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1 Infection Research Group, Dental Institute, King's College London, London SE1 9RT, UK
2 Division of Biomedical Sciences, School of Applied Sciences, Northumbria University, Newcastle upon Tyne NE1 8ST, UK
3 Department of Molecular Genetics, The Forsyth Institute, Boston, MA 02115, USA
Correspondence
William G. Wade
william.wade{at}kcl.ac.uk
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Published online ahead of print on 1 March 2005 as DOI 10.1099/ijs.0.63634-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of P. marshii E9.34T, P. baroniae E9.33T, P. loescheii NCTC 11321T, P. oralis NCTC 11459T, P. denticola ATCC 35308T, P. melaninogenica ATCC 25845T and P. veroralis ATCC 33779T are AF481227, AY840553, AY836508, AY323522, AY323524, AY323525 and AY836507, respectively.
Transmission electron micrographs of P. baroniae E9.33T and P. marshii E9.34T, an extended phylogenetic tree and details of FAME profiles are available as supplementary material in IJSEM Online.
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). Seventeen of the Prevotella species with validly published names are found in the oral cavity. The use of molecular methods, particularly 16S rRNA gene sequence analysis, for the identification of oral bacterial isolates has revealed that a significant proportion of strains do not correspond to species with validly published names (Kroes et al., 1999; Munson et al., 2002, 2004). In this study, 11 strains of anaerobic Gram-negative bacilli, isolated from human oral infections and dental plaque in healthy subjects, provisionally identified as belonging to the genus Prevotella, were subjected to a range of phenotypic and genotypic tests. Strains E9.33T, E9.34T and W7346 were isolated from endodontic lesions, W5520 and W5712 were isolated from dental abscesses, W1833 was isolated from a pericoronitis lesion, D016C-10 and D031A-28 were isolated from supragingival plaque from individuals with periodontitis and strains D190A-02, D153G-12 and W6967 were isolated from subgingival plaque in periodontally healthy individuals. Strains D016C-10, D031A-28, D190A-02 and D153G-12 were obtained from the collection of W. E. C. Moore and L. V. Holdeman Moore, formerly of the Virginia Polytechnic Institute. Prevotella denticola ATCC 35308T, Prevotella melaninogenica ATCC 25845T, Prevotella veroralis ATCC 33779T, Prevotella loescheii NCTC 11321T, Prevotella oralis NCTC 11459T, Prevotella shahii DSM 15611T and Prevotella buccae CCUG 15401T were obtained from the American Type Culture Collection (Manassas, VA, USA), the National Collection of Type Cultures, Central Public Health Laboratory (London, UK), the Deutsche Sammlung von Mikroorganismen und Zellkulturen (Braunschweig, Germany) or the Culture Collection of the University of Göteborg (Gothenburg, Sweden), respectively.
Strains were grown at 37 °C on fastidious anaerobe agar (FAA; LabM), supplemented with 5 % horse blood, under anaerobic conditions (in N2/H2/CO2: 80 10 ; 10, by vol.) in an MAC anaerobic chamber (Don Whitley). Colonial morphologies were determined using a plate microscope after 5 days incubation. Cellular morphology was recorded after Gram staining of 2-day-old plate cultures. Hanging-drop preparations of 18 h cultures of peptone/yeast extract/glucose (PYG; Holdeman et al., 1977) broth were examined under phase-contrast microscopy (Axioskop; Zeiss) for cellular motility. Transmission electron microscopy (H7600; Hitachi) was used to examine the cell-wall ultrastructure of strains E9.34T and E9.33T as described previously (Downes et al., 2003).
