W G Wade

King's College London, Londinium, England, United Kingdom

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Publications (125)356.86 Total impact

  • William G. Wade
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    ABSTRACT: The human mouth is colonised by a diverse community of microorganisms including bacteria, archaea, fungi, protozoa and viruses. The mouth is unusual in the body in that members of the normal microbiota are associated with disease, particularly dental caries and the periodontal diseases. Culture-independent methods targeting the 16S ribosomal RNA have been developed which have enabled the comprehensive description of the oral microbiome. The Human Oral Microbiome Database (HOMD), a list of oral bacteria with a description of their characteristics and genomic information, together with a 16S rRNA identification tool is available on-line at www.homd.org. A small number of phylotypes belonging to the genus Methanobrevibacter are the only representatives of the Archaea. Fifteen phyla from the domain Bacteria are found in the mouth but 96% of sequences are accounted for by six phyla: Actinobacteria, Bacteroidetes, Firmicutes, Fusobacteria, Proteobacteria and Spirochaetes. The adoption of next generation sequencing techniques for community profiling has greatly increased the depth of coverage of analyses of the human microbiome. One reason for the uncultivability of oral bacteria is that organisms naturally grow in a multi-species biofilm and share nutrients and communicate with other members of the community. Colony hybridisation enrichment of mixed laboratory cultures has been successfully used to culture a previously uncultured member of the recently described phylum Synergistetes, which has subsequently been named Fretibacterium fastidiosum. Recent developments in microbiomics, metagenomics and transcriptomics will enable a new understanding of host-bacterial interactions in oral disease and should lead to new methods of prevention and treatment.
    Journal of Oral Biosciences 01/2013; 55(3):143–148.
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    ABSTRACT: Current knowledge of the microbial composition of dental plaque in early gingivitis is based largely on microscopy and cultural methods, which do not provide a comprehensive description of oral microbial communities. This study used 454-pyrosequencing of the V1-V3 region of 16S rRNA genes (approximately 500 bp), and bacterial culture, to characterize the composition of plaque during the transition from periodontal health to gingivitis. A total of 20 healthy volunteers abstained from oral hygiene for two weeks, allowing plaque to accumulate and gingivitis to develop. Plaque samples were analyzed at baseline, and after one and two weeks. In addition, plaque samples from 20 chronic periodontitis patients were analyzed for cross-sectional comparison to the experimental gingivitis cohort. All of the healthy volunteers developed gingivitis after two weeks. Pyrosequencing yielded a final total of 344 267 sequences after filtering, with a mean length of 354 bases, that were clustered into an average of 299 species-level Operational Taxonomic Units (OTUs) per sample. Principal coordinates analysis (PCoA) plots revealed significant shifts in the bacterial community structure of plaque as gingivitis was induced, and community diversity increased significantly after two weeks. Changes in the relative abundance of OTUs during the transition from health to gingivitis were correlated to bleeding on probing (BoP) scores and resulted in the identification of new health- and gingivitis-associated taxa. Comparison of the healthy volunteers to the periodontitis patients also confirmed the association of a number of putative periodontal pathogens with chronic periodontitis. Taxa associated with gingivitis included Fusobacterium nucleatum subsp. polymorphum, Lachnospiraceae [G-2] sp. HOT100, Lautropia sp. HOTA94, and Prevotella oulorum, whilst Rothia dentocariosa was associated with periodontal health. Further study of these taxa is warranted and may lead to new therapeutic approaches to prevent periodontal disease.
    PLoS ONE 01/2013; 8(8):e71227. · 3.73 Impact Factor
  • William G Wade
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    ABSTRACT: The human mouth harbours one of the most diverse microbiomes in the human body, including viruses, fungi, protozoa, archaea and bacteria. The bacteria are responsible for the two commonest bacterial diseases of man: dental caries (tooth decay) and the periodontal (gum) diseases. Archaea are restricted to a small number of species of methanogens while around 1000 bacterial species have been found, with representatives from the phyla Actinobacteria, Bacteroidetes, Firmicutes, Proteobacteria, Spirochaetes, Synergistetes and Tenericutes and the uncultured divisions GN02, SR1 and TM7. Around half of oral bacteria are as yet uncultured and culture-independent methods have been successfully used to comprehensively describe the oral bacterial community. The human oral microbiome database (HOMD, www.homd.org) provides a comprehensive resource consisting of descriptions of oral bacterial taxa, a 16S rRNA identification tool and a repository of oral bacterial genome sequences. Individuals' oral microbiomes are highly specific at the species level, although overall the human oral microbiome shows few geographical differences. Although caries and periodontitis are clearly bacterial diseases, they are not infectious diseases in the classical sense because they result from a complex interaction between the commensal microbiota, host susceptibility and environmental factors such as diet and smoking. Periodontitis, in particular, appears to result from an inappropriate inflammatory reaction to the normal microbiota, exacerbated by the presence of some disease-associated bacterial species. In functional terms, there appears to considerable redundancy among the oral microbiota and a focus on functional rather than phylogenetic diversity may be required in order to fully understand host-microbiome interactions.
