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1 IRD, UR 101 Extrêmophiles, IFR-BAIM, Universités de Provence et de la Méditerranée, ESIL case 925, 163 avenue de Luminy, 13288 Marseille cedex 09, France
2 Laboratorio de microscopía electrónica, Centro Nacional de Investigación y Capacitación Ambiental (CENICA), Universidad Autónoma Metropolitana, México, DF, Mexico
3 Programa de Biotecnología del Petróleo, Instituto Mexicano del Petróleo, México, DF, Mexico
Correspondence
Bernard Ollivier
ollivier{at}esil.univ-mrs.fr
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). Several authors have reported the isolation (microbiological studies) or presence (molecular ecological studies) of microaerophiles in such ecosystems (Gevertz et al., 2000; Telang et al., 1997; Voordouw et al., 1996). Besides microaerophiles, manganese-, iron-, elemental sulfur-, sulfate-, carbon dioxide- and nitrate-reducing micro-organisms inhabit oil reservoirs (Greene et al., 1997; Huu et al., 1999; Magot et al., 2000; Myhr & Torsvik, 2000; Rees et al., 1997). Most studies have dealt with methanogens, sulfate-reducers and heterotrophs, and little attention has been paid to other microbial communities originating from this subterrestrial ecosystem. However, the addition of nitrate in oil reservoirs has been shown to stimulate the activity of indigenous nitrate-reducing, sulfide-oxidizing microaerophiles, and also that of heterotrophic denitrifiers that outcompete sulfate-reducing bacteria for energy sources (Gevertz et al., 2000; Telang et al., 1997). Amongst microaerophilic nitrate-reducing bacteria, Gevertz et al. (2000) reported the isolation of strains of Thiomicrospira, Arcobacter and Campylobacter (phylogenetically related micro-organisms) from brine extracted at the Coleville oilfield in Canada. Nitrate-reducing anaerobes or facultative anaerobes include (i) the thermophilic, manganese- and iron-reducing bacterium Deferribacter thermophilus, isolated from the Beatrice oilfield in the North Sea (Greene et al., 1997), (ii) the thermophilic, citrate-fermenting bacterium Anaerobaculum thermoterrenum, isolated from the Redwash oilfield in Utah (Rees et al., 1997), (iii) the citrate- and succinate-oxidizing bacterium Marinobacter aquaeolei, isolated from a southern Vietnamese oil reservoir (Huu et al., 1999), and (iv) the acetate-oxidizing bacterium Denitrovibrio acetiphilus, isolated from an oil reservoir model column (Myhr & Torsvik, 2000). Here, we describe a novel thermophilic, heterotrophic, nitrate-reducing isolate from a water separator collecting fluids produced from different oil wells located in the SAMIII oilfield, Gulf of Mexico. It belongs to the order Clostridiales, cluster XII, and has a number of significant phenotypic, genotypic and phylogenetic differences from other members of cluster XII that justify its assignment to a new genus and species, Garciella nitratireducens gen. nov., sp. nov.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Enrichment, isolation and growth conditions.
Enrichment was performed in a medium containing (l-1 distilled water) 0·3 g K2HPO4, 0·3 g KH2PO4, 0·2 g MgSO4.7H2O, 0·1 g CaCl2, 0·1 g KCl, 30 g NaCl, 1 g NH4Cl, 0·5 g cysteine hydrochloride, 0·2 g yeast extract (Difco), 10 ml trace mineral solution (Balch et al., 1979) and 1 mg resazurin. The pH was adjusted to 7·0 with 10 M KOH and the medium was boiled under a stream of O2-free N2 gas and cooled to room temperature. The medium was dispensed into serum bottles (20 ml) and Hungate tubes (5 ml) under a stream of O2-free N2 gas, subsequently replaced by a mixture of N2/CO2 (80 : 20 %, v/v). Vessels were autoclaved for 45 min at 110 °C and, prior to inoculation, Na2S.9H2O, NaHCO3, peptone (Difco) and thiosulfate were added from sterile stock solutions to obtain respective final concentrations of 0·04, 0·2 and 0·5 % and 20 mM. Hydrogen (2 bars) was added in the gas phase. For enrichment, a 2-ml oil-well-water sample was inoculated into 20 ml medium and incubated at 40 °C without agitation. Three enrichment series were performed in the same medium before isolation. Strains were isolated by repeated use of the roll-tube technique (Hungate, 1969), with medium solidified with 1·6 % agar. The process of serial dilution in roll tubes was repeated at least twice in order to purify the cultures.
