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International Journal of Systematic and Evolutionary Microbiology logoLink to International Journal of Systematic and Evolutionary Microbiology
. 2013 Apr;63(Pt 4):1323–1328. doi: 10.1099/ijs.0.041731-0

Neisseria oralis sp. nov., isolated from healthy gingival plaque and clinical samples

William J Wolfgang 1,2,✉, Teresa V Passaretti 1, Reashma Jose 1, Jocelyn Cole 1, An Coorevits 3,4, Andrea N Carpenter 1, Sherly Jose 1, Anita Van Landschoot 3,4, Jacques Izard 5,6, Donna J Kohlerschmidt 1, Peter Vandamme 4, Floyd E Dewhirst 5,6, Mark A Fisher 7,8, Kimberlee A Musser 1,2
PMCID: PMC3709538  PMID: 22798652

Abstract

A polyphasic analysis was undertaken of seven independent isolates of Gram-negative cocci collected from pathological clinical samples from New York, Louisiana, Florida and Illinois and healthy subgingival plaque from a patient in Virginia, USA. The 16S rRNA gene sequence similarity among these isolates was 99.7–100 %, and the closest species with a validly published name was Neisseria lactamica (96.9 % similarity to the type strain). DNA–DNA hybridization confirmed that these isolates are of the same species and are distinct from their nearest phylogenetic neighbour, N. lactamica. Phylogenetic analysis of 16S and 23S rRNA gene sequences indicated that the novel species belongs in the genus Neisseria. The predominant cellular fatty acids were C16 : 0, summed feature 3 (C16 : 1ω7c and/or iso-C15 : 0 2-OH) and C18 : 1ω7c. The cellular fatty acid profile, together with other phenotypic characters, further supports the inclusion of the novel species in the genus Neisseria. The name Neisseria oralis sp. nov. (type strain 6332T  = DSM 25276T  = LMG 26725T) is proposed.

In 2005, the Wadsworth Center Bacteriology Laboratory received two independent isolates of bacteria from clinical specimens as part of their reference testing for New York State laboratories (designated 6332T and 8261) that had identical nearly full-length 16S rRNA gene sequences. The most closely related species, based on sequence similarity, was Neisseria lactamica (96.9 % similarity to the type strain returned by EzTaxon; Chun et al., 2007), suggesting that the isolates may represent a novel species (Tindall et al., 2010). A blast search of GenBank revealed an additional isolate with 100 % sequence similarity, Neisseria sp. oral taxon 014 strain F0314 (GenBank accession no. GQ131417), which we acquired (Dewhirst et al., 2010). Four additional isolates were acquired from Associated Regional and University Pathologists (ARUP) Laboratories and found to have 99.7–99.9 % 16S rRNA gene sequence similarity to the three other isolates. Suggesting a widespread prevalence for this organism, the GenBank blast search also identified other studies in which the same 16S rRNA gene sequence was detected (sequence similarity >99.6 %) by culture-independent methodologies. The sources of these clones were subgingival plaque (healthy and diseased), healthy skin and respiratory samples from cystic fibrosis patients, (Dewhirst et al., 2010; Grice et al., 2009; Paster et al., 2001; Rylev et al., 2011; Staudinger et al., 2011; van der Gast et al., 2011). In the polyphasic study described here, the seven acquired isolates were found to belong to a single novel species, for which we propose the name Neisseria oralis sp. nov.

The seven isolates were maintained at 37 °C in a 5 % CO2 atmosphere on trypticase soy agar (TSA) plates (Becton Dickinson) supplemented with 5 % sheep blood. Four of the isolates were from blood cultures; one was from urine, one was from paracentesis fluid and one was from subgingival oral biofilm at a healthy site (Table 1). A representative strain, 6332T, was chosen as the type strain.

Table 1. Strains used in this study.

Strain Isolation date Source GenBank accession no.
16S rRNA gene 23S rRNA gene
6332T ( = LMG 26725T  = DSM 25276T) July 2005 Blood, 55-year-old male; Dutchess County, NY, USA JN104029 JN104031
8261 ( = LMG 26726  = DSM 25277) October 2005 Blood, 56-year-old female; Saratoga County, NY, USA JN104030 JN104032
F0314 ( = 11-24509) June 1982 Subgingival oral biofilm, 23-year-old female; Blacksburg, VA, USA GQ131417 JN986585
11-26358 nk Urine, 56-year-old; FL, USA JN986581 JN986586
11-26359 nk Blood, >89-year-old; OH, USA JN986582 JN986587
11-26360 nk Blood, 19-month-old; LA, USA JN986583 JN986588
11-26361 nk Paracentesis fluid, 80-year-old; IL, USA JN986584 JN986589
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nk, Not known.

