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Transfer of Kingella Indologenes (Snell and Lapage 1976) to the Genus Suttonella Gen

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Transfer of Kingella Indologenes (Snell and Lapage 1976) to the Genus Suttonella Gen INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Oct. 1990, p. 426-433 Vol. 40, No. 4 0020-7713/90/040426-08$02.00/0 Copyright 0 1990, International Union of Microbiological Societies Transfer of Kingella indologenes (Snell and Lapage 1976) to the Genus Suttonella gen. nov. as Suttonella indologenes comb. nov. ; Transfer of Bacteroides nodosus (Beveridge 1941) to the Genus Dichelobacter gen. nov. as Dichelobacter nodosus comb. nov. ; and Assignment of the Genera Cardiobacterium, Dichelobacter, and Suttonella to Cardiobacteriaceae fam. nov. in the Gamma Division of Proteobacteria on the Basis of 16s rRNA Sequence Comparisons FLOYD E. DEWHIRST,l* BRUCE J. PASTER,, SHARON LA FONTAINE,3 AND JULIAN I. ROOD3 Departments of Pharmacology' and Microbiology,2 Forsyth Dental Center, Boston, Massachusetts 021 15, and Department of Microbiology, Monash University, Clayton 31 68, Australia3 The 16s rRNA sequences of Kingella indologenes, Cardiobacterium horninis, and Bacteroides nodosus were determined by direct RNA sequencing, using a modified Sanger method. Sequence comparisons indicated that these three species represent a novel family in the gamma division of Proteobacteria. On the basis of these data, K. indologenes and B. nodosus cannot retain their current generic status as they are not closely related to other members of their assigned genera. Therefore, we propose transfer of K, indologenes to the new genus Suttonella as Suttonella indologenes and transfer of B. nodosus to the new genus Dichelobacter as Dichelobacter nodosus and assign the genera Cardiobacterium, Suttonella, and Dichelobacter to a new family, Cardiobacteriaceae, in the gamma division of Proteobacteria. Comparison of 16s rRNA sequences has proven to be goats, and cattle (33). Infected hooves are the only known extremely useful for determining phylogenetic relationships habitat of Bacteroides nodosus. Previous reports have also among eucaryotic and procaryotic organisms (46). Previ- indicated that Bacteroides nodosus is not closely related to ously, we sequenced the 16s rRNAs of a number of micro- other species of the genus Bacteroides and is generically organisms, including several species in the family Neisseri- misnamed (16, 19, 31, 37). Below we use brackets in refer- aceae, to determine the phylogeny of the beta division of ring to [Kingella] indologenes and [Bacteroides] nodosus to Proteobacteria (10). Sequence comparisons indicated that indicate that they do not belong in these genera. two of the microorganisms which we examined, Kingella indologenes and Cardiobacterium hominis, are not closely MATERIALS AND METHODS related to the Neisseriaceae, but rather are related to one Bacterial strains and culture conditions. The sources of the another as members of a novel family in the gamma division strains which we examined in this study are shown in Table of Proteobacteria. A subsequent comparison of a partial 1. Cardiobacterium hominis and [Kingella] indologenes sequence of the cloned 16s rRNA gene of Bacteroides were cultured aerobically at 37°C in commercially available nodosus (19) with the sequence of Kingella indologenes and Todd-Hewitt broth (BBL Microbiology Systems, Cockeys- Cardiobacterium hominis indicated that Bacteroides no- ville, Md.). [Bacteroides] nodosus was cultured on TAS dosus also belongs to this novel family. We determined (Trypticase-arginine-serine) agar at 37°C in an 80% N,-10% virtually the complete rRNA sequence of Bacteroides no- CO,-lO% H, atmosphere as described by Skerman (32). dosus in order to have a comparable number of bases for Isolation and purification of rRNA. rRNA was isolated and sequence comparisons with other species in our database. partially purified by using a modification of the procedure of The sequences of Cardiobacterium hominis, Kingella in- Pace et al. (24), as previously described (25). dologenes, and Bacteroides nodosus were compared with 16s rRNA sequencing. rRNA was sequenced by using a the sequences of nine beta division proteobacteria and nine modified Sanger dideoxy chain termination technique in gamma division proteobacteria in order to determine the which primers complementary to conserved regions were phylogenetic relationships among these bacteria. elongated by using reverse transcriptase (20). The details of Cardiobacterium hominis is an occasional resident of our protocol have been described previously (10, 25). human respiratory tracts and has been recovered from blood Data analysis. A program set for data entry, editing, samples of humans with endocarditis (18, 34, 45, 48). Kin- sequence alignment, secondary-structure comparison, simi- gella indologenes has been recovered