Fermentation tests were performed using pre-reduced, anaerobically sterilized sugars prepared in an anaerobic workstation (Holdeman et al., 1977). Other biochemical tests were performed using standard methods (Holdeman et al., 1977; Jousimies-Somer et al., 2002). Bacterial strains were grown in peptone/yeast extract (PY) broth (Holdeman et al., 1977) with and without glucose and short-chain volatile and non-volatile fatty acids were extracted by standard methods and analysed by GC (Holdeman et al., 1977). Enzyme profiles were generated with the Rapid ID 32A anaerobe identification kit (bioMérieux), according to the manufacturer's instructions, using bacteria harvested from blood agar plates (blood agar base no. 2; LabM) supplemented with 5 % horse blood, and performed in triplicate.
The cellular fatty acid composition was determined for 10 strains as described previously (Sutcliffe, 2000). In brief, fatty acids from lyophilized whole cells were derivatized to produce fatty acid methyl esters (FAMEs) by acid-catalysed methanolysis. FAMEs were recovered by hexane extraction and concentration under nitrogen, followed by GC analysis (Sutcliffe, 2000). FAMEs were identified by comparison with authentic FAME standards (Sigma).
The G+C content of the DNA was estimated by using an HPLC method for E2 strains E9.34T and D153G-12 and E4 strains E9.33T and W1833 as described previously (Wade et al., 1999). A thermal denaturation method (Huß et al., 1983) was used to determine the DNA–DNA relatedness between strains.
DNA was isolated from the bacteria by using a standard method. Briefly, cells were suspended in TE buffer (10 mM Tris/HCl, 1 mM EDTA, pH 8; Sigma) and treated with lysozyme (500 µg ml–1) for 30 min at 37 °C followed by proteinase K (500 µg ml–1) and 20 % N-lauroyl-sarcosine (Sarkosyl; Sigma) (2 %) for 2 h at 37 °C. After two phenol/chloroform extractions and one chloroform extraction, DNA was precipitated by the addition of two volumes of ethanol (stored at –20 °C) and washed in 70 % ethanol. The 16S rRNA gene was amplified by a PCR with primers 27F and 1492R (Lane, 1991) and a Uno II Thermocycler (Biometra) using Ready to Go PCR beads (Pharmacia/Amersham). PCR products were sequenced directly using a dye terminator cycle sequencing kit (CEQ DTCS; Beckman Coulter) and 60 ng template DNA, according to the manufacturer's instructions. Sequencing was performed using an automated sequencer (CEQ2000; Beckman Coulter) with primers 27f, 342r, 357f, 519r, 907r, 926f, 1100r, 1114f and 1492r (Lane, 1991); primers 1100r and 1114f had minor modifications (1100Ar, 5'-GGGTTGCGCTCGTTA-3'; 1114ATf, 5'-ATAACGAGCGCAACCC-3'). Sequences were connected using the BioEdit program (Hall, 2004) and identified by BLAST interrogation of the GenBank database (Altschul et al., 1990). Related sequences were aligned by means of CLUSTAL X (Thompson et al., 1997). Further analysis was performed using the PHYLIP suite of programs (Felsenstein, 1993). Specifically, a distance matrix was constructed using the Jukes–Cantor algorithm with DNADIST, and NEIGHBOR was used to construct phylogenetic trees, which were viewed using TREEVIEW (Page, 1996).
The 11 strains studied were found to fall into two groups. Five strains, E9.34T, D190A-02, D153G-12, D016C-10 and D031A-28, designated group E2, had cells that were 0·4 µm wide by 0·9–3 µm long, with the occasional cell reaching 6 µm in length, and occurred singly and in pairs. After 5 days incubation on FAA plates, E2 colonies were 1·8–3·5 mm in diameter, circular and entire, convex, watery, opaque and grey to off-white/grey to greenish grey. Areas of heavier growth at the end of the streak lines on FAA were cream in colour. Viewed under a plate microscope, the colonies had a striated appearance with concentric rings of varying opacity and iridescent hues of pink, green and yellow.