16S rRNA gene sequences (1463–1515 nt) were determined for the isolates as described previously (Dewhirst et al., 2010; Wolfgang et al., 2011); see Table 1 for GenBank accession numbers. Additionally, for strain F0314, the whole-genome shotgun sequence (accession no. ADEA01000039) had been deposited previously at GenBank as part of the Human Microbiome Project (Dewhirst et al., 2010; Nelson et al., 2010).

To identify the type strains most closely related to 6332T for inclusion in our polyphasic analysis, the blast (Altschul et al., 1997) and megablast (Zhang et al., 2000) search programs were used with the 16S rRNA gene sequence against the database of type strains of prokaryotic species with validly published names (Chun et al., 2007). The 50 sequences with the highest scores were then selected for the calculation of pairwise sequence similarity using the global alignment algorithm implemented at the EzTaxon server (http://www.eztaxon.org/; Chun et al., 2007). Five of the most similar type strains by sequence similarity (96.1–96.9 %) were acquired for this study, Neisseria lactamica LMG 26610T, N. animalis LMG 26609T, N. macacae LMG 26611T, N. elongata subsp. elongata LMG 5124T and N. sicca LMG 5290T.

Previous studies indicate that, for organisms with more than 97 % 16S rRNA gene sequence similarity, alternative methods must be employed, such as DNA–DNA hybridization, to determine inclusion with or exclusion from closely related species (Tindall et al., 2010). Although none of the most closely related organisms crossed this threshold, N. lactamica LMG 26610T, with a similarity of 96.9 %, was the closest, and so was selected for DNA–DNA hybridization analysis. DNA was purified as described by Logan et al. (2000) and hybridization was performed using the microplate method described by Ezaki et al. (1989), with modifications described by Willems et al. (2001). Means of two reciprocal hybridization values were determined for all pairwise combinations of strains 6332T, 8261 and 11-26358 and N. lactamica LMG 26610T (Table S1, available in IJSEM Online). Based on a 70 % cut-off value for defining species (Wayne et al., 1987), strains 6332T, 8261 and 11-26358 belong to the same species, and that species is distinct from N. lactamica.

For cellular fatty acid (CFA) analysis, the seven strains of N. oralis sp. nov. and the five most closely related type strains were cultured aerobically for 48 h on trypticase soy broth agar (TSBA) at 37 °C and harvested in late-exponential growth phase. Fatty acid methyl esters were prepared according to the manufacturer’s instructions (Sherlock Microbial Identification Systems; MIDI, Inc.) and analysed on an Agilent Technologies 6890N gas chromatograph. For the type strain 6332T, the predominant CFAs were C16 : 0, summed feature 3 (C16 : 1ω7c and/or iso-C15 : 0 2-OH) and C18 : 1ω7c. These were the same as the predominant CFAs of the most closely related type strains (Table 2). The variation seen among these strains in Table 2 was similar to that seen among the seven strains of N. oralis (Table S2). Hence, the CFA composition is concordant with assigning the novel species to the genus Neisseria, but is not useful in distinguishing among the species within the genus.

Table 2. CFA compositions of Neisseria type strains.

Strains: 1, 6332T; 2, N. elongata subsp. elongata LMG 5124T; 3, N. sicca LMG 5290T; 4, N. animalis LMG 26609T; 5, N. lactamica LMG 26610T; 6, N. macacae LMG 26611T. Values are percentages of total fatty acids, and were determined in this study. Fatty acid methyl esters for which no values were greater than 1 % were omitted. The three most prevalent fatty acids for each strain are in bold. nd, Not detected.

Fatty acid 1 2 3 4 5 6
Saturated
C12 : 0 7.8 5.8 8.9 6.9 9.6 5.2
C14 : 0 3.5 3.6 2.1 3.7 5.7 3.4
C16 : 0 33.7 33.7 19.4 34.7 34.3 31.4
C17 : 0 nd 1.1 nd nd nd nd
C18 : 0 0.4 0.7 0.3 1.0 0.4 0.3
Unsaturated
C16 : 1ω5c 0.2 nd 1.2 0.5 0.7 1.1
C17 : 1ω6c nd 0.3 0.2 1.3 nd nd
C18 : 1ω7c 17.4 21.4 20.8 19.0 11.2 14.6
Hydroxy
C12 : 0 3-OH 5.3 4.2 6.1 0.3 6.1 3.3
C16 : 0 2-OH nd nd 1.1 nd nd 1.9
Summed features*
Summed feature 2 3.3 2.9 4.0 7.9 3.6 2.6
Summed feature 3 27.5 25.4 33.8 24.2 27.6 35.3
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*

Summed features are groups of two or three fatty acids that cannot be separated by GLC with the MIDI System. Summed feature 2 contained one or more of C12 : 0 ALDE?, C14 : 0 3-OH and iso-C16 : 1 I. Summed feature 3 contained C16 : 1ω7c and/or iso-C15 : 0 2-OH.