from human eye larity matrix generation, and dendrogram construction for infections and from the blood of a patient with endocarditis 16s rRNA data was written in Microsoft QuickBASIC for (15, 39, 42). It has been reported previously that Kingella use on IBM PC-AT and compatible computers (25). RNA indologenes is not closely related to other Kingella species sequences were entered and aligned as previously described (10, 28) and thus is generically misnamed. Bacteroides (25). Our sequence database contains approximately 200 nodosus is the essential causative agent of footrot in sheep, sequences, including sequences determined in our labora- tory, previously published sequences, and unpublished se- quences provided to us by other scientists. Nine beta and * Corresponding author. nine gamma division proteobacteria were chosen for com- 426 VOL.40, 1990 CARDIOBACTERIACEAE FAM. NOV. 427 TABLE 1. Sources and accession numbers of the strains studied tree was calculated by using a modified unweighted pair group method in which differing branch lengths reflected Accession Refer- Organism StrainU no.‘ ence“ differing numbers of base changes relative to the other species in the tree. The root of the tree was established by Sequenced organisms performing several analyses, using multiple alpha or beta Cardiobacterium hominis ATCC 16826T M35014 division proteobacteria or more distantly related eubacteria [Kingella]indologenes ATCC 25869T M35015 as outgroups. Cardiobacterium hominis, [Kingella] indolo- [Bacteroides]nodosus 198A M35016 Reference organisms: gamma genes, and [Bacteroides] nodosus formed a cluster with an division average level of similarity of 93%; we refer to this cluster Escherichia coli rrnB cistron 501695 4 below as the Cardiobacteriaceae cluster. This cluster Proteus vulgaris Monteil 501874 6 branched deeply within the gamma division of the Proteo- Actinobacillus lignieresii ATCC 19393T M35017 A bacteria. The position of the tree root was somewhat sensi- Pasteurella multocida NCTC 10322T M35018 A tive to selection of the outgroup. The Cardiobacteriaceae Haemophilus influenzae ATCC 33391T M35019 A cluster occasionally branched as a deep member of the beta Ruminobacter amylophilus DSM 1361T NA 22 division of the Proteohacteria. An analysis of positions Oceanospirillum linum ATCC 11336T M22365 B which normally differentiate the beta and gamma divisions of Pseudomonas aeruginosa ATCC 25330 M34133 B Chromatium vinosum M. Madigan M26629 B the Proteobacteria indicated that the organisms included in Reference organisms: beta the Cardiobacteriaceae cluster possessed 8 gamma division division signatures and 4 beta division signatures, whereas the Eikenella corrodens ATCC 23834T M22512 10 slightly less deeply branching organism Chromatium vino- Neisseria denitrijkans ATCC 14686T M35020 A sum and other gamma division organisms possessed 12 of 12 Kingella denitrijicnns ATCC 33394T M22516 10 gamma division signatures and the 9 beta division species Neisseria gonorrhoeae NCTC 8375T X07714 27 contained 12 of 12 beta division signatures. Thus, the results Kingella kingae ATCC 23330T M22517 10 of the signature analysis supported placement of the Cardio- Spirillum volutans ATCC 19554T M34131 B bacteriaceae cluster as a deep branch of the gamma division Alcaligenes faecalis ATCC 8750T M22508 10 Rhodocyclus pupura M. Madigan M34132 B of the Proteobacteria. [Pseudomonas]cepacia ATCC 25416T M22518 10 DISCUSSION a ATCC, American Type Culture Collection, Rockville, Md.; DSM, Deut- sche Sammlung von Mikroorganismen, Braunschweig, Federal Republic of Germany; NCTC, National Collection of Type Cultures, London, United Until recently, the phylogenetic position of Cardiobacte- Kingdom. rium horninis relative to other genera was unknown, as Sequences are available for electronic retrieval from GenBank under the demonstrated by the placement of this organism in “other accession numbers given. These sequences should also be available from the genera of facultatively anaerobic gram-negative rods” in European and Japanese collections. NA, Not available from GenBank. A, Unpublished sequences deposited in GenBank by F. E. Dewhirst and Bergey ’s Manual of Systematic Bacteriology (45). There was B. J. Paster; B, unpublished sequences deposited in GenBank by C. Woese. suspicion that Cardiobacterium hominis was related to the family Neisseriaceae, although no DNA-DNA hybridization (40) or genetic transformation (41) was observed. While our parison with the three sequenced organisms. The reference work was in progress, rRNA cistron analysis placed Cardio- strains, their GenBank accession numbers, and literature bacterium hominis between rRNA superfamilies I and I1 and references are shown in Table 1. Phylogenetic trees were rRNA superfamily 111 (9, 28), which is equivalent to our constructed by using the modified unweighted pair group placement of this organism
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