Determination of growth parameters.
The basal medium used for characterization of the pH, temperature and NaCl ranges for growth of the isolate and resistance to antibiotics was similar to the enrichment medium with the following modifications: the NaCl concentration was decreased to 10 g l-1, glucose was added at a concentration of 20 mM and 0·2 g MgSO4.7H2O l-1 was replaced by 1 g MgCl2.6H2O l-1. The culture medium was adjusted to different pH values by injecting 1 M HCl, NaHCO3 or Na2CO3 from 10 % (w/v) sterile anaerobic stock solutions. For studies on NaCl requirements, NaCl was weighed directly into tubes prior to dispensing the medium. The strain was subcultured at least once under the same experimental conditions prior to determination of the growth rate.
Substrate utilization tests.
Substrates were tested at a final concentration of 20 mM in basal medium or 1 % for cellulose, starch and xylan or 0·2 % for peptone, bio-Trypticase and Casamino acids.
Electron acceptors and H2S production.
To test for electron acceptors, sodium thiosulfate (20 mM), sodium sulfate (20 mM), sodium fumarate (20 mM), sodium sulfite (5 mM), elemental sulfur (1 %), sodium nitrate (10 mM) and sodium nitrite (5 mM) were added individually to the medium. The use of electron acceptors was evaluated by measuring OD580 and H2S, succinate, ammonium or nitrite production. Nitrate reduction was tested in the absence of ammonium chloride as nitrogen source.
Antibiotic susceptibility.
The sensitivity of the isolate to ampicillin, chloramphenicol, kanamycin, rifampicin and vancomycin was tested at 10, 25, 50 and 100 µg ml-1. Controls were performed with ethanol and DMSO (respectively solvents for chloramphenicol and rifampicin). Growth was monitored by measuring OD580 and by microscopic observations.
Sporulation test and oxygen susceptibility.
The presence of spores was analysed by phase-contrast microscopic observations of young and old cultures and pasteurization tests performed at 80, 90 and 100 °C for 10 and 20 min. The effect of O2 on growth was determined in Hungate tubes containing basal medium supplemented with 20 mM glucose. After inoculation, 20 ml sterile air was added to the gas phase. The cultures were incubated at 55 °C under agitation (150 r.p.m.). Growth was monitored by turbidity measurements (OD580). Experiments were conducted in duplicate and repeated at least twice.
Analytical techniques.
Unless otherwise indicated, duplicate culture tubes were used throughout these studies. Growth was measured at 580 nm using a UV-Visible spectrophotometer 50 Scan (Varian). Sulfide was determined photometrically as colloidal CuS by using the method of Cord-Ruwisch (1985). Ammonium was detected by the Nessler method. Fermentation products were determined by HPLC using a pump (Spectra Series P100; Thermo Separation Products), an automatic sampler (Spectra Series AS100), an Aminex HPX 87H column (300x7·8 mm) (Bio-Rad), a differential refractometer detector (Spectra System RI-150) and an integrator (Azur Microsoft). An aliquot of 20 µl cell-free supernatant was injected into the column, which was maintained at 37 °C. A solution of 0·01 M H2SO4 was used as solvent at a flow rate of 0·6 ml min-1. The presence of L-alanine as an end product of sugar metabolism was determined enzymically at 340 nm as described previously (Fardeau et al., 1997).
