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Nitrate Reductase and Respiratory Adaptation in Bacillus Stearothermophilus R

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Nitrate Reductase and Respiratory Adaptation in Bacillus Stearothermophilus R JOURNAL OF BACTERIOLOGY, Feb., 1966 Vol. 91, No. 2 Copyright © 1966 American Society for Microbiology Prined fn U.S.A. Nitrate Reductase and Respiratory Adaptation in Bacillus stearothermophilus R. J. DOWNEY Lobund Laboratory, Department ofBiology, University ofNotre Dame, Notre Dame, Indiana Received for publication 13 September 1965 ABSTRACT DOWNEY, R. J. (University of Notre Dame, Notre Dame, Ind.). Nitrate reduc- tase and respiratory adaptation in Bacillus stearothermophilus. J. Bacteriol. 91:634- 641. 1966.-Bacillus stearothermophilus 2184 required nitrate to grow in the ab- sence of oxygen. Like many facultative microorganisms, the growth obtained anaerobically was considerably less than that obtained aerobically, even though the dissimilatory reduction of nitrate is, in effect, anaerobic respiration. The ability to re- duce nitrate depended on the induction of nitrate reductase. Although oxygen at low levels did not retard induction of the enzyme, enzyme synthesis was consider- ably lessened by aeration. A semisynthetic medium containing nitrate supported aerobic growth of the thermophile but did not support anaerobic growth. The adaptation to nitrate resulted in a decrease in the level of cytochrome oxidase nor- mally present in aerobically grown cells. Although the aerobic oxidation of suc- cinate by the respiratory enzymes from aerobically grown cells was inhibited by 2-N-heptyl-4-hydroxyquinoline-N-oxide, the anaerobic oxidation of succinate by nitrate in a similar preparation from nitrate-adapted cells was not. The nitrate reductase in the bacillus was strongly inhibited by cyanide and azide but not by carbon monoxide. The nitrate reductase catalyzed the anaerobic oxidation of re- duced nicotinamide adenine dinucleotide, and appeared to transfer electrons from cytochrome bi to nitrate. Cytochrome cl did not appear to be involved in the trans- fer. Bacillus stearothermophilus, like most aerobic dant serve to limit growth on a complex spore formers, utilizes an aerobic respiration medium. whenever the supply of oxygen permits. As a deni- In addition to describing the changes noted in trifler, the organism possesses the ability to respire the constitutive oxidative components of the anaerobically with nitrate as an oxidant. To do bacillus after adaptation to nitrate, this report so, an adaptive enzyme, nitrate reductase, must be includes some observations on the relationship synthesized. In addition to the presence of nitrate, of nitrate reductase to the respiratory chain, its one of the conditions necessary for induction of role in anaerobic oxidation of reduced nicotin- nitrate reductase appears to be a low oxygen amide adenine dinucleotide (NADH2), and its tension. An organism possessing both means of behavior in the presence of conventional respira- respiration presumably alters its oxidative tory inhibitors. mechanisms to suit the availability of the oxidant. Although the free energy available from nitrate MATERLALS AND METHODS reduction is less than that available via oxygen Organism, growth medium, and method of cultiva- respiration, it is conceivable that more extensive tion. B. stearothermophilus 2184 was grown on a use of the former could serve as a compensatory medium containing Trypticase (BBL), 20 g; yeast mechanism in meeting the biosynthetic require- extract, 10 g; FeCl136H20, 7 mg; MnCl2.4H20, 15 ments of growth. mg; MgSO4-7H2O, 15 mg; and sucrose, 5 g; in 1,000 Once a culture has adapted to nitrate, the ml of water. Potassium nitrate (1 g per liter) was used where indicated for anaerobic growth. After availability (solubility) of this oxidant, being autoclaving, the medium was adjusted to pH 7.4 considerably greater than oxygen, might permit with sterile KOH. Mass culture of aerobic cells was growth rates comparable to those obtained with achieved in shake flasks rotating at 200 rev/mnn in a oxygen. The experiments reported here show that New Brunswick gyrotary incubator describing a 1- factors other than the availability of an oxi- inch (2.5-cm) circle. Each flask contained 1 liter of 634 VOL. 91, 1966 NITRATE RESPIRATION IN B. STEAROTHERMOPHILUS 635 medium and received approximately 2.8 X 108 mid The NADH2 oxidase was assayed by a method de- log-phase cells as inoculum. After 5 hr of growth at scribed previously (4). The oxidation of NADH2 60 C, the cells were harvested and washed twice with nitrate as sole hydrogen acceptor was observed in phosphate buffer (0.067 M, pH 7.4) and 0.87% with Thunberg cuvettes. The reaction mixture con- KCl (1:1, v/v). tained 0.15 M phosphate buffer (pH 7.6), enzyme (300 Cultivation under anaerobic conditions was ,ug of protein), 20 mm KNO3, 0.72 mm NADH2, accomplished in large carboys (14 liters), filled to the and