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Revision of Campylobacter, Helicobacter, and Wolinella Taxonomy: Emendation of Generic Descriptions and Proposal of Arcobacter Gen

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Revision of Campylobacter, Helicobacter, and Wolinella Taxonomy: Emendation of Generic Descriptions and Proposal of Arcobacter Gen INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Jan. 1991, p. 88-103 Vol. 41, No. 1 0020-7713/91/010088-16$02.00/0 Copyright 0 1991, International Union of Microbiological Societies Revision of Campylobacter, Helicobacter, and Wolinella Taxonomy: Emendation of Generic Descriptions and Proposal of Arcobacter gen. nov. P. VANDAMME,l* E. FALSEN,2 R. ROSSAU,’t B. HOSTE,l P. SEGERS,l R. TYTGAT,l AND J. DE LEY’ Laboratorium voor Microbiologie en Microbiele Genetica, Rijksuniversiteit Gent, B-9000 Ghent, Belgium,’ and Culture Collection, Department of Clinical Bacteriology, University of Goteborg, S-413 46 Goteborg, Sweden2 Hybridization experiments were carried out between DNAs from more than 70 strains of Campylobacter spp. and related taxa and either 3H-labeled 23s rRNAs from reference strains belonging to Campylobacter fetus, Campylobacter concisus, Campylobacter sputorum, Campylobacter coli, and Campylobacter nitrofigilis, an unnamed Campylobacter sp. strain, and a Wolinella succinogenes strain or 3H- or 14C-labeled23s rRNAs from 13 gram-negative reference strains. An immunotyping analysis of 130 antigens versus 34 antisera of campylobacters and related taxa was also performed. We found that all of the named campylobacters and related taxa belong to the same phylogenetic group, which we name rRNA superfamily VI and which is far removed from the gram-negative bacteria allocated to the five rRNA superfamilies sensu De Ley. There is a high degree of heterogeneity within this rRNA superfamily. Organisms belonging to rRNA superfamily VI should be reclassified in several genera. We propose that the emended genus Campylobacter should be limited to Campylobacter fetus, Campylobacter hy ointestinalis , Campylobacter concisus, Campylobacter m ucosalis , Campylobacter sputorum, Campylobacter jejuni, Campylobacter coli, Campylobacter lari, and “Campylobacter upsaliensis. ” Wolinella curva and Wolinella recta are transferred to the genus Campylobacter as Campylobacter curvus comb. nov. and Campylobacter rectus comb. nov., respectively. Bacteroides gracilis and Bacteroides ureolyticus are generically misnamed and are closely related to the genus Campylobacter. Campylobacter nitrofigilis, Campylobacter cryaerophila, and an unnamed Campylobacter sp. strain constitute a new genus, for which the name Arcobacter is proposed; this genus contains two species, Arcobacter nitrofigilis comb. nov. (type species) and Arcobacter cryaerophilus comb. nov. Wolinellu succinogenes so far is the only species of the genus Wolinella. The genus Helicobacter is also emended; Campylobacter cinaedi and Campylobacter fennelliae are included in this genus as Helicobacter cinaedi comb. nov. and Helicobacter fennelliae comb. nov., respectively. The genus “Flexispira,” with “Flexispira rappini” as the only species, is closely related to the genus Helicobacter. The free-living, sulfur-reducing campylobacters do not belong to any of these genera; they probably constitute a distinct genus within rRNA superfamily VI. At present, the genus Campylobacter consists of 13 well- Dewhirst (39) found a close relationship between Wolinella defined species (40). Recently, two additional species, Cam- curva, Wolinella recta, Bacteroides gracilis, and Bacteroi- pylobacter pylori and Campylobacter mustelae, were in- des ureolyticus on the one hand and the so-called true cluded in the new genus Helicobacter as Helicobacter pylori campylobacters (i-e., the Campylobacter taxa belonging to and Helicobacter mustelae, respectively (20). The clinical rRNA homology group I of Thompson et al. [58] on the significance of all of these organisms was reviewed recently other. These Wolinella and Bacteroides species have been by Penner (40). A study of the taxonomic structure of the isolated from humans with both oral and nonoral infections genus Campylobacter in which partial 16s rRNA sequence (39). analysis was used revealed that the Campylobacter species It was the aim of this study to include all known campylo- can be divided into three major rRNA homology groups (58). bacters and possible relatives in a single phylogenetic study. The first homology group contains Campylobacterfetus (the Therefore, we selected reference strains of the 15 Campylo- type species of the genus Campylobacter), Campylobacter bacter and Helicobacter species, representative strains of hyoin testin ah , Campylo ba cter sp u torum , Campylo ba cter the saprophytic campylobacters (i.e. , the aspartate-ferment- jejuni, Campylobacter coli, Campylobacter lari (62) , “Cam- ing, free-living Campylobacter species of Laanbroek et al. pylobacter upsaliensis,” Campylobacter