The remaining six strains, designated group E4, consisted of coccoid and short bacilli, the majority of cells being 0·6x0·6–2·0 µm, with occasional cells ranging from 3 to 8 µm in length. After 5 days incubation on FAA plates, E4 colonies were 1·2–3·8 mm in diameter, circular, high convex and opaque with an off-white centre, which appeared matt in some strains and had a shiny grey periphery. Colony morphology varied from entire to undulate; this variation appeared to be strain-related but in some instances both forms were present in the same strain.
Transmission electron microscopic examination of ultrathin sections through the cells of E9.34T (group E2) and E9.33T (group E4) showed the presence of a typical Gram-negative cell wall composed of a thin peptidoglycan layer surrounded by an outer membrane (micrographs are available as Supplementary Fig. S1 in IJSEM Online).
Growth of all E2 strains in PY broth was good and produced a moderately turbid suspension (3+ on a scale of 0 to 4+) with a deposit of cells on standing. Growth was markedly enhanced by the addition of either glucose, fructose or maltose (1 %, w/v, in each case), resulting in a heavily turbid suspension of 4+. Strains were saccharolytic and fermented glucose and maltose strongly and fructose and mannose weakly and variably. Other sugars tested, listed in the species description, were not fermented. The major end-products of fermentation were acetic acid and succinic acid; minor to moderate amounts of propionic acid were also produced. Hydrolysis of gelatin was strongly positive, with pre-reduced, anaerobically sterilized gelatin tests not solidifying at 4 °C. All E2 strains were positive for 
-glucosidase, alkaline phosphatase, leucyl glycine arylamidase, pyroglutamic acid arylamidase and alanine arylamidase in the Rapid ID 32A identification panel, while reactions for glutamyl glutamic acid arylamidase were weak and variable. All strains gave negative results in the remaining 23 tests, resulting in a Rapid ID 32A profile of 0400 4442 00/2. The G+C content of the DNA of strains E9.34T and D153G-12 was 51 mol%.
Growth of E4 strains in PY broth was good (3+) and produced a deposit of cells with a slightly turbid suspension (1+) in PY broth and a clear supernatant in PYG broth on standing. Growth was somewhat enhanced by the addition of 1 % (w/v) fermentable carbohydrates. The major end-products of fermentation in PYG broth were acetic acid and succinic acid; isovaleric acid was a minor end-product. In addition to these acids, minor amounts of isobutyric acid were produced in PY broth, and larger amounts of isovaleric acid were produced in PY broth than in PYG broth. All E4 strains were positive for -galactosidase, 
-galactosidase, -glucosidase, -glucosidase, N-acetyl--glucosaminidase, alkaline phosphatase, leucyl glycine arylamidase, alanine arylamidase and -fucosidase in the Rapid ID 32A identification panel, while reactions for mannose and raffinose fermentation and for glutamyl glutamic acid arylamidase were variable. All strains were negative for the remaining 17 tests, resulting in a Rapid ID 32A profile of 4511/5/7 4402 20/2. The G+C content of the DNA of strains E9.33T and W1833 was 52 mol%.
A phylogenetic tree showing the relationship between representative strains of groups E2 and E4 and other closely related species of the genus Prevotella is shown in Fig. 1. The 16S rRNA genes of the type strains of P. denticola, P. loescheii, P. melaninogenica, P. oralis and P. veroralis were sequenced and deposited with GenBank to improve the quality of the phylogenetic analysis, in view of the relatively large number of ambiguous bases present in the sequences then available for these strains in the database. Group E2 strain E9.34T was found to be most closely related to P. shahii (92·2 % 16S rRNA gene sequence identity over 1455 unambiguously aligned bases). In addition, the 16S rRNA gene was sequenced in E2 strains D190A-02, D153G-12, D016C-10 and D031A-28: over 1415 bases, each strain had >99·7 % sequence similarity to the other three strains and to strain E9.34T. E4 strain E9.33T was most closely related to P. buccae (91·3 % sequence identity over 1440 bases). E4 strains W1833, W6967 and W7346 each exhibited >99·5 % 16S rRNA gene sequence identity to the other two strains and to strain E9.33T over 1404 bases.