Light and electron microscopy.
Morphological characteristics of isolates were observed with a phase microscope (Nikon). For scanning electron microscopy studies, cells were stained with osmium tetroxide, prepared as described by Bozzola & Russell (1991) and observed in a JEOL-5900 low-vacuum electron microscope at an accelerating voltage of 10 kV. For transmission electron microscopy studies, cells were negatively stained with sodium phosphotungstate and prepared and observed as described by Koussémon et al. (2001).
Determination of G+C content and 16S rDNA sequence analysis.
The G+C content of DNA was determined at the DSMZ by using HPLC as described by Mesbah et al. (1989). Non-methylated lambda DNA (Sigma) was used as the standard. The 16S rRNA gene of the isolate was amplified by adding 2·5 µl cell culture to a thermocycler microtube containing 5 µl 10x Taq buffer (Promega), 3 µl 25 mM MgCl2, 0·5 µl 25 mM dNTPs, 0·5 µl 100 nM primers, 37·5 µl sterile distilled water and 0·5 µl 5 U Taq polymerase µl-1 (Promega). The universal primers Fd1 (5'-AGAGTTTGATCCTGGCTCAG-3', positions 8–28) and Rd1 (5'-AAGGAGGTGATCCAGCC-3', positions 1547–1531, MWG) (Escherichia coli numbering) were used to obtain the PCR product (Winker & Woese, 1991). PCR was performed by an initial denaturation at 96 °C for 3 min followed by 30 cycles of annealing at 57·1 °C for 30 s, extension at 72 °C for 2 min and denaturation at 96 °C for 30 s and, finally, an extension cycle of 72 °C for 7 min. The amplified fragment contained 1471 nucleotides. PCR products were purified with a QIAquick gel extraction kit. Direct sequencing of the PCR product was performed by Genome Express. The new sequence was aligned to a full-length consensus 16S rDNA sequence, assembled and checked for accuracy manually, using the alignment editor BioEdit version 5.0.9 (Hall, 1999). These were compared with other sequences in GenBank (Benson et al., 1999) and the RDP (Maidak et al., 2001) using BLAST (Altschul et al., 1997) to identify the closest relatives. Positions of sequence and alignment ambiguity were omitted and pairwise evolutionary distances based on 1267 unambiguous nucleotides were computed by using the method of Jukes & Cantor (1969). A dendrogram was constructed using the neighbour-joining method (Saitou & Nei, 1987). Confidence in the tree topology was determined by using 100 bootstrapped trees (Felsenstein, 1985).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). Amongst these, the occurrence of methanogenic, sulfate-reducing and heterotrophic bacteria belonging to the families Thermotogaceae and Thermoanaerobiaceae has been established from various oil reservoirs throughout the world (Magot et al., 2000). Microaerophilic nitrate-reducing bacteria have been shown to be helpful in oil reservoirs because they oxidize sulfur-containing compounds and reduce H2S production (Telang et al., 1997). However, few studies have reported the isolation of such bacteria from oil production waters (Gevertz et al., 2000). Besides microaerophilic nitrate-reducing bacteria, few studies have provided evidence of the existence of anaerobic nitrate-reducers in oil reservoirs (Greene et al., 1997; Myhr & Torsvik, 2000; Rees et al., 1997). Here, we report a novel anaerobic, nitrate-reducing bacterium isolated from an oilfield separator in the Gulf of Mexico. Enrichment cultures were positive after incubation at 40 °C for 15 days. Microscopic examination revealed the presence of motile, rod-shaped bacteria. Round, slightly black-coloured colonies (2 mm diameter) developed on roll tubes after 1 week. Single colonies were picked and serially diluted and reinoculated in roll tubes three times before cultures were considered pure. Several strains similar in morphology were isolated from the oil reservoir, and one strain, designated MET79T, was used for further characterization.
