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Applied and Environmental Microbiology, October 2006, p. 6854-6858, Vol. 72, No. 10
0099-2240/06/$08.00+0     doi:10.1128/AEM.01216-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

SHORT REPORT

Response of the Microaerophilic Bifidobacterium Species, B. boum and B. thermophilum, to Oxygen{triangledown}

Shinji Kawasaki,* Tsuyoshi Mimura, Takumi Satoh, Kouji Takeda, and Youichi Niimura

Department of Biosciences, Tokyo University of Agriculture, Setagaya-ku, Tokyo 156-8502, Japan

Received 26 May 2006/ Accepted 10 August 2006


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ABSTRACT
 
We investigated the effects of O2 on Bifidobacterium species using liquid shaking cultures under various O2 concentrations. Although most of the Bifidobacterium species we selected showed O2 sensitivity, two species, B. boum and B. thermophilum, demonstrated microaerophilic profiles. The growth of B. bifidum and B. longum was inhibited under high-O2 conditions accompanied by the accumulation of H2O2 in the medium, and growth was restored by adding catalase to the medium. B. boum and B. thermophilum grew well even under 20% O2 conditions without H2O2 accumulation, and growth was stimulated compared to anoxic growth. H2O-forming NADH oxidase activities were detected dominantly in cell extracts of B. boum and B. thermophilum under acidic reaction conditions (pH 5.0 to 6.0).


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INTRODUCTION
 
Although anaerobes are defined as being unable to grow in the presence of O2, their degree of O2 sensitivity exhibits wide variation (2, 3, 10, 11, 14, 15, 16, 17, 18, 20, 21, 25, 28). The genus Bifidobacterium is a well-investigated anaerobe known to be beneficial to human health. Its sensitivity to O2 causes a loss of viability during manufacture and storage as well as after incorporation into the human body (36). The O2 sensitivity differs among strains and species (13). de Vries and Stouthamer (7) classified Bifidobacterium species into three categories according to their sensitivities to O2. They proposed that some O2-sensitive species produce H2O2 through NADH oxidase activity. Since then, there have been several approaches taken to investigate bifidobacterial oxidative growth inhibition (1, 6, 9, 32, 33, 37); however, the mechanism of growth inhibition under oxic conditions remains unclear.

In this study, microaerophilic Bifidobacterium species were found. The main objectives of the present study were to (i) determine growth characteristics with respect to O2 using several Bifidobacterium species, (ii) determine the factor responsible for aerobic growth inhibition using O2-sensitive species, (iii) investigate the metabolic properties of O2-sensitive and microaerophilic Bifidobacterium species under oxic growth conditions, and (iv) investigate the properties of O2 reduction systems that should differ between O2-sensitive and microaerophilic Bifidobacterium species.


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Effect of O2 on the growth of Bifidobacterium species.
 
Bifidobacterium species are classified as typical anaerobic bacteria; however, their differing degrees of O2 sensitivity in liquid shaking culture are not well characterized. We selected several species by referring to reports concerning the physiological effects of O2. B. bifidum, B. longum, B. breve, and B. infantis were selected from among strains often used in milk products and intestinal probiotics. B. asteroides is reported to possess catalase (13, 30). B. indicum has characteristics similar to those of B. asteroides but shows catalase activity only when hemin is added to the medium (13, 30). B. boum, B. globosum, and B. thermophilum are reported to form colonies under atmospheric conditions of 90% air-10% CO2 without the cells becoming catalase or pseudo-catalase positive (29, 31). Strains were grown at 37°C in modified MRS medium (without 0.5% sodium acetate) containing 1% (wt/vol) glucose, 1% proteose peptone, 0.2% beef extract, 0.5% yeast extract, 0.2% ammonium citrate, 0.02% MgCl2, 0.2% K2HPO4, and 0.005% MnSO4. The culture medium was sparged with O2-free N2 gas, and 30 ml of anoxic medium was transferred into 150-ml serum bottles with rubber tube stoppers, which were then sealed and autoclaved; the pH was approximately 6.7. To avoid the effect of CO2 on oxic growth, CO2-free gas was used in the anaerobic atmospheres. Sterile 100% O2 was added to the headspace of the culture bottles to the concentrations indicated. Headspace gas conditions were checked with a Shimadzu GC-14 gas chromatograph equipped with a thermal conductivity detector and a Shincarbon-ST column (Shimadzu, Tokyo, Japan). Anoxically grown strains were inoculated into the sealed serum bottles, and the bottles were placed horizontally and cultured with vigorous shaking (150 rpm) at 37°C. After inoculation, the starting medium pH decreased to 6.2 or 6.3. Most of the species, except B. boum and B. thermophilum, showed significant growth inhibition under 20% O2-80% N2 conditions (Table 1).


