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Isolation of Anitrogen-Fixing Vibrio Species from the Roots of Eelgrass (Zostera Marina)

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Isolation of Anitrogen-Fixing Vibrio Species from the Roots of Eelgrass (Zostera Marina) J. Gen. App!. Microbiol., 33, 321-330 (1987) ISOLATION OF ANITROGEN-FIXING VIBRIO SPECIES FROM THE ROOTS OF EELGRASS (ZOSTERA MARINA) WUNG YANG SHIER, USIO SIMIDU, ANDYOSHIHARU MARUYAMA* Ocean Research Institute, University of Tokyo, Nakano, Tokyo 164, Japan * Department of Agricultural Chemistry, Faculty of Agriculture, University of Tokyo, Bunkyo, Tokyo 113, Japan A facultative nitrogen-fixing bacterium was isolated from the roots of eelgrass (Zostera marina) growing in Aburatsubo Inlet, Kanagawa Prefecture, Japan. The isolate grew anaerobically using molecular ni- trogen as the sole nitrogen source. However, NH4C1 could also serve as a nitrogen source, under either aerobic or anaerobic conditions. The nitrogenase activity of the isolate was very weak under aerobic conditions, but was easily detected within a few hours under anaerobic conditions. It was enhanced by some sugars and was Na +-dependent. Morphological, physiological, and biochemical characteristics, as well as the guanine-plus- cytosine content of its DNA (45.4 + 0.3 mol%) placed the isolate in the genus Vibrio of the family Vibrionaceae. The isolate was not identical to two previously described nitrogen-fixing species of the genus Vibrio, Vibrio diazotrophicus and Vibrio natriegens. Zostera marina (eelgrass) develops an extensive rhizome-root system beneath the sediment surface in coastal seawater. Different views have been presented on the importance of nitrogen fixation in supplying nitrogen to eelgrass (1-3). Although heterotrophic nitrogen fixation probably supplies a part of the nitrogen require- ment (4), nitrogen-fixing bacteria have not been isolated before this. In our preliminary study, we found that the nitrogenase activity of eelgrass roots was greatly enhanced by the addition of glucose under either aerobic or anaerobic conditions. The results indicate that heterotrophic nitrogen-fixing bac- teria are associated with the eelgrass roots. This report describes the isolation and characterization of a halophilic, facultatively anaerobic, nitrogen-fixing bacterium from eelgrass roots. Address reprint requests to: Dr. W. Y. Shieh, Ocean Research Institute, University of Tokyo, Minamidai 1-15-1, Nakano-ku, Tokyo 164, Japan. 321 322 SHISH, SIMIDU, and MARUYAMA VOL. 33 MATERIALS AND METHODS Media. A nitrogen-free liquid medium (NFL medium) used for the en- richment of nitrogen-fixing bacteria contained the following components: (i) basal medium (NaCI, 28 g; MgSO4.7H2O, 2 g; KBr,100 mg; SrCl2.6H2O, 26 mg; H3B03, 20 mg; Na2MoO4.2H2O, 10 mg; Tris, 50 mmol; distilled water, 800m1) adjusted to pH 7.8; (ii) glucose, 5 g; FeCl3.6H2O, 15 mg dissolved in 100 ml of distilled water; (iii) K2HPO4, 1 g dissolved in 50 ml of distilled water; (iv) sodium L-ascorbate, 0.5 g dissolved in 50 ml of distilled water. These were mixed after autoclaving separately. The PYG broth medium contained 2.0 g Polypepton (Daigo, Tokyo, Japan), 0.5 g Yeast extract (Difco), 5.0 g glucose, and 50 mmol Tris in 1 l of 9OO seawater. The pH was adjusted to 7.6. The PY medium was identical to PYG medium except that glucose and Tris were omitted. Isolation. Eelgrass roots were collected from an eelgrass field in Aburatsubo Inlet, Kanagawa Prefecture, Japan, and were washed free of sediment by vigorous shaking in sterile seawater. To measure the nitrogenase activity of the eelgrass roots, 1-g, wet weight, samples were placed in 20-m1 test tubes. To each tube was added 2 ml of seawater buffer (20 mM Tris in 80O seawater, pH 7.6) or the buffer containing glucose at a concentration of 1 j;. The nitrogenase activity of eelgrass roots was found to be greatly enhanced by the addition of glucose under either aerobic or anaerobic conditions. One of the glucose-amended root samples that showed high nitrogenase activity under anaerobic conditions was used for the isolation of nitrogen-fixing bacteria. The roots together with the supplemented solution were homogenized and then 1 ml of the homogenate was serially diluted with 9 ml of sterile seawater containing 0.05°c sodium L-ascorbate. A 0.1 ml aliquot of each diluent was transferred to a 40-ml L-shaped tube containing 5 ml of NFL medium. After the tube was sealed with a rubber stopper, the contained air was replaced with nitrogen. The cultures were gently shaken at 25°C for about 3 days. The culture of the highest dilution that showed marked turbidity was again serially diluted, and the above procedure was repeated. For the final isolation of nitrogen- fixing bacteria, the second enrichment culture of the highest dilution positive for growth was spread on PY agar plates and the plates were