    Pharmacological Research 11/2012; · 4.35 Impact Factor
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    ABSTRACT: BACKGROUND: The UK Biobank (UKB) is a national epidemiological study of the health of 500 000 people, aged 40-69 years, who completed health-related tests and a questionnaire and gave samples of blood and urine. Salivas collected from 120 000 of these subjects were transported at 4°C and were placed in ultra-low temperature archives at up to 24 h after collection. The present study assessed how changes in saliva composition under UKB conditions influence a range of potential biomarkers resulting from holding saliva at 4°C for 24 h. METHODS: Unstimulated whole-mouth saliva samples were collected from 23 volunteers aged 45-69 years. Salivas were split into aliquots some of which were immediately frozen at -80°C, whereas others were stored at 4°C for 24 h and then frozen at -80°C, mimicking the UKB protocol. RESULTS: Assessment of mRNA by real-time polymerase chain reaction revealed no difference between samples that were analysed after the UKB protocol and those that were immediately preserved. Immunochemical analysis showed some loss of β-Actin under UKB conditions, whereas other salivary proteins including cytokines and C-reactive protein appeared to be unaffected. Cortisol and showed no reduction by UKB conditions, but salivary nitrite was reduced by 30%. The oral microbiome, as revealed by sequencing 16S rRNA genes, showed variations between subjects, but paired samples within subjects were very similar. CONCLUSIONS: Our results suggest that many salivary components remain little affected under UKB collection and handling protocols, suggesting that the resource of 120 000 samples held in storage will be useful for phenotyping subjects and revealing potential prognostic disease biomarkers.
    International Journal of Epidemiology 11/2012; · 6.98 Impact Factor
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    ABSTRACT: Five strains of anaerobic, Gram-negative bacilli isolated from the human oral cavity were subjected to a comprehensive range of phenotypic and genotypic tests and were found to comprise a homogeneous group. Phylogenetic analysis of full-length 16S rRNA gene sequences showed that these strains represented a novel group within the family Prevotellaceae, and the most closely related species was Prevotella tannerae. P. tannerae and the novel taxon are deeply branched from the genus Prevotella with sequence identities to the type species of Prevotella, P. melaninogenica of 82.2 and 85.6 %, respectively. The novel genus Alloprevotella gen. nov. is proposed to accommodate the novel species Alloprevotella rava gen. nov, sp. nov., and the previously named P. tannerae as Alloprevotella tannerae gen. nov., comb. nov. The type species is Alloprevotella tannerae (Moore, Johnson & Moore, 1994). Alloprevotella rava is weakly to moderately saccharolytic and produces moderate amounts of acetic acid and major amounts of succinic acid as end products of fermentation. Strains are sensitive to 20 % bile and hydrolyze gelatin. The principal cellular long chain fatty acids are ai-C15:0, i-C15:0, C16:0, i-C17:0 and 3OH i-C17:0. The G+C content of the DNA of the type strain is 47 mol%. The type strain of Alloprevotella rava is 81/4-12T (= DSM 22548T = CCUG 58091T).
    INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY 06/2012; · 2.11 Impact Factor
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    ABSTRACT: SGP1T , a strain belonging to a lineage of the phylum Synergistetes with no previously cultivated representatives was subjected to a comprehensive range of phenotypic and genotypic tests. The strain was dependent for good growth on co-culture with, or extracts from, selected other oral bacteria. Phylogenetic analysis of the full-length 16S rRNA gene showed that the strain represented a novel group within the phylum Synergistetes. A new genus Fretibacterium and the new species Fretibacterium fastidiosum gen. nov. sp. nov. are proposed. The cells are asaccharolytic and major amounts of acetic acid and moderate amounts of propionic acid are produced as end products of metabolism in peptone-yeast extract-glucose broth supplemented with a filtered cell sonicate of Fusobacterium nucleatum (25% v/v). Hydrogen sulphide is produced and gelatin is weakly hydrolysed. The major cellular fatty acids are C14:0, C18:0 and C16:0. The G+C content of the DNA of the type strain is 63 mol%. The type strain of Fretibacterium fastidiosum is SGP1T (=DSM 25557T =JCM 16858T).
    INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY 04/2012; · 2.11 Impact Factor
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    ABSTRACT: The phylogenetic significance of the diversity of key enzymes of methylotrophic and autotrophic metabolism is discussed. Primers for these key enzymes were designed using gene sequences encoding methanol dehydrogenase (mxaF; using subsets from database sequences for 22 Bacteria), hydroxypyruvate reductase (hpr; 36 sequences), methylamine dehydrogenase (mauA; 12 sequences), methanesulfonate monooxygenase (msmA; four sequences), and the ccbL and cbbM genes of ribulose bisphosphate carboxylase (26 and 23 sequences). These were effective in amplifying the correct gene products for the target genes in reference organisms and in test organisms not previously shown to contain the genes, as well as in some methylotrophic Proteobacteria isolated from the human mouth. The availability of the new primers increases the probability of detecting diverse examples of the genes encoding these key enzymes both in natural populations and in isolated bacterial strains.
    Polish journal of microbiology / Polskie Towarzystwo Mikrobiologów = The Polish Society of Microbiologists 01/2012; 61(1):11-22. · 0.77 Impact Factor
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    ABSTRACT: It has been suggested that the use of alcohol-containing mouthrinses could lead to the presence of acetaldehyde in saliva. In this cross-over study, salivary acetaldehyde levels and microbial profiles were determined before and after rinsing with ethanol-containing mouthrinses with essential oils (EO) and cetyl pyridinium chloride (CPC) as the active ingredients, and with 21.6% ethanol and water controls. After rinsing with all ethanol-containing rinses, acetaldehyde was detected in saliva after 30 s but declined to low levels after 5 min. The highest peak levels were seen with the ethanol control (median = 82.9 μM at 2 min) and were significantly higher than those seen at the same time after rinsing with the EO rinse (43.1 μM). There was no correlation between microbial counts or plaque scores and acetaldehyde levels, although dividing the subjects on the basis of a peak acetaldehyde salivary concentration of > 90.8 μM after the ethanol rinse revealed that the high responders were highly significantly more likely to harbour salivary yeasts than were the low responders. Rinsing with ethanol-containing mouthrinses causes a rapid, but transient, increase in salivary acetaldehyde levels.
    European Journal Of Oral Sciences 12/2011; 119(6):441-6. · 1.42 Impact Factor
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    ABSTRACT: A collection of Streptococcus sanguinis strains from patients with endocarditis (n = 21) and from the oral cavity (n = 34) was subjected to a multi-locus sequence typing analysis using seven housekeeping genes, carbamoyl-phosphate synthetase (carB), Co/Zn/Cd efflux system component (czcD), d-alanyl-d-alanine ligase (ddl), DNA polymerase III (dnaX), glucose-6-phosphate dehydrogenase (gdh), DNA-directed RNA polymerase, beta subunit (rpoB) and superoxide dismutase (sodA). The scheme was expanded by the inclusion of two the putative virulence genes, bacitracin-resistance protein (bacA) and saliva-binding protein (ssaB), to increase strain discrimination. Extensive intra-species recombination was apparent in all genes but inter-species recombination was also apparent with strains apparently harbouring gdh and ddl from unidentified sources and one isolate harboured a sodA allele apparently derived from Streptococcus oralis. The recombination/mutation ratio for the concatenated housekeeping gene sequences was 1.67 (95% confidence limits 1.25-2.72) and for the two virulence genes the r/m ratio was 3.99 (95% confidence limits 1.61-8.72); recombination was the major driver for genetic variation. All isolates were distinct and the endocarditis strains did not form distinct sub-clusters when the data were analysed using ClonalFrame. These data support the widely held opinion that infecting S. sanguinis strains are opportunistic human pathogens.
    Molecular oral microbiology. 10/2011; 26(5):291-302.