water to a final volume of 2 ml. When used, in- neck with sterile medium and sparged with purified hibitors were added to the final concentrations indi- nitrogen (300 ml/min) for 90 min prior to receiving cated in the text. After 10 min of preincubation at 1 liter of mid log-phase nitrate-adapted cells. After 6 60 C, the NADH2 was tipped in, and the change in hr of growth at 60 C, the cells were harvested and absorbance at 340 mMu was recorded for 3 to 5 min washed as above. in a Beckman DB spectrophotometer. The activity Growth curves were determined with the use of is expressed as micromoles of NADH2 oxidized per nephelometer flasks containing 100 ml of complex minute per milligram of protein. medium (TY), complex medium with sucrose (TYS), The oxygen consumption of aerobic cells and elec- complex medium with nitrate (TY-NO3), or complex tron-transport particles from such cells was deter- medium with sucrose and nitrate (TYS-NO3). For mined in a Gilson differential respirometer at 125 anaerobic growth, the screw-cap nephelometer flasks oscillations per min with air as the gas phase. The contained medium up to the neck. This was bubbled temperature used in these experiments was 55 C, the with nitrogen prior to addition of inoculum. The maximum attainable with the above instrument. flasks were not shaken. A minimal medium with or For the induction experiments, cells were grown without casein hydrolysate (17) was used in the study aerobically for 3 hr on TYS medium, harvested, of the induction of nitrate reductase. With either the and washed two times with sterile buffer-salts solution complex or minimal medium, the flasks were inocu- containing: Na2HPO4, 2.5 g; KH2PO4, 1.0 g; KCI, lated to an absorbancy of 0.1 to 0.15 and incubated 1.0 g; (NH4)2SO4, 1.0 g; FeCl3-6H20, 5 mg; MgCl2* at 60 C in a rotary shaker. The growth rate is expressed 6H20, 5 mg; and CaCl2-2H20, 5 mg; per liter of dis- by the constant (k) from the relationship dA/dt= tilled water. The washed cells were suspended in 100 kA. A is the absorbancy of the culture and t is the ml of the above buffer solution and added to 300 time in hours. The linear portion of semilogarithmic ml of the minimal medium supplemented with 0.1% plots of growth provided the values for k. casein hydrolysate. The flasks were inoculated to an Preparation of the particulate nitrate reductase. absorbancy of 0.10 to 0.15 and incubated at 60 C The electron transfer particles (ETP) were prepared for 5 to 6 hr. The medium was bubbled with nitrogen from washed sonically disrupted protoplast mem- for 30 min at 60 C prior to adding KNO3 (0.1%). branes of B. stearothermophilus (4). The bulk of Every 30 min during the 5-hr period of adaptation, nitrate reductase activity resided in a particulate samples (2.0 ml) were removed for assay of nitrate fraction obtained after a centrifugation at 140,000 X reductase and dry-weight determination. When in- g for 90 min. The pellet was resuspended in a solution dicated, chloramphenicol (50,ug/ml) was added to the containing 67 mm tris(hydroxymethyl)aminomethane medium. (Tris)-chloride buffer (pH 7.6), 5 mm MgCl2, and Determination of cytochromes. The cytochrome 30 mm KCI, and was sedimented at 60,000 X g for patterns in the ETP from aerobically and anaerobi- 60 min. The pellet, containing 87% of the total nitrate cally grown bacilli were determined by the difference reductase activity of the parent fraction, was used in spectra methods of Chance (2). The spectrum repre- the experiments reported here. sents the difference between oxidized and substrate Enzyme assay procedures. Nitrate reductase was (malate)-reduced particles. A few crystals of potas- assayed anaerobically in Thunberg tubes by the Diazo sium ferricyanide were added to each cuvette to oxi- coupling reaction for nitrate (10). The reaction mix- dize the components of the respiratory chain. Sub- ture contained 0.15 M phosphate buffer (pH 7.6), sequently, the cytochromes in the ETP were reduced enzyme (300 jig of protein), and water in the main by the addition of 0.1 ml of 0.25 M sodium malate to body, and 20 mM KNO3 and 15 mm sodium malate one of a pair of cuvettes. in the side arm, in a final volume of 2.0 ml. The vessel Determination of oxygen concentration during was evacuated and preincubated for 10 min at 60 C growth. The concentration of oxygen during growth prior to tipping in substrate. After 30 min, the tubes was monitored by use of a Clark electrode (Beckman were plunged into crushed ice, and 0.5 ml of 1.0% physiological gas analyzer, model 160). The macro- sulfanilamide was added immediately. After addition electrode was calibrated against 0.1 M phosphate buf- of 0.5 ml of 0.02% N-(l-naphthyl)-ethylenediamine fer (pH 7.4) saturated with oxygen at 60 C (700 ,AM). dihydrochloride to develop the color, the tube con- The electrode was inserted in the side port of a special tents were cleared of precipitate by sedimentation, the of the shake flask.
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