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  		TABLE 1. Growth of Bifidobacterium species in liquid shaking culture under 20% O2-80% N2 conditions

The growth profiles of the selected species are shown in Fig. 1. B. bifidum, a type species of the genus Bifidobacterium, stopped growing under 10% O2. B. longum stopped growing under 10% O2, but, interestingly, growth under 5% O2 was stimulated compared to anoxic growth. B. boum and B. thermophilum grew well in the presence of O2, and their growth was stimulated compared to that under anoxic conditions. The growth of B. boum and B. thermophilum reached a maximum at 16 h after inoculation, when approximately 2% to 3% of the starting O2 in the headspace (5%, 10%, and 20% O2) was consumed. The growth of B. thermophilum under 20% O2 was sometimes completely halted at the initial phase of growth, accompanied by the production of H2O2 (approximately 20% of cultures showed arrested growth; otherwise, the cultures grew well) (Fig. 1; Table 2).


Figure 1
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  		FIG. 1. Growth of Bifidobacterium species under various oxygen conditions in liquid shaking culture. Growth was measured as the increase in optical density at 660 nm (OD660) by taking 0.2 ml of the 30-ml culture into a gas-tight syringe. Circles, 100% N2 cultures; squares, 5% O2-95% N2 cultures; triangles, 10% O2-90% N2 cultures; and diamonds, 20% O2-80% N2 cultures. The growth of B. thermophilum was sometimes arrested in cultures grown under 20% O2-80% N2 (dashed line).


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  		TABLE 2. Growth and H2O2 accumulation of Bifidobacterium species under 0% to 20% O2 conditionsa


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Determination of H2O2 production and growth recovery by catalase.
 
The accumulation of H2O2 in the culture medium was measured. The culture supernatants were diluted 6:4 with a solution containing 0.01% horseradish peroxidase, 0.2% Triton X-100, and 0.63 mM o-dianisidine dihydrichloride in 50 mM acetate buffer, pH 5.0. The production of H2O2 was monitored spectrophotometrically at 460 nm by detecting the oxidation of o-dianisidine dihydrochloride (4). In all samples in which growth inhibition was observed, H2O2 accumulation was detected (Table 2). No H2O2 accumulation was seen in the culture medium of B. boum or B. thermophilum under 0% to 20% O2 conditions.

The growth inhibition of B. bifidum and B. longum under 20% O2 conditions was partially reversed when catalase (Roche, Japan) was added to the medium (Table 2). The inability of exogenously added catalase to decompose intracellular H2O2 might be a reason for the failure to obtain complete growth recoveries. These results indicate that the primary factor in aerobic inhibition is the production of H2O2 derived from O2 reduction.


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Fermentation under various O2 concentrations.
 
Glucose consumption and fermentation products in the late exponential phase of growth under various O2 concentrations were analyzed. Glucose consumption as well as acetate and lactate production were determined with a Waters LC module 1-plus high-performance liquid chromatograph equipped with a Shodex RI detector and a Shodex SH1011 column (300 mm by 8 mm; Shodex, Tokyo, Japan); the column temperature was 60°C, and the mobile phase was 0.01 N H2SO4 at a flow rate of 1.0 ml/min. Data are the means of two independent experiments. The mean standard deviations were less than 5%. In the absence of O2, B. bifidum, B. boum, and B. thermophilum showed similar lactate/acetate molar ratio profiles (glucose consumed:acetate produced:lactate produced, 1:1.34:0.82 [for B. bifidum], 1:1.32:1.14 [B. boum], and 1:1.29:1.03 [B. thermophilum]). B. longum showed the highest production of lactate among the tested species (1:1.17:1.49). In the presence of 5% O2, no dramatic change in the lactate/acetate production ratio was observed for B. bifidum and B. thermophilum. In the case of B. longum, a slight increase in acetate production and slight decrease in lactate production were observed (1:1.27:1.21). For B. boum, the ratio of acetate production was slightly decreased under 10% and 20% O2 conditions (1:1.02 to 1.18:0.91 to 0.93). No other fermentation products (CO2, acids, and alcohols from C1 to C6 other than acetate and lactate) were detected under any set of culture conditions (detected by gas chromatograph; data not shown). We expected an aerobic metabolic shift from lactate to acetate for B. boum and B. thermophilum as well because of the drainage of reducing power to O2, which has been speculated upon in some reports on lactic acid bacteria and Bifidobacterium species (5, 34, 35), but these metabolic shifts were not observed.


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Determination and characterization of NADH oxidase activities.
 
O2-sensitive Bifidobacterium species accumulated H2O2 under high-O2 conditions. Several reports have mentioned a correlation between the production of H2O2 and NADH oxidation activity (6, 7, 32, 33, 37). NADH oxidases have been divided into several groups based on their final reaction products: H2O, H2O2, O2–, or mixtures thereof (8, 12, 22, 23, 26, 38, 39). To our knowledge, none of the NADH oxidases in Bifidobacterium species have been characterized in terms of their function. To characterize the O2 reduction system in Bifidobacterium species, several substrate-dependent oxidase activities in cell extracts were tested using glucose, lactate, pyruvate, alanine, and NADH as electron donors. These oxidase activities were detected as the reduction of O2 monitored by an O2 electrode, as described previously (15, 16). The reactions were carried out under different pH conditions in sodium phosphate buffer (pH 5.0 to 7.0). None of the substrates other than NADH reduced O2. NADH-dependent H2O2 reductase activity, assayed anaerobically as described previously (15, 16, 18), was also detected in cell extracts of every tested species, but the activities were very low (0.5 to 1.8 mU/mg protein at a pH range of 5.0 to 7.0 in every tested species) compared to the NADH oxidase activities, and no significant inductions were detected by aeration. These activities are also very low compared to the activities detected in O2-tolerant species as reported by Shimamura et al. (approximately 100 mU/mg protein was detected in cell extracts) (33).