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    ABSTRACT: The human oral cavity is host to a complex microbial community estimated to comprise >700 bacterial species, of which at least half are thought to be not yet cultivable in vitro. To investigate the plasmids present in this community, we used a transposon-aided capture system, which allowed the isolation of plasmids from human oral supra- and subgingival plaque samples. Thirty-two novel plasmids and a circular molecule that could be an integrase-generated circular intermediate were isolated.
    FEMS Microbiology Ecology 06/2011; 78(2):349-54. · 3.56 Impact Factor
  • Julia Downes, William G Wade
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    ABSTRACT: Two strains of anaerobic, Gram-negative bacilli isolated from the human oral cavity were subjected to a comprehensive range of phenotypic and genotypic tests and were found to belong to two separate taxa. Phylogenetic analysis of full-length 16S rRNA gene sequences showed that the strains were both related to, but distinct from, the type strain of Prevotella melaninogenica. Two novel species, Prevotella fusca sp. nov. and Prevotella scopos sp. nov., are proposed to accommodate these strains. Both strains were saccharolytic and produced acetic and succinic acids, with lesser amounts of lactic and isovaleric acids, as end products of fermentation, and both were sensitive to 20 % bile. The principal cellular long-chain fatty acids of both strains were ai-C(15 : 0), 3-OH i-C(17 : 0), 3-OH C(16 : 0), i-C(15 : 0) and C(16 : 0). The DNA G+C contents of the type strains of Prevotella fusca (W1435(T)  = DSM 22504(T)  = CCUG 57946(T)) and Prevotella scopos (W2052(T)  = DSM 22613(T ) = CCUG 57945(T)) were 43 and 41 mol%, respectively. The two species could be differentiated by gelatin hydrolysis, cellobiose and ribose fermentation, and production of β-glucosidase.
    INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY 04/2011; 61(Pt 4):854-8. · 2.11 Impact Factor
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    ABSTRACT: We show that bacteria with methylotrophic potential are ubiquitous in the human mouth microbiota. Numerous strains of Actinobacteria (Brevibacterium, Gordonia, Leifsonia, Microbacterium, Micrococcus, Rhodococcus) and Proteobacteria (Achromobacter, Klebsiella, Methylobacterium, Pseudomonas, Ralstonia) were isolated, and one strain of each of the eleven genera was studied in detail. These strains expressed enzymes associated with methylotrophic metabolism (methanol, methylamine, and formate dehydrogenases), and the assimilation of one-carbon compounds by the serine pathway (hydroxypyruvate reductase). Methylotrophic growth of the strains was enhanced by the addition of glass beads to cultures, suggesting that they may naturally occur in biofilms in the mouth. This is the first report of Gordonia, Leifsonia, and Rhodococcus being present in the mouth and of the unequivocal demonstration for the first time of the methylotrophic potential of strains of Gordonia, Leifsonia, and Microbacterium.
    Archives of Microbiology 03/2011; 193(6):407-17. · 1.91 Impact Factor
  • William Geoffrey Wade
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    ABSTRACT: Only around half of oral bacteria can be grown in the laboratory using conventional culture methods. Molecular methods based on 16S rRNA gene sequence are now available and are being used to characterize the periodontal microbiota in its entirety. This review describes the cultural characterization of the oral and periodontal microbiotas and explores the influence of the additional data now available from culture-independent molecular analyses on current thinking on the role of bacteria in periodontitis. Culture-independent molecular analysis of the periodontal microbiota has shown it to be far more diverse than previously thought. A number of species including some that have yet to be cultured are as strongly associated with disease as those organisms traditionally regarded as periodontal pathogens. Sequencing of bacterial genomes has revealed a high degree of intra-specific genetic diversity. The use of molecular methods for the characterization of the periodontal microbiome has greatly expanded the range of bacterial species known to colonize this habitat. Understanding the interactions between the human host and its commensal bacterial community at the functional level is a priority.
    Journal Of Clinical Periodontology 03/2011; 38 Suppl 11:7-16. · 3.69 Impact Factor
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    ABSTRACT: Metagenomic techniques are used to analyse bacterial communities allowing both culturable and unculturable species to be represented. However, the screening of oral metagenomic samples can be hindered by high animal host DNA content. This study evaluated methods for the reduction of human DNA concentrations within oral metagenomic samples. Plaque samples were collected from 27 patients presenting with periodontal disease and treated to remove human DNA using either selective lysis of eukaryotic cells at several buffer concentrations or differential centrifugation after treatment with trypsin and/or detergents. Human and bacterial DNA levels were determined by quantitative polymerase chain reaction (qPCR). The human DNA content of plaque extracts was significantly reduced by all treatments compared with an untreated control (P < 0.05). However, differential centrifugation simultaneously reduced the bacterial DNA content unless samples were pretreated with a detergent. Observations of Gram stained samples that were processed using differential centrifugation without detergent suggest that many bacteria remain adhered to human cells. An approach that uses differential centrifugation in parallel with selective lysis is recommended to fully represent the oral microbiota in metagenomic samples, including those tightly adhered to human cells and more delicate bacteria such as Mycoplasma.