Phylogenetic analysis was performed using nearly full-length 16S rRNA gene sequences from the seven strains of N. oralis and the top 50 blast hits returned for type strain 6332T from the EzTaxon database (Chun et al., 2007). These sequences were aligned using the clustal w utility in mega 4.0.2 (Tamura et al., 2007) and exported to PhyML 3.0 (Guindon & Gascuel, 2003). A rooted maximum-likelihood tree was recreated using the general time reversible model, six substitution rate categories and five random starting trees (Guindon & Gascuel, 2003). Tree reliability was evaluated using the approximate likelihood ratio test (aLRT) (Anisimova & Gascuel, 2006) (Fig. 1). The seven novel strains reside in a well-supported clade that harbours N. lactamica as its closest relative as well as N. elongata, two species of Kingella and the one species of Eikenella. The other most closely related species (based on sequence distance) reside in other, distinct clades (Fig. 1).

Fig. 1.

Fig. 1.

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Maximum-likelihood phylogenetic tree reconstructed from 16S rRNA gene sequences of strains of N. oralis sp. nov. and the 50 closest taxa returned from a blast search of the EzTaxon database. The tree was rooted with Oligella ureolytica DSM 18253T. Branch probability is indicated at nodes and was determined by the aLRT; probabilities below 50 % are not shown. Bar, 0.01 expected changes per site.

To seek further support for the novel species designation, 23S rRNA gene sequences were determined for the seven new isolates as well as the five most closely related type strains. Sequencing was performed as described previously (Wolfgang et al., 2011). Sequence similarity for the seven novel strains ranged from 99.4 to 100 %. A maximum-likelihood tree was reconstructed from sequences generated in this study as well as sequences from closely related species for which data were available at GenBank (Fig. S1) (note that the 23S rRNA gene sequence was not available for the type strain of some species; e.g. the sequence of strain MS11 was used for Neisseria gonorrhoeae). The seven isolates of N. oralis formed a clade that is distinct from all other Neisseria species, further supporting the novel species designation.

As in other studies, our phylogenetic analysis using the 16S rRNA gene sequence reveals that the genus Neisseria is polyphyletic (Vandamme et al., 2006; Wolfgang et al., 2011). We found that N. oralis resides in a well-supported clade that harbours two additional species of Neisseria, two species of Kingella and Eikenella corrodens (Fig. 1). This clade is distinct from the clade that harbours the type species of the genus, N. gonorrhoeae. As such, it is necessary to identify additional characters that support or reject the inclusion of the novel species in closely related genera. Characteristics that support inclusion of our isolates in the genus Neisseria are the formation of Gram-negative-staining cocci, the presence of catalase and oxidase activities, the absence of motility and the CFA profile (Tønjum, 2005; Weyant et al., 1984). Characteristics that support exclusion from closely related genera are the absence of catalase activity in the genera Bergeriella, Eikenella and Kingella, the formation of long filaments and gliding motility in the genera Alysiella, Simonsiella and Conchiformibium, which additionally reside in distinct clades (Tønjum, 2005), and the fact that the single species of the genus Uruburuella falls in a separate clade and has additional characters that distinguish it from our isolates (Vela et al., 2005).

Characteristics that aid in distinguishing all seven strains of N. oralis from the closely related type strains examined in this study are the ability to reduce nitrate, the absence of acid phosphatase activity and acid production from d-glucose, maltose and sucrose (Tables 3 and S3) [for methods, see Forbes et al. (1998) and Kohlerschmidt et al. (2009)]. Other species, not analysed in this study, that may also be excluded on the basis of the absence of nitrate reduction are N. gonorrhoeae, N. cinerea, N. dentiae, N. flavescens, N. meningitidis, N. subflava, N. weaveri and N. polysaccharea (Janda & Gaydos, 2007; Tønjum, 2005). For the remaining taxa that reduce nitrate, with the exception of Neisseria mucosa and N. elongata subsp. nitroreducens, the absence of acid production from glucose, maltose and/or sucrose is diagnostic. For N. mucosa and N. elongata subsp. nitroreducens, the presence of large mucoid colonies or rod-shaped cells, respectively, are diagnostic.

Table 3. Characteristics that distinguish N. oralis sp. nov. from closely related species.

