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1 Portland State University, Department of Biology, Portland, OR 97201, USA
2 Department of Microbiology, College of Biological Science, University of Guelph, Guelph, Ontario, Canada N1G 2W1
Correspondence
A.-L. Reysenbach
reysenbacha{at}pdx.edu
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; Pitulle et al., 1994). All members of the Aquificales, with the exception of ‘Hydrogenobacter subterraneus’, are chemolithoautotrophic, microaerophilic, thermophilic to hyperthermophilic, hydrogen-oxidizing (‘Knallgas’) bacteria (Aragno, 1992). Currently, the order Aquificales harbours seven genera: Aquifex (Huber et al., 1992), Hydrogenobacter (Saveleva et al., 1982; Kawasumi et al., 1984; Stöhr et al., 2001), Hydrogenobaculum (Shima & Suzuki, 1993; Stöhr et al., 2001), Thermocrinis (Huber et al., 1998; Eder & Huber, 2002), Hydrogenothermus (Stöhr et al., 2001), Persephonella (Götz et al., 2002) and the recently described Sulfurihydrogenibium (Takai et al., 2003). Members of the order are widespread in both terrestrial and deep-sea hydrothermal systems and have been isolated from shallow marine (Huber et al., 1992; Nishihara et al., 1990; Stöhr et al., 2001) and terrestrial hydrothermal systems (Kryukov et al., 1983; Kawasumi et al., 1984; Shima & Suzuki, 1993; Huber et al., 1998; Kristjansson et al., 1985), from heated compost (Beffa et al., 1996), from deep-sea hydrothermal vents (Reysenbach et al., 2000a) and recently from a subsurface gold mine (Takai et al., 2002, 2003).
Using molecular phylogenetic techniques it has been shown that near neutral terrestrial thermal springs (above 65 °C) are often dominated by members of the Aquificales (Yamamoto et al., 1998; Reysenbach et al., 2000b; Skirnisdottir et al., 2000) and referred to as ‘black filaments' (Reysenbach et al., 2000b) or ‘sulfur-turf’ (Yamamoto et al., 1998; Hjörleifsdottir et al., 2001) due to their tendency to form extensive microbial mats that appear black or yellow from iron or sulfur mineral deposits. Using a combination of culture-dependent techniques and molecular analyses, we isolated the first terrestrial representative of these Aquificales from a terrestrial hot spring in the Azores, Portugal (Reysenbach et al., 2002a), and we propose a new species, Sulfurihydrogenibium azorense sp. nov.
Water and filamentous biomass samples were collected in Bellco serum bottles (Bellco Glass) in the area of Água do Caldeirão, Furnas, on São Miguel Island, Azores, in January of 2001. The temperature measured at the sampling sites varied between 65 and 70 °C and the pH varied between 5·9 and 7·0. A sample (0·5 ml) was inoculated into 5 ml modified MSH medium with a final gas phase of CO2/O2/H2 (41·6 : 1·8 : 56·6, by vol., 242·5 kPa). Modified MSH medium (Boone et al., 1989) was prepared with anoxic distilled water under a CO2 atmosphere and contained (l-1): 2 g NaOH, 0·5 g KCl, 1·36 g MgCl2.6H2O, 7 g MgSO4.7H2O, 2 g Na2S2O3.5H2O, 0·4 g CaCl2.2H2O, 0·2 g NH4Cl, 0·3 g K2HPO4.3H2O and 10 ml of a trace element stock solution (adapted from Ferguson & Mah, 1983). Prior to autoclaving, the pH of the medium was adjusted to 6·0 with 10 M NaOH. O2 was added after autoclaving and the tubes were pressurized with H2 after inoculation.
Enrichments were incubated for 1 day at 70 °C, without agitation, and immediately transferred. The cultures were purified by four consecutive end-point dilutions on modified MSH medium. Colonies were isolated on 2 % (w/v) gelrite roll tubes (Jones et al., 1983). The gelrite medium (iron-reducing or H2-oxidizing) was supplemented with 0·001 % (w/v) CuSO4.5H2O, according to Masaharu et al. (1987). Pure cultures were stored in modified MSH medium containing 15 % (v/v) glycerol both at -80 °C and in liquid nitrogen.
