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Wolinella Recta, Wolinella Curva, Bactevoides Ureolyticus, and Bactevoides Gvacilis Are Microaerophiles, Not Anaerobes Y.-H

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Wolinella Recta, Wolinella Curva, Bactevoides Ureolyticus, and Bactevoides Gvacilis Are Microaerophiles, Not Anaerobes Y.-H INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Apr. 1991, p. 218-222 Vol. 41, No. 2 0020-7713/91/020218-05$02.00/0 Copyright 0 1991, International Union of Microbiological Societies Wolinella recta, Wolinella curva, Bactevoides ureolyticus, and Bactevoides gvacilis Are Microaerophiles, Not Anaerobes Y.-H. HAN,l R. M. SMIBERT,2 AND N. R. KRIEG1* Microbiology and Immunology Section, Department of Biology, and Department of Anaerobic Microbiology,2 Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061 Although the nonfermentative, asaccharolytic, putative anaerobes Wulinella curva, Wolinella recta, Bacterui- des ureolyticus, and Bacteroides gracilis are phylogenetically related to the true campylobacters, the type strains of these species exhibited 0,-dependent microaerophilic growth in brucella broth and on brucella agar. The optimum 0, levels for growth of these strains ranged from 4 to 14% in brucella broth and from 2 to 8% on brucella agar, when H, was provided as the electron donor. No growth occurred under 21% O,, and scant or no growth occurred under anaerobic conditions unless fumarate or nitrate was provided as a terminal electron acceptor. Aspartate, asparagine, and malate also served as apparent electron acceptors. The organisms were catalase negative and, except for B. gracilis, oxidase positive. Catalase added to brucella broth enhanced growth. 0, uptake by all species was inhibited by cyanide and 2-heptyl-4-hydroxyquinolineN-oxide. We concluded that these organisms are not anaerobes but instead are microaerophiles, like their campylobacter relatives. Among the proteobacteria, a major taxonomic problem (21), it is oxidase positive, a characteristic usually associated has been finding phenotypic characteristics that correlate with organisms that can respire with 02.This raises the with the various phylogenetic groups delineated by rRNA question of whether W. succinogenes is in fact an anaerobe. analyses. This problem is exemplified by studies of campylo- Although W. succinogenes grows anaerobically by using bacters and campylobacter-like organisms. On the basis of fumarate as a terminal electron acceptor (5,6, 10-13), Wolin the results of rRNA sequence analyses (15), the nonfermen- et al. (24) and Jacobs and Wolin (5, 6) have shown that it is tative, asaccharolytic , putative anaerobes Wolinella recta, also capable of using 0, as a terminal electron acceptor Wolinella curva, Bacteroides ureolyticus, and Bacteroides under microaerobic conditions (approximately 2% 0,). Be- gracilis belong to the “true campylobacters,” a group that cause anaerobes do not use 0, as a terminal electron includes all Campylobacter species except Campylobacter acceptor for respiration, W. succinogenes must be consid- cryaerophila , Campylobacter nitrofigilis, Campylobacter ci- ered a H,-requiring microaerophile. naedi, and Campylobacter fennelliae, as well as Helicobac- Similarly, W. recta, W. curva, B. ureolyticus, and B. ter pylori (formerly called Campylobacter pylori) (14, 17, gracilis are presently considered to be anaerobes (4, 19-21), 23). The addition of the two Wolinella and two Bacteroides but their phylogenetic placement with the campylobacters, species to the true campylobacters makes it difficult to as well as the fact that three of the species (W. recta, W. describe the group in phenotypic terms. These four species curva, and B. ureolyticus) are oxidase positive, suggests that do resemble campylobacters in the following respects: (i) they may actually be microaerophiles. This would make like campylobacters, W. recta and W. curva are motile by their inclusion with the true campylobacters much more means of polar flagella; (ii) W. recta, W. curva, and B. satisfying in phenotypic terms. Some previous reports sug- ureolyticus are oxidase positive; (iii) W. curva has a vibrioid gest that this may be the case. Tanner et al. (19,20) reported shape; and (iv) like some campylobacters (Campylobacter that some strains of W.recta, W. curva, and B. gracilis could concisus, Carnpylobacter mucosalis, C. cinaedi, and C. grow under microaerobic conditions (4%0,). Jackson and fennelliae), W. recta, W. curva, B. gracilis, and B. ureolyti- Goodman (4) showed that B. ureolyticus could grow under cus all require H, or formate as an electron donor. However, microaerobic conditions and that it has cytochrome b and there are some important differences: (i) W. recta, B. ureo- cytochrome c. However, it has not been shown previously lyticus, and B. gracilis are straight rods; (ii) B. ureolyticus