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Prevotella species are reported to synthesize both non-hydroxylated and 3-hydroxylated fatty acids (Shah & Collins, 1990; Willems & Collins, 1995). More than 90 % of the FAMEs recovered from the strains studied were identifiable by GC as being non-hydroxylated (FAME data are available as Supplementary Table S1 in IJSEM Online). Of the non-hydroxylated fatty acids in Prevotella, methyl-branched fatty acids (notably anteiso-C15 : 0) are reported to predominate, along with C16 : 0 (Logar et al., 2001; Moore et al., 1994; Sakamoto et al., 2004). Consistent with the assignment of E2 and E4 to the genus Prevotella, the main FAMEs detected in the present study were iso-C15 : 0 and anteiso-C15 : 0, whilst C16 : 0 was abundant in strains from group E4. However, strains from group E4 were also distinguished by a high content of anteiso-C17 : 0 FAMEs. Strains from group E2 were distinguished by a reduced content of C16 : 0 and markedly increased C15 : 0 content. Intriguingly, Sakamoto et al. (2004) identified significant quantities of unsaturated fatty acids in representative Prevotella species, including P. shahii and P. loescheii, which are phylogenetically closely related to group E2. However, unsaturated fatty acids have not been noted as major components by others using GC (Debelian et al., 1997; Logar et al., 2001; Moore et al., 1994) and were not observed in strains of groups E2 and E4 (see Supplementary Table S1). It is noted that mass spectrometry studies have also identified unsaturated fatty acids in Prevotella species, including mono-, di- and tri-unsaturated forms (Radcliffe et al., 2001; Tavana et al., 1998). It is clear that a comprehensive, integrated re-examination of the hydroxylated and non-hydroxylated fatty acid composition of members of the genus Prevotella is warranted.
The phenotypic and genotypic tests described here show that the strains tested fall into two groups that are distinct from any Prevotella species with validly published names. We propose the name Prevotella marshii sp. nov. for the strains in the E2 group and Prevotella baroniae sp. nov. for the E4 group, with E9.34T (=DSM 16973T=CCUG 50419T) and E9.33T (=DSM 16972T=CCUG 50418T) as the respective type strains.
Phenotypic characteristics that distinguish P. marshii and P. baroniae from other Prevotella species are shown in Table 1. P. marshii is unusual in that it produces minor to moderate amounts of propionic acid as a by-product of fermentation. Although the characteristics shown will help in the identification of clinical isolates, unequivocal identification will not be possible in all cases. 16S rRNA gene sequence analysis is recommended for the identification of clinical isolates in this genus, not least because the many additional unnamed Prevotella taxa will be recognized by this method.
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The description is based on five strains isolated from the human oral cavity. Cells are obligately anaerobic, non-motile, Gram-negative bacilli (0·4x0·9–3 µm) occurring singly and in pairs with an occasional elongated cell up to 6 µm long. After 5 days incubation on FAA plates, colonies are 1·8–3·5 mm in diameter, circular and entire, convex, watery, opaque and grey to off-white/grey to greenish grey. Areas of heavier growth at the end of the streak lines on FAA are cream in colour. Viewed under a plate microscope the colonies have a striated appearance with concentric rings of varying opacity and iridescent hues of pink, green and yellow. Growth in broth media produces moderate turbidity that is markedly enhanced by the addition of glucose, fructose or maltose. Cells are saccharolytic and ferment glucose and maltose strongly and fructose and mannose weakly and variably. Arabinose, cellobiose, lactose, mannitol, melezitose, melibiose, raffinose, rhamnose, ribose, salicin, sorbitol, sucrose and trehalose are not fermented. Major amounts of acetic acid and succinic acid and moderate amounts of propionic acid are produced as end-products of metabolism in PYG broth. Gelatin is hydrolysed; aesculin, arginine and urea are not hydrolysed. Indole and catalase are not produced and nitrate is not reduced. There is no growth in 20 % bile. The Rapid ID 32A profile is 0400 4442 00/2. The fatty acid profile predominantly comprises anteiso-C15 : 0, iso-C15 : 0, C15 : 0 and iso-C14 : 0. The G+C content of the DNA of the type strain is 51 mol%.