incubated at 25°C for 3 days under anaerobic conditions using a GasPak Anaerobic System (BBL). Thirty colonies were picked up at random and assayed for nitrogenase activity in NFL medium. Measurement of nitrogenase activity. The nitrogenase activity of the isolates was measured by the acetylene-reduction assay method. After incubation in NFL medium under nitrogen atmosphere for 30 to 40 hr, the cells were harvested by centrifugation and then washed with artificial seawater containing 0.0500 sodium L- ascorbate. The artificial seawater consisted of 0.4 M NaCI, 0.1 M MgSO4.7H2O, 0.02 M KCI, and 0.02 M CaCl2.2H2O. The cells were resuspended in 5 ml of NFL or its modified medium, distributed in the 32-ml test tubes, and incubated at 25°C. The optical density at 600 nm of the cell suspensions was adjusted to about 0.25. To 1987 A N2-fixing Bacterium Isolated from Eelgrass Roots 323 measure aerobic nitrogenase activity, 3.2 ml of the air in the test tube was removed and then the same volume of acetylene gas was injected with a gas-tight syringe; for measuring anaerobic nitrogenase activity, all the air in the test tube was replaced with Ar/C2H2 (90% :10%, v/v). At 4-hr intervals, 0.2 ml of gas was removed with a gas-tight syringe and analyzed for ethylene and acetylene using a Shimadzu G-4CM gas chromatograph equipped with a flame ionization detector (Porapak R column 3 mm x 50 cm, 50°C, nitrogen carrier gas, 40 ml mm). Specific activities were calculated between 4 and 8 or 8 and 12 hr of incubation. No growth occurred during the period when nitrogenase activity was measured. Growth studies. The strain RSI19, which showed the highest nitrogenase activity among the isolates, was gently shaken at 25°C in NFL medium. NH4C1 when added to NFL medium served as a nitrogen source for cells growing under aerobic or anaerobic conditions. Taxonomic tests. Taxonomic tests were carried out according to the con- ventional procedures as described by SMIBERTand KRiEG(5) with exceptions and additional tests as cited below. Pigmentation, swarming, and luminescence were determined after growth for 24 to 48 hr on the PY agar plates. Luminescence was recorded after the plate had been observed for 5 min in the dark. Poly-/3-hydroxybutyrate (PHB) accumulation was tested on modified NFL media containing O.2° glucose or O.2° sodium-DL-/3- hydroxybutyrate instead of glucose as the carbon source and supplemented with 2mmol of NH4C1 per liter. The cultures were examined with a phase-contrast microscope, daily for 5 days (6). Sensitivity to 2,4-diamino-6,7-diisopropyl-pteridine (0/ 129) phosphate was determined by a disc-sensitivity testing method on PY agar plate. The discs contained 10 ug or 150 ug of 0/ 129 phosphate. Growth at different concentrations of NaCI was determined in tryptone (100, w/v) broth containing 0, 1, 3, 6, and 8 % NaCI. Ability to grow at various temperatures was tested using PY broth medium. Growth was recorded after incubation for 14 days at 4°C, and 2 days at 20, 35, and 40°C. The presence of alginase and chitinase was tested as described by BAUMANNet al. (7). The ability to produce acid from different carbohydrates was tested on stab media which differed from PY medium by containing 3 g of agar per liter, 15 ml of 0.2°c (w/v) of bromthymol blue solution per liter, and 10 g of the carbohydrates per liter. The surface of the medium was sealed with sterile liquid paraffin after inoculation. The cultures were examined for color change for a period of 7 days. NaCI was added to all tested media that did not already contain at least 0.500 NaCI to a final 100 concentration. Cells grown for 6 hr in PY broth medium at 25°C were negatively stained with potassium phosphotungstate (1.0%, w/v, pH 7.0). Photographs were taken with a JEM-100C electron microscope. Ability to utilize various compounds as sole sources of carbon and energy was determined using the modified NFL media containing 0.2°c of the tested carbon sources instead of glucose and supplemented with 2 mmol of NH4C1 per liter. Unless otherwise stated, all the tested cultures were incubated at 25°C for 7 days under aerobic conditions. Guanine-plus-cytosine content of the DNA. The guanine-plus-cytosine content 324 SHISH, SIMIDU, and MARUYAMA VOL. 33 of the bacterial DNA was determined by high-performance liquid chromatogFaphy (HPLC). Directly determining the guanine-plus-cytosine content of DNA using different models of HPLC and a wide range of column types have been found to give satisfactory results (8-10). DNA was extracted and purified by the method of MARMuR(11) with some modifications. For enzymic hydrolysis of RNA, ribonu- clease A (Sigma) and ribonuclease T1 (Sigma) were used. The purified DNA was dissolved in 10 mM phosphate buffer (pH 7.0,1 mg/ml). Then the DNA solution was heated at 100°C for 15 min, and cooled rapidly in an ice bath.
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