that these organisms are capable of 0,-dependent growth. In and B. gracilis are nonmotile; (iii) B. gracilis is oxidase this report, we provide evidence in support of this conten- negative; and (iv) W. recta, W. curva, B. gracilis, and B. tion. ureolyticus have all been considered to be anaerobes. The latter difference seems to be a particularly fundamental difference. MATERIALS AND METHODS The problem of including anaerobes with microaerophiles in a phylogenetic group existed previously in another group, Bacterial strains. The strains used in this study were W. viz., rRNA group I1 of Thompson et al. (23). This group curva ATCC 35224T (T = type strain), W. recta ATCC contains the putative anaerobe Wolinella succinogenes and 3323gT, B. ureolyticus NCTC 10941T, and B. gracilis ATCC the microaerophiles H. pylori, C. cinaedi, and C. fennelliae 33236T. Stock cultures were grown under an atmosphere (14,17, 23). Although W. succinogenes was described as an containing 6% O,, 3% CO,, 23% N,, and 68% H, at 37°C in anaerobe of Bergey ’s Manual of Systematic Bacteriology semisolid brucella medium (brucella broth [Difco] supple- mented with 0.15% agar) and transferred weekly. Inocula and general culture conditions. The top 1 cm was removed from a 2-day-old culture grown in semisolid bru- * Corresponding author. cella medium and mixed to yield a homogeneous suspension. 218 VOL.41, 1991 MICROAEROPHILIC BACTERIA 219 One drop (0.05 ml) of this suspension was inoculated into TABLE 1. Growth responses of Wolinellu and Bucteroides each 5-ml portion of test broth. For inoculation of agar species in brucella broth in the presence of different 0, media, one loopful of the suspension was streaked over the concentrations when H, was used as the electron donor" entire surface of a test slant or plate. Turbidity (optical density at 660 nm) For testing growth responses in liquid media, organisms 0, concn (%Ih were cultured in 5-ml volumes of media contained in 50-ml W. curvu W.rectu B. ureolyticus B. gracilis cotton-stoppered serum bottles. For testing growth re- 0 0.07 -+ 0.01' 0.07 -+ 0.01 0.05 -+ 0.01 0.05 L 0.01 sponses on solid media, organisms were cultured on 10-ml 2 0.37 t 0.04 0.21 5 0.01 0.57 2 0.13 0.18 t 0.02 agar slants or in petri plates containing 20 ml of medium. 4 0.44 -+ 0.01 0.30 * 0.01 0.72 -+ 0.07 0.18 t 0.02 Cultures were incubated statically at 37°C in sealed ves- 6 0.46 -+ 0.02 0.31 & O.Md 0.81 t 0.02 0.21 2 0.03 sels (Oxoid anaerobic jar system) equipped with a vent to 8 0.49 -+ 0.04 0.27 t 0.02 0.83 t 0.08 0.20 t 0.03 allow filling with various gas mixtures. Gas atmospheres 10 0.58 & 0.04 0.18 t 0.02 0.86 2 0.02 0.20 * 0.05 were obtained manometrically by evacuating the Oxoid jars 12 0.58 & 0.01 0.02 t 0.01 0.88 A 0.02 0.10 * 0.04 and refilling them with various combinations of CO,, H,, N,, 14 0.56 -+ 0.03 0.01 t 0.01 0.85 t 0.05 0.03 * 0.02 16 0.43 -+ 0.07 0.01 t 0.00 0.56 2 0.01 0.01 5 0.00 and 0,. When anaerobic conditions were required, 0, was 18 0.02 t 0.01 0.01 & 0.00 0.04 2 0.00 0.01 * 0.00 omitted and an activated palladium catalyst was used to 21 0.00 t 0.00 0.00 2 0.00 0.01 2 0.00 0.00 * 0.00 remove residual 0,. Measurement of growth. Growth responses in liquid media "Cultures were grown in 5-ml portions of brucella broth contained in cotton-stoppered SO-ml serum bottles and incubated at 37°C for 48 h. were estimated turbidimetrically at 660 nm with a Bausch & Jars containing the bottles were initially evacuated to various extents to Lomb Spectronic 2000 spectrophotometer by using 1-cm give the desired residual levels of oxygen manometrically. Carbon dioxide cuvettes. Growth responses on solid media were estimated (final concentration, 3%) was added, and the jars were restored to 1 atm by washing the cells from the agar surface with 5 ml of (101.29 kPa) with H,. When 0% 0, was desired (anaerobic conditions), a palladium catalyst was used to remove the residual 0,. When 21% 0, was physiological saline (0.85% NaCl) and measuring the turbid- desired, the jars were evacuated and pure 0, gas was added to give this level ity of the resulting suspension. of oxygen before addition of CO, and H,; this allowed a sufficient level of H2 Oxidase and catalase tests. The oxidase test was performed to be provided for growth of all four species, including W. recta, which by using 1% tetramethyl-p-phenylenediamine dissolved in requires at least 30% H,. Values are the averages L standard deviations for three or four replicate dimethyl sulfoxide (22). Growth was removed with a plati- cultures. num wire loop from cultures grown on brucella agar slants Values in boldface type represent maximum growth responses. for 48 to 72 h. When the growth was smeared onto filter paper moistened with the test reagent, the development of a purple color within 10 s was considered positive.
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