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Thermoanaerobacter Siderophilus Sp. Nov., a Nove I D I Ss I M I I a T Ory Fe

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Thermoanaerobacter Siderophilus Sp. Nov., a Nove I D I Ss I M I I a T Ory Fe International Journal of Systematic Bacteriology (1 999), 49, 147 1-1 478 Printed in Great Britain Thermoanaerobacter siderophilus sp. nov., a noveI di ss im i I at ory Fe(I I I) = reduc i n g, a naero b i c, thermophilit bacterium A. I. Slobodkin, T. P. Tourova, B. B. Kuznetsov, N. A. Kostrikina, N. A. Chernyh and E. A. Bonch-Osmolovskaya Author for correspondence: Alexander Slobodkin. Tel: +7 95 135 4458. Fax: +7 95 135 6530. e-mail : slobodki @inmi.host. ru Institute of Microbiology, A thermophilic, anaerobic, spore-forming, dissimilatory Fe(lll)-reducing Russian Academy of bacterium, designated strain SR4T, was isolated from sediment of newly Sciences, Prospect 60-letiya Oktyabrya 7/2, 11781 1 formed hydrothermal vents in the area of the eruption of Karymsky volcano Moscow, Russia on the Kamchatka peninsula. Cells of strain SR4T were straight-to-curved, peritrichous rods, 04-0-6 pm in diameter and 3-5-9.0 pm in length, and exhibited a slight tumbling motility. Strain SR4T formed round, refractile, heat- resistant endospores in terminally swollen sporangia. The temperature range for growth was 39-78 "C, with an optimum at 69-71 "C. The pH range for growth was 48-8-2, with an optimum at 63-6-5. Strain SR4T grew anaerobically with peptone as carbon source. Amorphous iron(ll1) oxide present in the medium stimulated the growth of strain SR4T; cell numbers increased with the concomitant accumulation of Fe(ll). In the presence of Fe(lll), strain SR4T grew on H,/CO, and utilized molecular hydrogen. Strain SR4T reduced 9,lO- anthraquinone-2,6-disulfonic acid, sulf ite, thiosulfate, elemental sulfur and MnO,. Strain SR4T did not reduce nitrate or sulfate and was not capable of growth with 0,. The fermentation products from glucose were ethanol, lactate, H, and CO,. The G+C content of DNA was 32 molo/o. 16s rDNA sequence analysis placed the organism in the genus Thermoanaerobacter. On the basis of physiological properties and phylogenetic analysis, it is proposed that strain SR4T (= DSM 122993 should be assigned to a new species, Thermoanaerobacter siderophilus sp. nov. Keywords : Thermoanaerobacter, Fe(II1) reduction, Mn(IV) reduction, therrnophiles, magnetite INTRODUCTION restrial subsurface (Boone et al., 1995; Liu et al., 1997) and submarine petroleum reservoirs (Greene et al., Reduction of Fe(II1) by micro-organisms has im- 1997). portant implications in the cycling of iron and organic matter and has been intensively studied in marine and Dissimilatory Fe(II1)-reducing micro-organisms can freshwater anoxic sediments and submerged soils be subdivided into several physiological groups ac- (Lovley, 1991, 1995; Nealson & Saffarini, 1994). cording to the electron donor used for Fe(II1) re- Dissimilatory Fe(II1)-reducing micro-organisms have duction : (i) fermentative, which use Fe(II1) reduction also been found in a variety of thermobiotic environ- as a minor pathway for electron flow while fermenting ments, including sediments of hydrothermal vents and sugars or amino acids ; (ii) hydrogen-oxidizing ; (iii) hot springs (Slobodkin et al., 1995; Slobodkin & sulfur-oxidizing ; and (iv) organisms that oxidize Wiegel, 1997), sedimentary basins in the deep ter- poorly fermentable substrates, such as organic acids, alcohols and aromatic compounds. Abbreviation: AQDS, 9,l O-anthraquinone-2,6-disulfonic acid. Iron-reducing thermophiles available in pure culture The GenBank accession number for the 165 rDNAsequence of strain SR4T is are represented by several phylogenetically diverse AFI 20479. micro-organisms. The aerobic archaeon Sulfolubus 00967 0 1999 IUMS 1471 A. I. Slobodkin and others acidocaldarius reduces Fe(II1) with elemental sulfur molecular hydrogen to serve as an electron donor was (Brock & Gustafson, 1976). The anaerobic Bacillus studied in 60-ml flasks containing 10 ml medium and H, infernus reduces Fe(II1) with formate or lactate as the (100 %) or H,/CO, (5:95 v/v) as the gas phase. The cultures were incubated for 2 weeks and the ability to utilize a electron donor (Boone et al., 1995). The anaerobic particulate substrate was judged from culture growth and (eu)bacteria Deferribacter thermophilus (Greene et Fe(I1) accumulation. A medium in which the organic carbon al., 1997) and Thermoterrabacteriurn ferrireducens source had been omitted was used as a control. (Slobodkin et al., 1997) couple Fe(II1) reduction with the oxidation of complex organic substrates, organic The ability to use various electron acceptors was studied in acids, alcohols and molecular hydrogen. Recently, the the basal medium containing peptone (10 g 1-l) as a sole electron donor, in which amorphous iron(II1) oxide was ability to reduce Fe(II1) with glycerol under oxygen omitted. The electron acceptors were added from autoclaved limitation was shown for the moderately thermophilic stock solutions. MnO, was prepared by the method of acidophiles Sulfobacillus