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Effects of the Herbicide, Butachlor, on Nitrogen Fixation in Phototrophic Nonsulfur Bacteria

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Effects of the Herbicide, Butachlor, on Nitrogen Fixation in Phototrophic Nonsulfur Bacteria Environ. Eng. Res. Vol. 12, No. 4, pp. 136～147, 2007 Korean Society of Environmental Engineers EFFECTS OF THE HERBICIDE, BUTACHLOR, ON NITROGEN FIXATION IN PHOTOTROPHIC NONSULFUR BACTERIA Lee, Kyung Mi, Jaisoo Kim1, and Hyun Soon Lee* Department of Biological Sciences, Sungkyunkwan University, Suwon 440-746, Korea 1Department of Life Science, Kyonggi University, Suwon 443-760, Korea (received January 2007, accepted September 2007) Abstract：In an effort to identify possible microbes for seeking bioagents for remediation of herbicide- contaminated soils, seven species of phototrophic nonsulfur bacteria (Rhodobacter capsulatus and sphaeroides, Rhodospirillum rubrum, Rhodopseudomonas acidophila, blastica and viridis, Rhodomicrobium vannielii) were grown in the presence of the herbicide, butachlor, and bacterial growth rates and nitrogen fixation were measured with different carbon sources. Under general conditions, all species showed 17-53% reductions in growth rate following butachlor treatment. Under nitrogen-fixing conditions, Rb. capsulatus and Rs. rubrum showed 1-4% increases in the growth rates and 2-10% increases in nitrogen-fixing abilities, while the other 5 species showed decreases of 17-47% and 17-85%, respectively. The finding that Rp. acidophila, Rp. bla- stica, Rp. viridis and Rm. vannielii showed stronger inhibitions of nitrogenase activity seems to indicate that species in genera Rhodobacter and Rhodospirillum are less influenced by butachlor than those in Rhodop- seudomonas and Rhodomicrobium in terms of nitrogen-fixing ability. Overall, nitrogenase activity was closely correlated with both growth rate and glutamine synthetase activity (representing nitrogen metabolism). When the carbon sources were compared, pyruvate (three carbons) was best for all species in terms of growth rate and nitrogen fixation, with malate (four carbons) showing intermediate values and ribose (five carbons) showing the lowest; these trends did not change in response to butachlor treatment. We verified that each of the 7 species had a plasmid (12.2~23.5 Kb). We found that all 7 species could use butachlor as a sole carbon source and 3 species were controlled by plasmid-born genes, but it is doubtful whether plasmid-born genes were responsible to nitrogen fixation. Key Words：Butachlor, Herbicide, Nitrogen fixation, Plasmid, Purple nonsulfur bacteria INTRODUCTION1 gen fixation in cyanobacteria are of interest to researchers because this process is vital to the 7-10) Nitrogen fixation by phototrophic nonsulfur fertility of the rice fields. However, only a bacteria was first demonstrated through the study few studies have examined the effect of herbi- of hydrogen production by Rhodospirillum rub- cides on nitrogen fixing phototrophic nonsulfur 11) rum,1) and subsequently shown in other phototro- bacteria. phic bacteria. However, although many phototro- Butachlor (2-chloro-2’, 6’-diethyl-N (butoxy- phic bacteria are able to fix nitrogen, the asso- methyl) acetanilide; commercial name Machete), ciated nitrogenases have been studied in only a alachlor and propachlor belong to the chloro- few species.2-6) The effects of herbicides on nitro- acetanilide chemical family and were used extensively in the 1980s and 1990s for killing †Corresponding author weeds in rice-fields, especially in Korea, Japan E-mail: [email protected] and other Southeast Asian countries. There have Tel: +82-31-249-9648, Fax: +82-31-249-9139 Effects of the Herbicide, Butachlor, on Nitrogen Fixation in Phototrophic Nonsulfur Bacteria 137 been reports of the negative effects of butachlor method. Those are Rhodobacter capsulatus DSM on cyanobacteria, Rhizobium and Nostoc; these 1710, Rhodobacter sphaeroides ATCC 17023, effects include mutagenesis, as well as inhibition Rhodospirillum rubrum KS 301, Rhodopseudomonas of growth, photosynthesis and nitrogenase activity.12) acidophila ATCC 25092, Rhodopseudomonas bla- In contrast, the growth and aerobic nitrogen stica ATCC 33485, Rhodopseudomonas viridis fixing ability of butachlor-treated Gloeocapsa DSM 133, Rhodomicrobium vannielii DSM 162. species (oxygen-utilizing diazotrophs) were shown to be possible due to plasmid-born herbicide Chemical resistance genes.12,13) Nitrogen fixation concurrent Butachlor (2-chloro-2’, 6’-diethyl-N (butoxymethyl) with oxygen or ammonia treatment was studied acetanilide; commercial name, Machete) with purity using phototrophic nonsulfur bacteria and diazo- of 98.7% was purchased from the Korean Agriculture trophic bacteria,13) whereas Habte and Alexander14) Chemical Company (Seoul, Korea). showed that herbicide-treated Chromatium and Thiospirilum showed increased nitrogen fixation Media and Growth Conditions ability, while cyanobacteria showed the opposite All strains were grown in Ormerod medium4) in lowland rice culture. supplemented with 0.3% of the indicated carbon Butachlor is generally removed from the soil source at pH 7.0, except that Rhodopseudomonas 15) through volatilization