastases: Clinical Trial Protocol Takami, Hirokazu; Nassiri, Farshad; Moraes, Fabio Y. Neurosurgery, Vol. 87, Issue 2 https://doi.org/10.1093/neuros/nyz442	journal	November 2019
High-Resolution Taxonomic Profiling of the Subgingival Microbiome for Biomarker Discovery and Periodontitis Diagnosis Szafranski, Szymon P.; Wos-Oxley, Melissa L.; Vilchez-Vargas, Ramiro Applied and Environmental Microbiology, Vol. 81, Issue 3 https://doi.org/10.1128/aem.03534-14	journal	December 2014
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

Similar Records

Insights into the Evolution of Host Association through the Isolation and Characterization of a Novel Human Periodontal Pathobiont, Desulfobulbus oralis

Journal Article · Tue Mar 13 00:00:00 EDT 2018 · mBio (Online) · OSTI ID:1435265

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

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

Journal Article · Tue Jun 05 00:00:00 EDT 2018 · mSystems · OSTI ID:1468065

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Science & Technology - Other Topics

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

Citation Formats

References (92)

Cited By (13)

Similar Records

Related Subjects