Isolated from the human oral cavity in subjects with endodontic and periodontal infections and from subgingival dental plaque in healthy subjects. The type strain is E9.34T (=DSM 16973T=CCUG 50419T).
Description of Prevotella baroniae sp. nov.
Prevotella baroniae (bar'on.i.ae. N.L. gen. n. baroniae of Baron, named in honour of Ellen Jo Baron, the American microbiologist, for her contributions to clinical microbiology).
The description is based on six strains isolated from the human oral cavity. Cells are obligately anaerobic, non-motile, Gram-negative coccoid and short bacilli (0·6 µmx0·6–2·0 µm) with occasional cells ranging from 3 to 8 µm long. After 5 days incubation on FAA plates, colonies are 1·2–3·8 mm in diameter, circular, high convex and opaque with a shiny grey periphery and an off-white centre, which appears matt in some strains. Colony morphology varies from entire to undulate. Growth in PY broth is good and is somewhat enhanced by the addition of 1 % (w/v) fermentable carbohydrates. Cells are saccharolytic and ferment cellobiose, fructose, glucose, lactose, maltose, mannose, melibiose, raffinose, salicin and sucrose. Arabinose, mannitol, melezitose, rhamnose, ribose, sorbitol and trehalose are not fermented. End-products of fermentation in PYG broth are major acetic and succinic acids and minor isovaleric acid. Minor amounts of isobutyric acid are also produced in PY broth. Aesculin is hydrolysed, gelatin is weakly hydrolysed and arginine and urea are not hydrolysed. Indole and catalase are not produced and nitrate is not reduced. There is no growth in 20 % bile. The Rapid ID 32A profile is 4511/5/7 4402 20/2. The non-hydroxylated fatty acid profile predominantly comprises iso-C15 : 0, anteiso-C15 : 0, C16 : 0 and anteiso-C17 : 0. The G+C content of the DNA of the type strain is 52 mol%.
Isolated from the human oral cavity in patients with endodontic and periodontal infections or dentoalveolar abscesses and from the dental plaque of healthy subjects. The type strain is E9.33T (=DSM 16972T=CCUG 50418T).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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Debelian, G. J., Olsen, I. & Tronstad, L. (1997). Distinction of Prevotella intermedia and Prevotella nigrescens from endodontic bacteremia through their fatty acid contents. Anaerobe 3, 61–68.
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Sakamoto, M., Suzuki, M., Huang, Y., Umeda, M., Ishikawa, I. & Benno, Y. (2004). Prevotella shahii sp. nov. and Prevotella salivae sp. nov., isolated from the human oral cavity. Int J Syst Evol Microbiol 54, 877–883.
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Wade, W. G., Downes, J., Dymock, D., Hiom, S. J., Weightman, A. J., Dewhirst, F. E., Paster, B. J., Tzellas, N. & Coleman, B. (1999). The family Coriobacteriaceae: reclassification of Eubacterium exiguum (Poco et al. 1996) and Peptostreptococcus heliotrinreducens (Lanigan 1976) as Slackia exigua gen. nov., comb. nov. and Slackia heliotrinireducens gen. nov., comb. nov., and Eubacterium lentum (Prevot 1938) as Eggerthella lenta gen. nov., comb. nov. Int J Syst Bacteriol 49, 595–600.
Willems, A. & Collins, M. D. (1995). 16S rRNA gene similarities indicate that Hallella seregens (Moore and Moore) and Mitsuokella dentalis (Haapsalo et al.) are genealogically highly related and are members of the genus Prevotella: emended description of the genus Prevotella (Shah and Collins) and description of Prevotella dentalis comb. nov. Int J Syst Bacteriol 45, 832–836.
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