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Microvirgula Aerodenitrificans Gen. Nov., Sp. Nov., a New Gram-Negative

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Microvirgula Aerodenitrificans Gen. Nov., Sp. Nov., a New Gram-Negative International Journal of Systematic Bacteriology (1 998), 48, 77 5-782 Printed in Great Britain Microvirgula aerodenitrificans gen. nov., sp. nov., a new Gram-negative bacterium exhibiting co-respiration of oxygen and nitrogen oxides up to oxygen-saturated conditions Dominique Patureau, Jean-Jacques Godon, Patrick Dabert, Theodore Bouchez, Nicolas Bernet, Jean Philippe Delgenes and Rene Moletta Author for correspondence : Dominique Patureau. Tel : + 33 468 42 5 1 69. Fax : + 33 468 42 5 1 60. e-mail : [email protected] lnstitut National de la A denitrifier micro-organism was isolated from an upflow denitrifying filter Recherche Agronomique, inoculated with an activated sludge. The cells were Gram-negative, catalase- Laboratoire de Biotechnolog ie de and oxidase-positivecurved rods and very motile. They were aerobic as well as I'Environnement (LBE), anoxic heterotrophsthat had an atypical respiratory type of metabolism in Avenue des Etangs, 111 00 which oxygen and nitrogen oxides were used simultaneously as terminal Narbonne, France electron acceptors. The G+C content was 65 mol%. Our isolate was phenotypically similar to Cornamonas testosteroni, according to classical systematic classificationsystems. However, a phylogenetic analysis based on the 16s rRNA sequence showed that the aerobic denitrifier could not be assigned to any currently recognized genus. For these reasons a new genus and species, Microvirgula aerodenitrificans gen. nov., sp. nov., is proposed, for which SGLYZT is the type strain. Keywords: Microvirgula aerodenitriJicansgen. nov., sp. nov., co-respiration of oxygen and nitrogen oxides, Proteobacteria, fluorescent in situ hybridization, oligonucleotide probes I INTRODUCTION denitrifying filter. It exhibits an atypical behaviour towards oxygen and nitrate (16), since it is able to co- The denitrifiers are facultative anaerobic bacteria that respire oxygen and nitrogen oxides and produce N,. can adjust their metabolic pathway to the prevailing This behaviour has been explained by the continuous growth conditions. Under aerobic conditions, the most expression of denitrifying enzymes whatever the aer- efficient electron acceptor is oxygen. During anoxic ation conditions (17). This strain, named SGLY2, has conditions, a lower free-energy transducing pathway is been tentatively characterized as Cornamonas testo- used, the denitrification pathway, reducing nitrate to steroni by phenotypic characterization. In this paper, N, gas. It had been believed for a long time that we compare the phenotypic and phylogenetic charac- denitrifying activity and enzyme synthesis were com- terization of this new bacterium and present the design pletely repressed by oxygen (11). However, some of a specific oligonucleotide probe for strain detection micro-organisms, like Thiosphaera pantotropha, iso- by fluorescent in situ hybridization. On the basis of lated from activated sludge, can reduce oxygen and these studies we propose a new genus and species, nitrate simultaneously to water and N,, respectively, Microvirgula aerodenitrlficans gen. nov., sp. nov., to up to oxygen-saturated conditions (21, 22, 23). A describe this bacterium. strain was isolated in our laboratory from an upflow METHODS Abbreviations: DAPI, 4,6-diamidino-2-phenylindole; TRITC, tetramethyl- Bacterial strains and culture conditions. The strain used in rhodamine 5-isothiocyanate. this study was isolated from an upflow anoxic filter pre- The GenBank accession number for the nearly complete sequence viously inoculated with activated sludge. The filter was (nt 9-1 509) of the 165 rRNA gene reported in this paper is U89333. maintained under anoxic conditions to remove nitrogen pol- 00638 0 1998 IUMS 775 D. Patureau and others lution. However, the anoxic conditions were not strict. 95 carbon sources of the unknown strain relative to a Part of the filter sludge was used to inoculate another reactor database containing those of previously identified bacteria, that was submitted to alternate aerobic and anoxic con- including non-clinical strains. ditions to enrich the population in aerobic denitrifiers. Ethanol, glycerol, testosterone, succinate, acetate, propi- SGLY2T was isolated from this reactor by spreading on onate, butyrate and valerate were also tested as electron nitrate complete medium (Merck) under aerobic conditions. donors for denitrification (final concentration in synthetic Then the strain was cultivated at 35 "C and pH 7 under medium: 500 mg C 1-'). The denitrifying potential of the aerobic as well as anoxic conditions in synthetic medium strain was evaluated through consumption of nitrogen containing 0.01 M potassium phosphate buffer, pH 7.0, oxides (nitrate, nitrite and N,O) and production of N,O and 380 mg MgSO, l-l, 250 mg yeast extract 1-', (NH,),SO, as nitrogen source (1 16 mg N l-'), KNO,,. KNO, or N,O as N,. electron acceptor (250 mg N l-'), succinate or acetate as 165 rDNA sequence analysis. The 16s rRNA gene (rDNA) electron donor (500 mg C 1-l) and 1 ml trace element sequence of strain SGLY2Twas determined by sequencing of solution 1-' (1 5). Cultures were grown either in batch culture PCR-amplified 16s rDNA. Genomic DNA extraction, (in 120 ml Penicillin flasks) or in a continuous stirred reactor PCR-mediated amplification of 16s rDNA and purification under various dissolved oxygen concentrations to observe of the PCR products were performed by using previously the behaviour of the strain in the presence of the two electron described protocols (7,25). The primers used for PCR were acceptors. Discontinuous cultures were also used (i) to test 9F (5' GAGTTTGATCMTGGCTCAG) and 1509R (5' different carbon sources, electrons acceptors and sodium salt GNTACCTTGTTACGACTT) (7). Purified PCR products concentrations and (ii) to determine optimum growth factors were sequenced by using a PRISM Ready Reaction Dye- (pH, temperature) and growth inhibitors. Deoxy Terminator Cycle Sequencing Kit (Applied Bio- systems). Sequence reaction mixtures were electrophoresed Escherichia coli TG1 was grown in LB (25). Other strains with an Applied Biosystems model 373A DNA sequencer. used to compare physiological capabilities (denitrifying The 16s rDNA sequence of the new strain was compared ability under various aeration conditions) and/or probe with all accessible 16s rDNA sequences in databases. The specificity to the isolated strain were : Pseudomonas testos- alignment of 16s rDNA sequences with representative teroni [ATCC 1 1996T; reclassified as Comamonas testosteroni organisms belonging to the /?-subclassof the Proteobacteria (27)], Paracoccus denitrificans (NCIMB 8944), Paracoccus was obtained by using CLUSTAL v software (10). Phylogenetic halodenitrificans (ATCC 25843), Pseudomonas stutzeri trees were calculated by Jukes-Cantor (12) and neighbour- (ATCC 14405) and Zoogloea ramigera (ATCC 19544N)(T, joining algorithms (24). type strain; N, neotype strain). They were all grown ac- cording to the recommendations of the American Type Dot blot hybridization. RNAs from pure cultures of Para- Culture Collection (ATCC, Rockville, MD, USA). coccus halodenitrificans, Zoogloea ramigera, Comamonas testosteroni, Paracoccus denitrifkans, Pseudomonas stutzeri Morphological characteristics. Gram staining was performed and E. coli were extracted by a low-pH hot-phenol extraction as described by Magee et al. (1 3). Colony-forming units were procedure (19). RNA was denatured as previously described observed on complete agar medium (g 1-': yeast extract, 5; (25). Approximately 1 pg of each extract was deposited as a NaC1, 5; pancreatic peptone, 15; agar, 18) as well as on dot on a nylon membrane (Hybond-N'; Amersham) and synthetic agar medium (synthetic medium containing 18 g linked to the membrane by UV exposure with a Spectro- agar 1-'). Spore formation was determined by malachite linker XL-1000 (Spectronics). green staining of cells grown on nutrient agar. Morpho- logical properties were examined by phase-contrast mi- The following oligonucleotide probes complementary to croscopy. Transmission electron microscopy was used to specific regions of 16s rRNA were used for hybridization : (i) examine flagellation and for cell wall characterization. S-D-Bact-0338-a-A-18 is specific for the Bacteria domain ; Cultures (48 h) were fixed in a solution of 3 O/O glutaraldehyde (26) (ii) S-*-Mae-0636-a-A-18 is complementary to posi- in 0-2 M cacodylate buffer, pH 7.4, for 1 h at 4 "C. The cells tions 636-653 (E. coli numbering) (5) of the SGLY2T 16s were centrifuged and washed three times with the same rRNA (this work). Non-radioactive labelling of oligonu- buffer. They were post-fixed with 1 YOosmic acid for 1 h at cleotides was performed with the DIG Oligonucleotide 3'- 4 "C, embedded in 1.3 YO agar and dehydrated for 10 min End Labelling Kit according to the manufacturer's instruc- each with 70, 95 and 100% ethanol. Preparations were tions (Boehringer Mannheim). Hybridization and stripping washed in propylene oxide for 30 min, infiltrated with epoxy of the membrane were performed as recommended by resin/propylene oxide (1 : 1) for 1 h and then embedded in Boehringer Mannheim (4). Hybridization was revealed by 100 YOepoxy resin. After hardening, ultrathin sections were chemiluminescence using anti-digoxigenin/alkaline phos- cut with a diamond knife, stained with uranyl acetate and phatase antibodies and CDP-star substrate with Kodak X- Reynold's lead citrate for 20 min (20) and examined with a OMAT AR film. Philips EM 400 microscope. In situ hybridization. The two oligonucleotides described
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