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Isolation and Characterization of Capnocytophaga Bilenii Sp. Nov., a Novel Capnocytophaga Species Detected in a Gingivitis Subject

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Isolation and Characterization of Capnocytophaga Bilenii Sp. Nov., a Novel Capnocytophaga Species Detected in a Gingivitis Subject pathogens Article Isolation and Characterization of Capnocytophaga bilenii sp. nov., a Novel Capnocytophaga Species Detected in a Gingivitis Subject Angéline Antezack 1,2,3,4 , Manon Boxberger 3,4 , Bernard La Scola 3,4 and Virginie Monnet-Corti 1,2,3,4,* 1 Ecole de Médecine Dentaire, Faculté des Sciences Médicales et Paramédicales, Aix-Marseille Université, 27 Boulevard Jean Moulin, 13385 Marseille, France; [email protected] 2 Assistance Publique-Hôpitaux de Marseille (AP-HM), Hôpital Timone, Service de Parodontologie, 264, Rue Saint Pierre, 13385 Marseille, France 3 Institut de Recherche Pour le Développement (IRD), Assistance Publique-Hôpitaux de Marseille (AP-HM), MEPHI, Aix-Marseille Université, 27 Boulevard Jean Moulin, 13005 Marseille, France; [email protected] (M.B.); [email protected] (B.L.S.) 4 IHU Méditerranée Infection, 19–21 Boulevard Jean Moulin, 13005 Marseille, France * Correspondence: [email protected] Abstract: Capnocytophaga species are commensal gliding bacteria that are found in human and animal oral microbiota and are involved in several inflammatory diseases, both in immunocompromised and immunocompetent subjects. This study contributes to increased knowledge of this genus by characterizing a novel species isolated from a dental plaque sample in a male with gingivitis. We investigated morphological and chemotaxonomic characteristics using different growth conditions, temperature, and pH. Cellular fatty acid methyl ester (FAME) analysis was employed with gas chro- matography/mass spectrometry (GC/MS). Phylogenetic analysis based on 16S rRNA, orthologous Citation: Antezack, A.; Boxberger, average nucleotide identity (OrthoANI), and digital DNA–DNA hybridization (dDDH) relatedness M.; La Scola, B.; Monnet-Corti, V. were performed. The Marseille-Q4570T strain was found to be a facultative aerobic, Gram-negative, Isolation and Characterization of ◦ Capnocytophaga bilenii sp. nov., a elongated, round-tipped bacterium that grew at 25–56 C and tolerated a pH of 5.5 to 8.5 and an Novel Capnocytophaga Species NaCl content ranging from 5 to 15 g/L. The most abundant fatty acid was the branched structure Detected in a Gingivitis Subject. 13-methyl-tetradecanoic acid (76%), followed by hexadecanoic acid (6%) and 3-hydroxy-15-methyl- Pathogens 2021, 10, 547. https://doi. hexadecanoic acid (4%). A 16S rDNA-based similarity analysis showed that the Marseille-Q4570T org/10.3390/pathogens10050547 strain was closely related to Capnocytophaga leadbetteri strain AHN8855T (97.24% sequence identity). The OrthoANI and dDDH values between these two strains were, respectively, 76.81% and 25.6%. Academic Editor: Shigeki Kamitani Therefore, we conclude that the Marseille-Q4570T strain represents a novel species of the genus Capnocytophaga, for which the name Capnocytophaga bilenii sp. nov. is proposed (=CSUR Q4570). Received: 6 April 2021 Accepted: 30 April 2021 Keywords: Capnocytophaga; dental plaque; gingivitis; culturomics; sp. nov. Published: 1 May 2021 Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 1. Introduction published maps and institutional affil- iations. The genus Capnocytophaga (Gr. n. kapnos, smoke; N.L. fem. n. Cytophaga, a bacterial genus name; N.L. fem. n. Capnocytophaga, bacteria requiring carbon dioxide and related to the cytophaga) belongs to the large family Flavobacteriaceae and currently counts 10 species with a validly published and correct name [1]. Capnocytophaga species are primarily com- mensals of the oral cavity in humans and animals, especially dogs and cats. They are Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. recognized as opportunistic pathogens, leading to various extra-oral infections, including This article is an open access article severe sepsis [2], bloodstream infections [3], abscess [4,5], vertebral osteomyelitis [6], pneu- distributed under the terms and monia [7], and perinatal infections [8] in both immunocompetent and immunosuppressed conditions of the Creative Commons patients. In addition, Capnocytophaga species have been thought to play a role in cancer Attribution (CC BY) license (https:// development. For example, Capnocytophaga gingivalis has been identified as strongly corre- creativecommons.org/licenses/by/ lated with oral squamous cell carcinoma (OSCC) and has been described as a promising 4.0/). diagnostic marker [9,10]. The genus Capnocytophaga was also found in increased amounts Pathogens 2021, 10, 547. https://doi.org/10.3390/pathogens10050547 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, x FOR PEER REVIEW 2 of 14 Pathogens 2021, 10, 547 2 of 