To investigate the difference in H2O2 accumulation profiles between O2-sensitive and microaerophilic species, the enzymatic properties of NADH-dependent oxidase activities were characterized. NADH-dependent oxidase activities from four tested species were potassium cyanide (2 mM) and NaN3 (2 mM) insensitive (no inhibitions were detected; data not shown), suggesting that those activities are not related to the cytochrome-type multiple-terminal oxidase activity (19). B. bifidum showed an optimum pH in the acidic region (28.8 mU/mg protein at pH 5.0, 21.4 mU/mg protein at pH 6.0, and 12.4 mU/mg protein at pH 7.0). B. longum showed the strongest activity among the tested species, with a pH optimum of 6.0 (64.6 mU/mg protein at pH 5.0, 77.8 mU/mg protein at pH 6.0, and 44.7 mU/mg protein at pH 7.0). B. boum showed rather low activity compared to B. bifidum and B. longum under all pH conditions (13.8 mU/mg protein at pH 5.0, 11.4 mU/mg protein at pH 6.0, and 13.8 mU/mg protein at pH 7.0). B. thermophilum also showed low activity (10.7 mU/mg protein at pH 5.0, 9.3 mU/mg protein at pH 6.0, and 10.4 mU/mg protein at pH 7.0). Aeration slightly increased the activity (about 1.2 to 1.5 times) of every tested species. Although total activity and the O2-induced properties of NADH oxidase activity did not differ significantly among species at any tested pH, the final reaction product differed significantly. H2O2 production from NADH oxidation was detected by monitoring O2 production with an O2 electrode after the addition of catalase to the NADH oxidation reaction (15, 16, 26, 27, 38). The ratio of H2O2-forming types of NADH oxidase activity in cell extracts was estimated by calculating the stoichiometric production of H2O2 during the NADH-dependent oxidase reaction, which is detectable by adding catalase to the reaction vessels (the H2O2-forming type of NADH oxidase produces 50% O2 after the addition of catalase to the total amount of O2 consumed by the NADH oxidase reaction) (15, 16, 26, 27, 38). The absence of O2– production by the NADH oxidase reactions was confirmed by monitoring the reduction of ferricytochrome c by O2– as described elsewhere (16, 23, 24, 38). As shown in Table 3, H2O2-forming NADH oxidase activity was predominant at all pH conditions in B. bifidum and B. longum. In B. boum, the NADH oxidase activity in the cell extract obtained from microoxically grown cells produced no H2O2 at all over the reaction pH range of 5.0 to 6.0. In the case of B. thermophilum, 10% to 20% of the NADH oxidase activity was of the H2O2-forming variety at pH 5.0 in CFE from anoxically grown cells, and this decreased to 0% in the CFE from microoxically grown cells.


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  		TABLE 3. Percentage of H2O2-forming NADH oxidase activity in the total NADH oxidase activity under different pH conditions


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Conclusions.
 
B. boum and B. thermophilum show growth stimulation in the presence of O2. These two species do not form colonies under air conditions, so they are reasonably classified as anaerobes. The accumulation of H2O2 in O2-sensitive species must be the end product of O2 reduction. NADH-dependent oxidase activities were detected as part of an O2 reduction system. Although the total activity of NADH-dependent oxidase in the CFE was similar among species, the activity profiles differed between O2-sensitive and microaerophilic species. Further investigation of NADH-dependent oxidase activity will clarify the difference in the H2O2 accumulation profiles of O2-sensitive and microaerophilic species.


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ACKNOWLEDGMENTS
 
We thank Tohru Kodama and Junichi Nakagawa for valuable discussions. We also thank Masahiro Nagasaku, Jun Anzai, Nobuko Sato, Shingo Tamaru, Mitsunori Todoroki, Tomoko Kohno, and Kurara Emi for helpful technical assistance at the Tokyo University of Agriculture.


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FOOTNOTES
 
* Corresponding author. Mailing address: Department of Bioscience, Tokyo University of Agriculture, 1-1-1 Setagaya-ku, Tokyo 156-8502, Japan. Phone: 81-3-5477-2764. Fax: 81-3-5477-2764. E-mail: kawashin{at}nodai.ac.jp. Back

{triangledown} Published ahead of print on 1 September 2006. Back


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Applied and Environmental Microbiology, October 2006, p. 6854-6858, Vol. 72, No. 10
0099-2240/06/$08.00+0     doi:10.1128/AEM.01216-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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