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Chromobacterium, Eikenella, Kingella, Neisseria, Simonsiella

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Chromobacterium, Eikenella, Kingella, Neisseria, Simonsiella INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, July 1989, p. 258-266 Vol. 39, No. 3 0020-7713/89/030258-09$02.00/0 Copyright 0 1989, International Union of Microbiological Societies Chromobacterium, Eikenella, Kingella, Neisseria, Simonsiella, and Vitreoscilla Species Comprise a Major Branch of the Beta Group Proteobacteria by 16s Ribosomal Ribonucleic Acid Sequence Comparison: Transfer of Eikenella and Simonsiella to the Family Neisseriaceae (emend .) FLOYD E. DEWHIRST,’” BRUCE J. PASTER,’ AND PATRICIA L. BRIGHT’ Departments of Pharmacology’ and Microbiology,‘ Forsyth Dental Center, Boston, Massachusetts 021 15 The 16s ribosomal ribonucleic acid sequences of the type strain and three other strains of Eikenella corrodens, the type strains of Alcaligenes faecalis, Alcaligenes xylosoxydans subsp. denitrificans, Chromobac- terium fluviatile, Chromobacterium violaceum, Kingella denitrificans, Kingella kingae, and Pseudomonas cepacia, and a strain of Vitreoscilla stercoraria were determined by direct sequencing of bacterial ribosomal ribonucleic acid by a modified Sanger method. These sequences were compared with previously published sequences of Neisseria gonorrhoeae and Pseudomonas testosteroni and unpublished sequences of Nitrosolobus sp., Nitrosomonas europaea, Rhodocyclus gelatinosus, Rhodocyclus purpura, Simonsiella muelleri, and Spirillum volutans. All of the bacteria sequenced in this study were members of the beta group of the class Proteobacteria, formerly called “purple bacteria and their relatives.” A phylogenetic tree was constructed based upon the sequence homologies. One of the findings of this study is that Eikenella corrodens is related, as indicated by percentage of sequence homology, to the following organisms: Kingella denitrificans (97.7 %), Simonsiella muelleri (95.7%), Kingella kingae (96.2 %), Neisseria gonorrhoeae (95.1 %), Vitreoscilla stercoraria (94.4%), Chromobacterium violaceum (91.7 %), and Chromobacterium fluviatile (89.8 %). These bacteria constitute a newly recognized branch of the beta group Proteobacteria. The remaining species, including Pseudomonas cepacia, Alcaligenes faecalis, and Alcaligenes xylosoxydans subsp. denitrificans, are members of the major cluster of the beta group Proteobacteria. On the basis of our data we propose that the genera Eikenella and Simonsiella be placed in the family Neisseriaceae. The initial goal of this research was to determine the corrodens was most closely related to Chromobacterium phylogenetic position of Eikenella corrodens, a gram-nega- violaceum, with a level of sequence homology of 92%. As we tive, facultatively anaerobic, rod-shaped bacterium that has were completing the sequences for these organisms, the been implicated as a potential pathogen in periodontal dis- sequence for the 16s rRNA gene of IVeisseria gonorrhoene ease (14, 59). The lack of knowledge regarding the relation- was published (45). A sequence comparison indicated that ship of Eikenella corrodens to species in other genera is Neisseria gonorrhoeae and Eikenella corrodens had a level reflected by its placement in the “other genera” group of of sequence homology of 95%. This information prompted us facultatively anaerobic gram-negative rods in Bergey ’s Man- to examine three additional organisms, Kingella denitrifi- idof Systematic Bacteriology, vol. 1 (18). Sequencing of cans, Kingella kingae, and Vitreoscilla stercoraria, which ribosomal ribonucleic acid (rRNA) subunits has proven to be we believed would be closely related based upon the results an extremely powerful tool for determining the phylogeny of of 16s cataloging studies (66) and rKNA-deoxyribonucleic both procaryotes and eucaryotes (64). Rapid sequencing acid (DNA) hybridization studies (9-13, 46, 47). Thus, the methods now make it possible to determine the 16s rRNA expanded goal of this research was to examine the phylog- sequence for a bacterial strain in less than 1week (28). Using eny of the beta group Proteobacteriu. these methods, we obtained the sequence for the type strain Many of the bacterial species examined in this study are of Eikenella corrodens. By comparing the Eikenella corro- not commonly encountered and may be as unfamiliar to dens sequence with 125 eubacterial sequences in our data readers as they were to us prior to these studies. Therefore, base, we found that this organism is a member of the beta a brief description of these organisms is given below. These group of the class formerly called “purple Proteobacteria, bacteria have been isolated from a variety of habitats and are bacteria and their relatives” (52; Dewhirst and Paster, J. quite diverse in their phenotypic traits. Most of the organ- Dent. Res. 