13 strongly correlated with oral squamous cell carcinoma (OSCC) and has been described as a promising diagnostic marker [9,10]. The genus Capnocytophaga was also found in in‐ creased amounts in the saliva of lung cancer patients [11]. Moreover, several studies have reportedin the salivamembers of lung of the cancer genus patients Capnocytophaga [11]. Moreover, as periodontal several studies pathogens have reported [12–14]. membersPerio‐ dontalof the diseases genus areCapnocytophaga multifactorialas inflammatory periodontal pathogenspathologies [ 12that–14 are]. Periodontal characterized diseases by pro‐ are gressivemultifactorial destruction inflammatory of the tooth pathologies‐supporting that apparatus are characterized [15]. An increase by progressive in an abundance destruction of Capnocytophagaof the tooth-supporting species was apparatus found in [ 15subjects]. An increasewith gingivitis in an abundance [16] and periodontitis of Capnocytophaga [17]. Furthermore,species was the found genus in subjectsCapnocytophaga with gingivitis is one of [16 the] and main periodontitis sources of β‐ [17lactamases]. Furthermore, in the the genus Capnocytophaga is one of the main sources of β-lactamases in the oral cavity and oral cavity and constitutes the main oral reservoir of macrolide–lincosamide–strepto‐ constitutes the main oral reservoir of macrolide–lincosamide–streptogramin genes, adding gramin genes, adding to their pathogenicity [18]. to their pathogenicity [18]. In thisIn this study, study, we we used used the the rapid rapid and and precise precise routine routine identification identification by bymatrix matrix-assisted‐assisted laserlaser desorption desorption ionization ionization time time-of-flight‐of‐flight (MALDI (MALDI-TOF)‐TOF) mass mass spectrometry spectrometry (MS) (MS) for for the the identificationidentification of an of unknown an unknown strain, strain, which which was isolated was isolated from a from dental a plaque dental sample plaque from sample a 25from‐year a‐old 25-year-old male with male gingivitis. with gingivitis. The Marseille The Marseille-Q4570‐Q4570T strain wasT strain described was described using mor using‐ phologicalmorphological examinations examinations and biochemical and biochemical characteristics characteristics and compared and compared to its closely to its closely re‐ latedrelated phylogenetic phylogenetic neighbors. neighbors. We propose We propose for this for thisstrain strain the thespecies species name name CapnocytophagaCapnocytophaga bileniibilenii sp. sp.nov nov (=CSUR (=CSUR Q4570). Q4570). 2. Results2. Results 2.1.2.1. Strain Strain Identification Identification and and Classification Classification T TheThe Marseille Marseille-Q4570‐Q4570T strainstrain was was isolated isolated from from a adental dental plaque plaque sample sample of of a 25-year-old25‐year‐ T oldmale male with with gingivitis gingivitis living living in in Marseille, Marseille, France. France. TheThe Marseille-Q4570Marseille‐Q4570T strain could not be be identifiedidentified by MALDI MALDI-TOF‐TOF MS, as the score was lowerlower thanthan 1.8 (Figure(Figure1 1).). FigureFigure 1. MALDI 1. MALDI-TOF‐TOF MS MSreference reference mass mass spectrum spectrum for the for Marseille the Marseille-Q4570‐Q4570T strain.T strain. Spectra Spectra from from 12 individual12 individual colonies colonies were were compared compared and and a reference a reference spectrum spectrum was was generated. generated. T TheThe 16S 16S rDNA rDNA-based‐based similarity similarity analysis analysis of the of the Marseille Marseille-Q4570‐Q4570T strainstrain against against Gen Gen-‐ BankBank yielded yielded the the highest highest nucleotide nucleotide sequence sequence similarities ofof 97.24% 97.24% sequence sequence identity identity with Capnocytophaga leadbetteri T with Capnocytophaga leadbetteristrain strain AHN8855 AHN8855(GenBankT (GenBank accession accession no. no. NR_043464.1). NR_043464.1). As this value was lower than the 98.65% threshold for differentiating two species [19], the As this value was lower than the 98.65% threshold for differentiating two species [19], the Marseille-Q4570T strain was considered to be a potential new species within the genus Marseille‐Q4570T strain was considered to be a potential new species within the genus Capnocytophaga. The 16S rRNA gene sequence was deposited into GenBank under the accession number MW762958. The phylogenetic tree highlighting the position of the Marseille-Q4570T strain relative to other closely related species is shown in Figure2. Pathogens 2021, 10, x FOR PEER REVIEW 3 of 14 Capnocytophaga. The 16S rRNA gene sequence was deposited into GenBank under the ac‐ Pathogens 2021, 10, 547 3 of 13 cession number MW762958. The phylogenetic tree highlighting the position of the Mar‐ seille‐Q4570T strain relative to other closely related species is shown in Figure 2. FigureFigure
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