    Journal of Basic Microbiology 02/2011; 51(4):442-6. · 1.20 Impact Factor
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    ABSTRACT: SummaryA collection of Streptococcus sanguinis strains from patients with endocarditis (n = 21) and from the oral cavity (n = 34) was subjected to a multi‐locus sequence typing analysis using seven housekeeping genes, carbamoyl‐phosphate synthetase (carB), Co/Zn/Cd efflux system component (czcD), d‐alanyl‐d‐alanine ligase (ddl), DNA polymerase III (dnaX), glucose‐6‐phosphate dehydrogenase (gdh), DNA‐directed RNA polymerase, beta subunit (rpoB) and superoxide dismutase (sodA). The scheme was expanded by the inclusion of two the putative virulence genes, bacitracin‐resistance protein (bacA) and saliva‐binding protein (ssaB), to increase strain discrimination. Extensive intra‐species recombination was apparent in all genes but inter‐species recombination was also apparent with strains apparently harbouring gdh and ddl from unidentified sources and one isolate harboured a sodA allele apparently derived from Streptococcus oralis. The recombination/mutation ratio for the concatenated housekeeping gene sequences was 1.67 (95% confidence limits 1.25–2.72) and for the two virulence genes the r/m ratio was 3.99 (95% confidence limits 1.61–8.72); recombination was the major driver for genetic variation. All isolates were distinct and the endocarditis strains did not form distinct sub‐clusters when the data were analysed using ClonalFrame. These data support the widely held opinion that infecting S. sanguinis strains are opportunistic human pathogens.
    Molecular Oral Microbiology 01/2011; 26(5). · 2.65 Impact Factor
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    ABSTRACT: The human oral cavity contains a number of different habitats, including the teeth, gingival sulcus, tongue, cheeks, hard and soft palates, and tonsils, which are colonized by bacteria. The oral microbiome is comprised of over 600 prevalent taxa at the species level, with distinct subsets predominating at different habitats. The oral microbiome has been extensively characterized by cultivation and culture-independent molecular methods such as 16S rRNA cloning. Unfortunately, the vast majority of unnamed oral taxa are referenced by clone numbers or 16S rRNA GenBank accession numbers, often without taxonomic anchors. The first aim of this research was to collect 16S rRNA gene sequences into a curated phylogeny-based database, the Human Oral Microbiome Database (HOMD), and make it web accessible (www.homd.org). The HOMD includes 619 taxa in 13 phyla, as follows: Actinobacteria, Bacteroidetes, Chlamydiae, Chloroflexi, Euryarchaeota, Firmicutes, Fusobacteria, Proteobacteria, Spirochaetes, SR1, Synergistetes, Tenericutes, and TM7. The second aim was to analyze 36,043 16S rRNA gene clones isolated from studies of the oral microbiota to determine the relative abundance of taxa and identify novel candidate taxa. The analysis identified 1,179 taxa, of which 24% were named, 8% were cultivated but unnamed, and 68% were uncultivated phylotypes. Upon validation, 434 novel, nonsingleton taxa will be added to the HOMD. The number of taxa needed to account for 90%, 95%, or 99% of the clones examined is 259, 413, and 875, respectively. The HOMD is the first curated description of a human-associated microbiome and provides tools for use in understanding the role of the microbiome in health and disease.