and decomposition by light (Rp.) acidophila and Rhodomicrobium (Rm.) or soil microorganisms. The herbicide, chloroace- vannielii were kept at pH 5.6, and the media for tanilide, was degraded 50 times faster by micro- Rp. blastica was supplemented with 0.4% NaCl. organisms than by light or volatilization, indicating For experiments testing growth in dinitrogen gas, that some microorganisms could use herbicide as the (NH4)2SO4 and yeast extract in the Ormerod 7,8,10,16,17) a carbon source. Likewise, microorganisms medium (basal medium) was replaced with biotin capable of using alachlor or propachlor as a car- (8 μg/mL) and a 50 mL/min flow of nitrogen bon source were found in sewage and lake water. gas. 18) 19) Madigan et al. and Serebrayakova et al. To study the utilization of butachlor as a sole examined the nitrogenase activities of nonsulfur carbon source, 10-2 to 10-5 M of butachlor was photosynthetic bacteria, and the studies have added to the basal medium without yeast extract. examined the relationships among nitrogen fixa- Bacteria were cultured in screw cap tubes (10 5,20-22) tion, plasmids and genes. mL) or glass bottles (30 or 50 mL) under 2000 This study examined the influence of butachlor Lux illumination at 28 ± 2°C. For growth under on the nitrogen-fixing ability and growth rates of nitrogen gas, a suction flask was filled with 50 phototrophic nonsulfur bacteria, and then further ml of medium and nitrogen gas was passed assessed the utilization of butachlor as a carbon through a high temperature copper tube for com- source, and the plasmids involved in butachlor plete elimination of oxygen. Growth of the micro- degradation. organisms was determined by measuring optical density (OD) at 660 nm and calculating the dry MATERIALS AND METHODS weight according to Hilmer and Gest.23) The spe- cific growth rate (μ, unit = h-1) was calculated Microorganisms from the equation of Schlegel.24) For protein All strains were purchased from American estimation, the Lowry method25) was used with Type Culture Collection (ATCC, USA) and bovine serum albumin employed as the standard. Deutsche Sammulung für Mikroorgnismen (DSM, The cells were disrupted by a sonicator. Germany), except Rhodospirillum rubrum KS-301, which was isolated in our laboratory from lake Ammonium Estimation water using an anaerobic enrichment culture For estimation of ammonium production, 10 VOL. 12, NO. 4, 2007 / ENVIRONMENTAL ENGINEERING RESEARCH 138 Lee, Kyung Mi, Jaisoo Kim, and Hyun Soon Lee mL of each cell culture was digested with 0.1 inoculated into 5 ml of LB medium including mL of digestion solution (conc. H2SO4, 1 L: Mitomycin C (0-20 μg/mL), and the inoculums potassium sulfate, 100 g; selenium, 1 g) at 300°C were cultured at 30°C for 48 hours. A second for 1 hour until the mixture became transparent. generation was cultured as above and then After centrifugation for 10 min, 50 μL of super- inoculated to LB medium including butachlor, natant was used for measuring the absorbance at the plasmids were isolated from cured cells, and 625 nm according to the method of Chaney and resolved by agarose gel electrophoresis. 26) March. NH4Cl was dried for 24 hours at 100°C was used as the standard. Agarose Gel Electrophoresis Electrophoresis was carried out on 0.8% agarose Enzyme Assays gels at 100 V for 2.5 hours using TEA buffer.32) Nitrogenase activity was determined by measure- Hind III DNA fragments were used as molecular ment of acetylene reduction, as described.8,27) size markers. After electrophoresis, the agarose Briefly, cell cultures were centrifuged, and each gels were stained with Ethidium Bromide (1 mg/ pellet was washed with nitrogen-free medium mL) for 40 min, washed with distilled water, and then suspended in Ormerod medium without and photographed with Polaroid film Type 667. a nitrogen source. Two ml of this cell suspension was inoculated into a tube, sealed with suba seal Analysis of Results (No. 17), treated with argon gas for 10 min and Each experiment was performed in triplicate then treated with acetylene gas (calcium carbide and repeated two times. The standard deviation + H2O) up to 10% (v/v). The cells were cul- was less than 10 % of the mean. All comparisons tured under 10,000 Lux at 30°C for 60 hours were statistically compared using a t-test with P and the production of ethylene gas (0.5-1 mL) < 0.05. was measured by gas chromatography (Varian 3700, CA, USA). RESULTS In order to assay the activity of glutamine synthetase, γ-glutamylhydroxamate formation was Effects of Butachlor on Bacterial Growth determined as described by Shapiro and Stadt- We first identified the effective concentration 28) 29) man and Bender et al. of butachlor required to build a proper experi- mental design. Protein concentration (mg/mL) at Preparation of Plasmids stationary phase was used as a representation of Plasmids from seven strains of phototrophic Rs. rubrum KS-301 growth in basal medium nonsulfur bacteria were prepared by the rapid containing pyruvate, malate or ribose as a carbon method described by Birnboim and Doly30) and source, supplemented with concentrations of but- Ish-Horowitz and Burke,31) which allows isolation achlor ranging from 10-1 to 10-6 M (Fig.
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