Strains/species: 1, N. oralis sp. nov. 6332T; 2, N. elongata subsp. elongata LMG 5124T; 3, N. sicca LMG 5290T; 4, N. animalis LMG 26609T; 5, N. lactamica LMG 26610T; 6, N. macacae LMG 26611T; 7, N. gonorrhoeae [data from Janda & Gaydos (2007) and the bioMérieux package insert]. Data were obtained in this study unless indicated otherwise. nd, No data available. Characteristics listed for 6332T were the same for all seven strains of N. oralis sp. nov. (see Table S3).

Characteristic 1 2 3 4 5 6 7
Acid production (peptone water) from:
 d-Glucose + − − − + + +
 Maltose + + + − + + −
Nitrate reduction + − − − − − −
Catalase reaction + + + + + − +
Acid production (API NH) from:
 d-Glucose + − + − + − +
 Maltose + − − − − − −
 Sucrose + − − + − − −
Enzyme activity (API NH)
 Proline 4-methoxy-β-naphthylamide + + + − + + +
 γ-Glutamyl 4-methoxy-β-naphthylamide + − − − − + −
Enzyme activity (API ZYM)
 Esterase (C4) − + − + + + nd
 Acid phosphatase − + + + + + nd
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Based on the 16S and 23S rRNA gene sequence comparisons, DNA–DNA hybridization, CFA composition and phenotypic and phylogenetic analyses, we propose that the seven novel strains (Table 1) represent a single novel species, Neisseria oralis sp. nov.

Description of Neisseria oralis sp. nov.

Neisseria oralis (o.ra′lis. N.L. fem. adj. oralis of the mouth, the source of the first isolate).

Colonies are small, circular, entire, raised, moist, yellow, weakly α-haemolytic (except 11-26358, which is β-haemolytic) and 1–1.5 mm in diameter after 48 h of growth at 37 °C in 5 % CO2. Facultative anaerobe. Growth is observed at 28 and 42 °C, with no growth at 10 °C. No growth is observed on MacConkey agar after 5 days. Cells are Gram-negative, 0.5 µm in diameter, may be present in chains and are non-motile. Produces catalase and cytochrome oxidase and reduces nitrate to nitrite. Negative for acid production using Hugh & Leifson O-F base with 1 % d-mannitol and d-xylose and displays interstrain variability (see Table S3 for details) for d-glucose (6/7 positive; type strain positive), maltose (6/7 positive; type strain positive), lactose (2/7 positive; type strain negative) and sucrose (5/7 positive; type strain positive). Positive for acid production in peptone water base with 1 % d-glucose and maltose and negative for acid production from adonitol, l-arabinose, dulcitol, inositol, d-mannitol, raffinose, d-rhamnose, d-salicin, d-sorbitol and d-xylose; displays interstrain variability for acid production from lactose (3/7 positive; type strain negative) and sucrose (6/7 positive; type strain positive). Negative for utilization of Simmons’ citrate, hydrolysis of aesculin, urea and gelatin, indole production, decarboxylation of arginine, lysine and ornithine using Moeller’s decarboxylase medium and production of H2S in triple-sugar iron agar [for methods, see Forbes et al. (1998) and Kohlerschmidt et al. (2009)]. Using the API NH system (bioMérieux), positive for acidification of d-glucose, maltose and sucrose and for the presence of proline arylamidase and γ-glutamyl transferase activities and negative for penicillinase, lipase, alkaline phosphatase and indole production; displays interstrain variability for acidification of d-fructose (6/7 positive; type strain negative), ornithine decarboxylase (1/7 positive; type strain negative), urease (2/7 positive; type strain negative) and β-galactosidase (2/7 positive; type strain negative). Using the API ZYM system (bioMérieux), displays interstrain variability for leucine arylamidase (3/7 positive; type strain positive) and β-galactosidase (2/7 positive; type strain negative) and is negative for all other activities tested in the kit. The DNA G+C content of the type strain is 52.6 mol%. The predominant CFAs are C16 : 0, summed feature 3 (C16 : 1ω7c and/or iso-C15 : 0 2-OH) and C18 : 1ω7c.

The type strain, 6332T ( = LMG 26725T  = DSM 25276T), was isolated from whole blood of a 55-year-old male in New York, USA. Details of other strains are given in Table 1.

Acknowledgements

The authors wish to thank the Wadsworth Center Applied Genomic Technologies Core and the Broad Institute of MIT and Harvard for sequencing, the Wadsworth Center Orphan Bacterium Collection for curation of the novel strains described in this study, Margo Cnockaert for assistance with the DNA hybridization studies and Dr Andrea Habura for helpful discussions relating to the phylogenetic analysis of the novel species. A. C. received a grant from the research fund of University College Ghent. F. E. D. and J. I. were supported by NIDCR grant DE016937.

Abbreviations:

CFA

cellular fatty acid

Footnotes

Three supplementary tables and a supplementary figure are available with the online version of this paper.

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