    Journal of bacteriology 10/2010; 192(19):5002-17. · 3.94 Impact Factor
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    ABSTRACT: Molecular ecology methods are now well established for the culture-independent characterization of complex bacterial communities associated with various environmental and animal habitats and are revealing the extent of their diversity. By comparison, it has become clear that only a small minority of microorganisms are readily cultivated in vitro, with the majority of all bacteria remaining 'unculturable' using standard methods. Yet, it is only through the isolation of bacterial species in pure culture that they may be fully characterized, both for their physiological and pathological properties. Hence, the endeavour to devise novel cultivation methods for microorganisms that appear to be inherently resistant to artificial culture is a most important one. This minireview discusses the possible reasons for 'unculturability' and evaluates advances in the cultivation of previously unculturable bacteria from complex bacterial communities. Methods include the use of dilute nutrient media particularly suited for the growth of bacteria adapted to oligotrophic conditions, and the provision of simulated natural environmental conditions for bacterial culture. This has led to the recovery of 'unculturables' from soil and aquatic environments, likely to be due to the inclusion of essential nutrients and/or signalling molecules from the native environment.
    FEMS Microbiology Letters 08/2010; 309(1):1-7. · 2.05 Impact Factor
  • W G Wade
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    ABSTRACT: The human mouth is host to a diverse collection of microorganisms including bacteria, viruses, fungi and protozoa. Recent advances using molecular methods for the analysis of complex bacterial communities have demonstrated the richness of the oral bacterial biota and the presence of numerous previously undescribed lineages. Dental plaque forms in a structured way with pioneer species able to colonise pellicle-coated enamel followed by secondary plaque formers such as Fusobacterium nucleatum that have the capability of coaggregating with a range of other genera and species. The mature plaque biofilm has many features of multicellular organisms with the constituent organisms cooperating to make nutrients available and resist environmental stresses, and communicating to regulate their overall numbers. Control of the oral microbiota to prevent disease has conventionally been by mechanical means augmented with toothpastes and mouthrinses, but improved knowledge of oral microbial ecology is allowing the development of pre and pro-biotic approaches. Other possibilities include interference with the plaque formation process and the perturbation of bacterial communication networks.
    Journal of dentistry 06/2010; 38 Suppl 1:S21-5. · 3.20 Impact Factor
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    ABSTRACT: Subgingival plaque samples obtained from human subjects with periodontitis, shown to include previously uncultivable members of the phylum Synergistetes, were used to inoculate Cooked Meat Medium (CMM). The presence of Cluster A (uncultivable) Synergistetes was monitored by fluorescent in situ hybridization (FISH) and quantitative PCR (Q-PCR). Cluster A Synergistetes were found to grow in CMM in co-culture with other plaque bacteria and growth was stimulated by the addition of mucin and serum. Plaque samples were also used to inoculate Blood Agar (BA) plates and growth of Cluster A Synergistetes was revealed after anaerobic incubation, by colony hybridization with specific probes. Surface growth on the plates in regions identified by colony hybridization was harvested and used to inoculate fresh plates, thus enriching for Cluster A Synergistetes. Cross-streaks of other plaque bacteria were also used to stimulate Synergistetes growth. In the early passages, no discrete Synergistetes colonies were seen, but after eight passages and the use of cross-streaks of other bacteria present in the enriched community, colonies arose, which consisted solely of Cluster A Synergistetes cells, as determined by 16S rRNA gene PCR and cloning. This is the first report of the successful culture of a member of the uncultivable branch of this phylum.
    Environmental Microbiology 04/2010; 12(4):916-28. · 5.76 Impact Factor
  • William G. Wade, Julie F. Downes
    03/2010; , ISBN: 9780470688618

Publication Stats

3k Citations
356.86 Total Impact Points

Institutions

  • 1999–2013
    • King's College London
      • Dental Institute
      Londinium, England, United Kingdom
  • 2010
    • Harvard Medical School
      Boston, Massachusetts, United States
  • 2001–2010
    • The Forsyth Institute
      Cambridge, Massachusetts, United States
    • King College
      Guymon, Oklahoma, United States
  • 2006
    • University of Zurich
      • Institut für Orale Biologie
      Zürich, ZH, Switzerland
  • 2005
    • Cardiff University
      Cardiff, Wales, United Kingdom
  • 2002
    • The Kings College
      Guymon, Oklahoma, United States
    • British Society for Restorative Dentistry
      Bristol, England, United Kingdom
  • 1997
    • University of the West of England, Bristol
      Bristol, England, United Kingdom
  • 1995–1997
    • University of Bristol
      • School of Oral and Dental Sciences
      Bristol, England, United Kingdom
  • 1996
    • Aarhus University
      • Faculty of Health Sciences
      Aars, Region North Jutland, Denmark
  • 1987–1996
    • University of Wales
      • College of Medicine
      Cardiff, Wales, United Kingdom