Cells of strain MET79T were straight rods, 0·5–0·7x1·4–2·8 µm in size (Fig. 1a, b), motile with a subpolar flagellum. Spherical and terminal spores appeared in old cultures. Irregular gas vacuoles were sometimes observed (Fig. 1a). Ultrathin sections of cells showed a Gram-positive-type cell wall composed of a thick (17 nm) and homogeneous S-layer (Fig. 1c). Strain MET79T grew at temperatures ranging from 25 to 60 °C, with optimum growth at 55 °C. Growth occurred at initial pH values between 5·5 and 9·0 at 55 °C and the optimum was pH 7·5. The isolate grew in the presence of NaCl concentrations ranging from 0 to 10 %, with an optimum NaCl concentration of 1 % at pH 7·5 and 55 °C. Strain MET79T grew in the presence of up to 25 µg kanamycin and chloramphenicol ml-1 and 100 µg ampicillin ml-1, but not in the presence of 10 µg vancomycin or rifampicin ml-1. Yeast extract was required for growth. Vitamins or bio-Trypticase could not replace yeast extract. Strain MET79T fermented the following compounds: cellobiose, fructose, galactose, glucose, lactose, maltose, mannose, ribose, sucrose, D-xylose, glycerol, mannitol, fumarate, lactate, malate, pyruvate and Casamino acids. One mol glucose was fermented into 1·5 mol lactate as the major end product, with minor amounts of acetate [0·03 mol (mol glucose consumed)-1] and butyrate [0·2 mol (mol glucose consumed)-1], and into H2 [0·3 mol (mol glucose consumed)-1] and CO2. The following compounds were not used: arabinose, raffinose, rhamnose, starch, cellulose, xylan, acetate, butyrate, propionate, methanol, ethanol, butanol, propanol, formate, methylamine, p-coumaric acid, ferulic acid, peptone, bio-Trypticase and H2. Strain MET79T reduced thiosulfate to H2S and nitrate to ammonium. The other electron acceptors tested were not used. Growth was enhanced in the presence of thiosulfate or nitrate. Strain MET79T grew under anaerobic conditions. The G+C content of strain MET79T was 30·9 mol%. 16S rDNA sequence analysis revealed that strain MET79T was a member of the order Clostridiales, cluster XII, as defined by Collins et al. (1994), and its closest phylogenetic relative was Caloranaerobacter azorensis (Wery et al., 2001), family Clostridiaceae (88·7 % similarity). Fig. 2 presents a dendrogram generated by the neighbour-joining method (Saitou & Nei, 1987).
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), and Fusibacter paucivorans, family Peptostreptococcaceae (Ravot et al., 1999), and the thermophilic Anaerobaculum thermoterrenum, family Syntrophomonadaceae (Rees et al., 1997). Dethiosulfovibrio peptidovorans is peripherally related to cluster V, consisting of the family Thermoanaerobiaceae (Magot et al., 1997), whereas Fusibacter paucivorans grouped with members of cluster XI (Ravot et al., 1999). Similarly to strain MET79T, Anaerobaculum thermoterrenum also reduced nitrate, but the latter forms a branch that is approximately equidistant from Dictyoglomus thermophilum and members of Thermoanaerobacter (Rees et al., 1997). In addition to phylogenetic differences between strain MET79T and these three species, there are also numerous phenotypic and genotypic differences (Table 1). Two other anaerobes isolated from oilfield ecosystems were reported to reduce nitrate, Deferribacter thermophilus and Denitrovibrio acetiphilus (Greene et al., 1997; Myhr & Torsvik, 2000). Neither bacterium belongs to the Clostridiales. The organism that is phylogenetically most closely related to Deferribacter thermophilus is Flexistipes sinusarabici (sequence similarity 88 %), whereas the closest relative of Denitrovibrio acetiphilus is Geovibrio ferrireducens (sequence similarity 86·9 %). In contrast to strain MET79T, Deferribacter thermophilus and Denitrovibrio acetiphilus are specialized in the oxidation of organic acids and are unable to ferment sugars (Greene et al., 1997; Myhr & Torsvik, 2000). Within cluster XII, strain MET79T has Caloranaerobacter azorensis (Wery et al., 2001) as its closest phylogenetic relative (sequence similarity 88·7 %). Strain MET79T differs from Caloranaerobacter azorensis, isolated from a deep-sea hydrothermal vent, by its cell-wall structure. Furthermore, Caloranaerobacter azorensis is a non-sporulating bacterium that does not reduce thiosulfate or nitrate but reduces elemental sulfur. The end products of glucose metabolism by these two bacteria are also very different (Table 1). The two strains also differ in the ranges and optima of growth conditions, in the range of substrates used and in the G+C content of DNA (Table 1).