thermosulfidooxidans, Sulfa- Lovley & Phillips (1988). The medium was pre-reduced with bacillus acidophilus and Acidimicrobium ferrooxidans Na2S.9H,O (0.5 g 1-l) in the experiments with sulfate, sulfite, (Bridge & Johnson, 1998). thiosulfate and elemental sulfur. No reducing agent was present in media containing 0,, MnO, or 9,lO-anthra- In this paper, we describe an anaerobic, dissimilatory quinone-2,6-disulfonic acid (AQDS). Both reduced and Fe(II1)-reducing, thermophilic bacterium, Thermo- reducing-agent-free media were used in nitrate-amended anaerobacter siderophilus sp. nov., isolated from hy- experiments. Cultures grown in pre-reduced basal medium drothermal vents on the Kamchatka peninsula. without any electron acceptor were used as inocula (5% v/v). The use of the electron acceptors was judged from culture growth (for all acceptors), sulfide production (for METHODS sulfate, sulfite, thiosulfate and elemental sulfur), change of Environmental samples. Samples of sediments and water visible colour of the medium or precipitate (for MnO, and were collected in March 1997 from newly formed hydro- AQDS) and from the accumulation of Mn(I1) (for MnO,). thermal vents in the area of the eruption of Karymsky Temperature, pH and NaCl concentration ranges for growth volcano on the Kamchatka peninsula. The temperatures at and susceptibility to antibiotics were determined in basal the sampling sites ranged from 70 to 94 "C, pH from 6.1 to medium in which amorphous iron(II1) oxide was omitted 7.1 and E, from -215 to -305 mV. and peptone was replaced by glucose (5 g 1-l). The medium Media and cultivation. A basal medium used for enrichment, was pre-reduced with Na,S.9H20 (0.5 g 1-l). The pH range isolation and cultivation of Fe(II1)-reducing bacteria was for growth was determined at 70 "C. The pH was adjusted prepared anaerobically by boiling and cooling it under CO, with sterile stock solutions of HC1 or NaOH and measured (100 %)gas phase. The basal medium contained (IF1 distilled at 70 "C with a model PHM 82 pH meter (Radiometer) water): 0-33 g KH,PO,, 0.33 g NH,Cl, 0.33 g KCl, 0.33 g equipped with a temperature probe and calibrated at 70 "C. g g MgC1,.2H20, 0.33 g CaC1,.2H20, 2.0 NaHCO,, 10 Microscopy. Routine examinations and cell counting were peptone, 0.20 g yeast extract (Difco), 10 ml vitamin solution performed under a phase-contrast Amplival microscope (Wolin et al., 1963) and 1 ml trace-element solution (Carl Zeiss Jena). Transmission electron microscopy was (Slobodkin et at., 1997). The pH was adjusted to 65-64 (at performed with a model JEM- 100 electron microscope 25 "C) with 10% (w/v) NaOH. No reducing agent was (JEOL) as described previously (Bonch-Osmolovskaya added to the medium. Fe(II1) was provided in the form of et 1990). Gram staining was performed according to Norris amorphous iron(II1) oxide at about 90 mmol Fe(II1) 1-1 al., & Swain (1971). medium. The amorphous iron(II1) oxide was synthesized by titrating a solution of FeCl, with 10% (w/v) NaOH to pH Analytical techniques. Fe(II1) reduction was monitored by 9.0. The pH of the autoclaved medium measured at 70 "C measuring the accumulation of Fe(I1) over time. Fe(I1) was was 6-8-6-9. measured by adding a 0.5 ml sample from the culture to 5 ml Unless otherwise noted, enrichments and pure cultures were 0.6 M HCl. After 24 h extraction, HCl-soluble Fe(I1) was grown in 10 ml medium in Hungate tubes under an determined with 2,2'-dipyridyl (Balashova & Zavarzin, atmosphere of CO, (100O/0). All transfers and sampling of 1980). Iron-containing precipitate was analysed by X-ray cultures were performed with syringes and needles. The diffraction analysis (Slobodkin et al., 1995). Mn(I1) was medium was heat-sterilized at 135 "C for 30 min. All analysed by atomic absorption spectrophotometry after incubations were at 70 "C unless otherwise noted. HC1 extraction (Lovley & Phillips, 1988). Determination of short-chain organic acids, alcohols and gaseous products of Physiological studies. Growth of bacteria in medium con- metabolism was performed by GC; sulfide was determined taining amorphous iron(II1) oxide or other insoluble com- by a colorimetric method as described previously (Slobodkin pounds was determined by direct counting with a phase- & Bonch-Osmolovskaya, 1994). contrast microscope and a counting chamber. In media with soluble components, growth was determined by counting Cultivation of referencestrains. Thermoanaerobacter suyuro- and by measuring the increase in optical density at 600 nm philus strain L-64T (= DSM 1 1584T)was from the culture (Spekol 10; Carl Zeiss Jena). collection of the Laboratory of Hyperthermophilic Mi- crobial Communities, Institute of Microbiology, Russian The ability of the organism to grow on different substrates Academy of Sciences, Moscow, Russia. Thermoanaerobacter was determined in basal medium, in which peptone was wiegelii strain Rt8.BlT(= DSM 10319T)was obtained from replaced by autoclaved or filter-sterilized substrates, both in the Deutsche Sammlung von Mikroorganismen und Zell- the presence and in the absence of amorphous iron(II1) kulturen, Braunschweig, Germany.
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