67[Special Issue]:395, abstract no. 2261, 1988). isms, even those normally found in soil and water, are The beta group of the Proteobacteria corresponds to rRNA superfamily III of De Ley (8). Because few beta group occasionally pathogenic for humans. Alcaligenes faecalis and subsp. (previ- Proteobacteria 16s rRNA sequences were available for Alcaligenes xylosoxydans denitrificans comparison to determine the position of Eikenella corrodens ously Alcaligenes denitrificans) occur in water and soil and within this group, sequences were obtained for Alcaligenes are saprophytic inhabitants of the intestinal tracts of verte- faecalis, Alcaligenes xylosoxydans subsp. denitrificans, brates (21, 22, 49). Strains have been isolated from clinical Chromobacteriirm jhviatile, Chromobacterium violaceum, samples of blood, urine, and purulent discharges (21,23,35). and Pseudomonas cepacia. Of these species, Eikenella Alcaligenes faecalis has received recent attention as the etiological agent of turkey coryza ( 31). Chromohacterium violacetun and Chromobacterium fluviatile are violet-pig- * Corresponding author mented organisms whose normal habitat is soil and water 258 VOL. 39. 1989 PHYLOGENY OF BETA GROUP PROTEOBACTERZA 259 TABLE 1. Sources and accession numbers of bacteria were harvested during the late logarithmic growth the strains sequenced phase. GenBank Isolation and purification of rRNA. rRNAs were isolated Organism Strain“ accession no.b and partially purified by a modification of the procedure of Pace et al. (38), as previously described (40). Alcaligenes faecalis ATCC 8750T M22508 16s rRNA sequencing. rRNA was sequenced by using a Alcaligenes xylosoxidans ATCC 15173T M22509 modified Sanger dideoxy chain termination technique in subsp. denitr$cans Chromobacterium violaceum ATCC 12472T M22510 which primers complementary to conserved regions were Chromo ha ct erium fluvia tile ATCC 33051T M22511 elongated by using reverse transcriptase (28). The details of Eikenella corrodens ATCC 23834T M22512 our protocol have been described previously (40). In these FDC 373 M22513 studies, four additional primers were used to obtain the FDC 558 M22514 complete 16s rRNA sequence except for about 50 bases at FDC 1073 M22515 the 3’-terminal end. The sequences for the additional primers Kingella denitrijkans ATCC 33394T M225 16 and the positions which they complement are as follows: Kingella kingae ATCC 23330T M22517 5’-ACTGCTGCCTCCCGT-3’, positions 344 to 358; 5’-CTA Pseudomonas cepacia ATCC 25416T M22518 CCAGGGTATCTAATC-3’, positions 786 to 803; 5’-GG Vitreoscilla stercoraria VT1 M22.519 TTGCGCTCGTTGCGGG-3’, positions 1,096 to 1,113; and ATCC, American Type Culture Collection; FDC, Forsyth Dental Center. positions 1,493 to Strain VTl was obtained from W. R. Strohl. 5’-TACGGYTACCTTGTTACGACT-3’,1,513 (Y indicates the presence of either cytosine or thymine The GenBank accession number for all 12 sequences is M22467. at a position; numbering is relative to the Escherichia coli sequence). All primers used in this study were purchased (36, 37, 50). There are isolated reports of fatal septicemia from the Microchemistry Department, Harvard Biolabs, caused by Chromobacterium violaceum (20). Eikenella cor- Harvard University, Cambridge, Mass. rodens is routinely isolated from human oral cavities. It has Data analysis. A program set for data entry, editing, been recovered from Bartholin’s gland, uterine, thyroid, sequence alignment, secondary structure comparison, ho- head and neck, and other abscesses as well as from cases of mology matrix generation, and dendrogram construction for endocarditis, meningitis, and osteomyelitis (3, 25, 41, 61; 0. 16s rRNA data was written in Microsoft QuickBASIC for Riche, V. Vernet, and P. Megier, Letter, Lancet ii:1089, use with an IBM PC-AT computer and other compatible 1987). Eikenella corrodens has been detected in elevated computers (40). Ribonucleic acid sequences were entered numbers from sites of periodontal tissue destruction and and aligned as previously described (40). Our sequence may be involved in periodontal disease (14, 59). Kingella database contains approximately 125 sequences comprised denitrijicans and Kingella kingae are occasional members of of sequences determined in our laboratory, previously pub- the rhinopharyngeal flora in humans (51). Kingella kingae lished sequences, and unpublished sequences provided to us has been recovered from cases of osteoarthritis, osteomyeli- by other scientists. In the beta group Proteobacteria, the tis, spondylitis, endocarditis, meningitis, and septicemia (5, sequences for Neisseria gonorrhoeae NCTC 8375T (T = 6,42). Pseudomonas cepacia (previously named Pseudomo- type strain) and Pseudomonas testosteroni ATCC 11996T nus multivorans and “Pseudomonas kingae” is both a (67) were obtained from the literature. Unpublished se- phytopathogen and,
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