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, 2000; Magot et al., 1997, 2000; Ravot et al., 1995a, b, 1999). Such activity might result in increasing biocorrosion processes in situ (Magot et al., 1997). In light of its phenotypic, genotypic and phylogenetic characteristics, strain MET79T represents a novel genus within cluster XII of the order Clostridiales that we propose to name Garciella nitratireducens gen. nov., sp. nov.
Description of Garciella gen. nov.
Garciella (Gar.ci.el'la. L. dim. ending -ella; N.L. fem. n. Garciella named in honour of the French microbiologist Jean-Louis Garcia, for his important contribution to the taxonomy of anaerobes).
Cells are straight rods with a Gram-positive-type cell wall. Terminal spores are formed. Growth is strictly anaerobic. Moderately thermophilic, fermentative member of the domain Bacteria, phylum Firmicutes, cluster XII of the order Clostridiales, family Clostridiaceae. Carbohydrates and organic acids serve as fermentable substrates. The type species is Garciella nitratireducens.
Description of Garciella nitratireducens sp. nov.
Garciella nitratireducens (ni.tra.ti.re.du'cens. N.L. n. nitratum nitrate; L. v. reduco to draw backwards, bring back to a state or condition; N.L. part. adj. nitratireducens nitrate-reducing).
Displays the following properties in addition to those given in the genus description. Cells (0·5–0·7x1·4–2·8 µm) occur singly or in pairs and possess one subpolar flagellum. Terminal spores appear in old cultures. Round colonies (2 mm diameter) develop in roll tubes after 1 week of incubation at 55 °C. Chemo-organotrophic. The optimum temperature for growth is 55 °C at pH 7·5; temperature range 25–60 °C. The optimum pH is 7·5; growth occurs between pH 5·5 and 9·0. Halotolerant, growing in the presence of up to 10 % NaCl with an optimum at 1 %. Yeast extract is required for growth and cannot be replaced by vitamins. Ferments cellobiose, fructose, galactose, glucose, lactose, maltose, mannose, ribose, sucrose, D-xylose, glycerol, mannitol, fumarate, lactate, malate, pyruvate and Casamino acids. Arabinose, raffinose, rhamnose, starch, cellulose, xylan, acetate, butyrate, propionate, methanol, ethanol, butanol, propanol, formate, methylamine, p-coumaric acid, ferulic acid, peptone, bio-Trypticase and H2 are not used. Lactate, acetate, butyrate, H2 and CO2 are produced during glucose fermentation. Thiosulfate is reduced to sulfide and nitrate to ammonium; elemental sulfur, sulfite, sulfate, fumarate and nitrite are not used as electron acceptors. Thiosulfate or nitrate enhance growth. Can grow in the presence of 25 µg kanamycin or chloramphenicol ml-1 and 100 µg ampicillin ml-1 but not in the presence of 10 µg vancomycin or rifampicin ml-1. The G+C content of the DNA of the type strain is 30·9 mol% (HPLC).
The type strain, MET79T (=DSM 15102T=CIP 107615T), was isolated from an oilfield separator in the Gulf of Mexico.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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