concisus, and [27] and Spirillum sp. strain 5175 of Wolfe and Pfennig [65]), Campylobacter mucosalis. The second rRNA homology and strain CLO-3 of Fennel1 et al. (16). In addition to these group contains Campylobacter pylori, Campylobacter fen- Campylobacter strains, we also included representative nelliae, and Campylobacter cinaedi; Wolinella succino- strains of Wolinella succinogenes, Wolinella curva, and genes, an organism found in bovine rumina, also belongs to Wolinella recta, and an unnamed Wolinella strain (57), as this second rRNA homology group. The third rRNA homol- ogy group consists of Campylobacter nitrojigilis and Cam- well as representative strains of Bacteroides gracilis, Bac- pylobacter cryaerophila. Furthermore, in another phyloge- teroides ureolyticus, and “Flexispira rappini,” which is a netic study of the genus Campylobacter, Paster and recently described organism that has been isolated from aborted fetuses (5, 26) and diarrheic stools (1). In order to study the genotypic coherence of these organ- * Corresponding author. isms and their phylogenetic relationships with other gram- t Present address: Innogenetics N. V., Antwerp, Belgium. negative bacteria, we used the DNA-rRNA hybridization 88 VOL.41, 1991 TAXONOMY OF rRNA SUPERFAMILY VI 89 technique of De Ley and De Smedt (11) and the immunotyp- cpmtpg for Campylobacter concisus CCUG 20534; 2,000 ing technique of Falsen (15). This enabled us to study several cpm/pg for Arcobacter nitrofigilis CCUG 12022; 70,000 strains of most taxa, whereas only single representative cpm/pg for CLO strain CCUG 10373; and 29,000 cpm/pg for strains have been included in previous partial 16s rRNA Wolinella succinogenes CCUG 13145T. These specific activ- sequence analyses (29, 39, 42, 58). ities were determined with a Beckman model 3310 Tri-Carb Below, we use the new names Campylobacter curvus, scintillation counter. Carnpylobacter rectus, Arcobacter nitrojigilis, Arcobacter DNA-rRNA hybridization experiments. Fixation of single- cryaerophilus, Helicobacter cinaedi, and Helicobacter fen- stranded DNAs on membrane filters, chemical determina- nelliae for the organisms formerly called Wolinella curva, tion of the amounts of DNAs on the filters, saturation Wolinella recta, Carnpylobacter nitrojigilis, Carnpylobacter hybridization, RNase treatment, and measurement of the cryaerophila, Carnpylobacter cinuedi, and Campylobacter thermostabilities of the hybrids were performed as described fennelliae, respectively. previously (11). We used labeled 23s rRNAs from Cumpylo- (Preliminary immunotyping results have been presented bacter, Arcobacter, and Wolinella strains (Table 2) and a previously [15a, 15bl.) variety of gram-negative reference strains (Table 3). Each DNA-rRNA hybrid was characterized by the following two MATERIALS AND METHODS parameters: (i) the melting temperature of elution [T,(,J, which was the temperature at which 50% of a DNA-rRNA Bacterial strains and growth conditions. All of the strains hybrid was denatured; and (ii) the percentage of rRNA used for DNA-DNA hybridization and DNA-rRNA hybrid- binding, which was a way to measure the amount of labeled ization experiments and the representative strains used for rRNA bound to 100 pg of filter-fixed DNA after RNase the immunotyping analysis are shown in Table 1. Names in treatment under standard conditions. A homologous duplex quotation marks have not been validly published. Below, the was formed between the DNA and the rRNA of the same genus names of all generically misnamed taxa are enclosed in strain; a heterologous hybrid was formed between DNA and brackets. Bacteriological purity was checked by plating and rRNA of different strains. The T,(,, is the most important examining living and Gram-stained cells. For mass cultures, parameter for drawing taxonomic conclusions (11, 13); the cells were grown on petri dishes on blood agar media higher the T,(,, of a heterologous hybrid, the more closely containing 5% (voVvol) horse blood and solidified with 1.8% the two strains are related. The Tm(e) values were used to agar. All Wolinella, Bacteroides, and saprophytic Campylo- calculate the average linkage level between each pair of bacter strains were incubated at 37°C in an anaerobic atmo- rRNA branches by using the unweighted average pair group sphere containing 5% CO,, 10% H2, and 85% N,. All other method (49). The percentage of rRNA binding can be useful strains except the Arcobacter nitrofigilis strains were grown for distinguishing strains with similar T,(,) values. The in a microaerophilic atmosphere containing approximately difference between the T,(,, of a homologous duplex and the 5% 0,, 3.5% CO,, 7.5% H,, and 84% N, at 37°C; the cultures Tmc,)of a heterologous hybrid is called the AT,,,,. of Arcobacter nitrofigilis strains were incubated at 30°C. The DNA-DNA hybridization experiments. The degree of DNA- strains to be used as antigens were incubated in
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