Growth was determined either by measuring changes in OD600, by total protein content (Coomassie protein assay) or by direct cell counts using a Petroff–Hauser counting chamber. Unless otherwise stated, all growth experiments were done at 68 °C, under the microaerophilic conditions described above, and conducted in triplicate. Az-Fu1T growth with and without agitation was compared. The effect of pH on growth was determined from pH 4·0 to 8·5 using acetate/acetic acid buffer, MES, PIPES, HEPES and Tris/HCl. The pH of the medium was adjusted prior to autoclaving, checked after 1 h incubation at 68 °C and checked again at the end of growth. NaCl requirements were determined at 0–4 % (w/v) NaCl. Oxygen requirements and tolerance were determined by injecting defined volumes of pure O2 into culture tubes. O2 final concentrations from 0 to 12 % (v/v) were tested. The optimal temperature for growth was determined by calculating specific growth rates of cultures incubated at various temperatures. The relationship of specific growth rate to temperature was then fitted with TableCurve (2D Windows, v4.07; AISN Software) to the square-root equation Ratkowsky et al. (1982).
Electron acceptors and electron donors were added after autoclaving to a minimal medium (modified MSH medium without Na2S2O3 and with only 4 g MgSO4.7H2O l-1 to ensure an adequate sulfur source) (Table 1). Soluble (ferric citrate, 10 mM) and insoluble (ferrihydrite) iron (III) (10 mM) was used. Ferrous iron was added at 10 mM, sulfur was added at 1 % (w/v) and 
was tested at 10 mM final concentration. 
, 
, 
, and 
were added according to Takai et al. (2002) and all other electron donors and acceptors were at concentrations reported by Götz et al. (2002). Controls contained no electron acceptor and no electron donor. Abiotic controls were also used when necessary to validate the tests. Additionally, growth of Sulfurihydrogenibium subterraneum under similar conditions was used as a control.
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Gram staining was carried out using standard procedures. For electron microscopy, samples were shipped overnight to Department of Microbiology, College of Biological Science, University of Guelph, Canada, in 1 % (v/v) glutaraldehyde. The samples were treated as described by Götz et al. (2002) using standard glutaraldehyde/osmium tetroxide fixation and LR White embedding regimens for thin sectioning (Beveridge et al., 1994).
Genomic DNA was extracted according to Götz et al. (2002). For the determination of DNA base composition, DNA was extracted from 1 g wet wt of the culture cell pellet. The cells were disrupted with a French pressure cell and the DNA was purified on hydroxyapatite according to the procedure of Cashion et al. (1977). For the DNA base composition the genomic DNA was hydrolysed according to Mesbah et al. (1989). The resulting deoxyribonucleosides were analysed by HPLC. Ten microlitres of sample were loaded in an HPLC system with a SelectaPore 90M, C18, 5 µm (250x4·6 mm) analytical column and the run was performed at 45 °C, with a 0·3 M (NH4)H2PO4/acetonitrile solvent, 40 : 1 (v/v), pH 4·4, at 1·3 ml min-1 (adapted from Tamaoka & Komagata, 1984). The calibration was done using non-methylated 
DNA (Sigma; G+C content 49·86 mol%) and the G+C content was calculated according to Mesbah et al. (1989).
The 16S rRNA genes were amplified by PCR from genomic DNA, purified and sequenced as described by Götz et al. (2002). Platinum Taq DNA polymerase high fidelity (Invitrogen) was used to confirm the sequence as two single mismatches were detected in the sequence. A total of 1447 nt were sequenced. Sequence alignment and phylogenetic analyses were done as described previously (Götz et al., 2002) using 1379 homologous nucleotides. Due to using a subset of Aquificales sequences and based on sequence alignments and secondary structure comparisons, 1430 nt were used to construct distance matrices by pairwise analysis with the Jukes & Cantor (1969) correction.
The new isolate Az-Fu1T is a thermophilic chemolithoautotrophic ‘Knallgas' bacterium isolated from the Furnas hot springs, São Miguel, Azores. Light brown-white filamentous clumps appeared in the liquid medium after 24 h incubation. Based on initial 16S rRNA gene sequence all the isolates (five cultures) were 100–99 % similar in sequence and the isolate designated strain Az-Fu1T (previously designated Fc8A70; Reysenbach et al., 2002a) was chosen for further study, although optimal growth conditions were confirmed for all strains. Translucent colonies were obtained from gelrite roll tubes under iron-reducing and H2-oxidizing conditions. Successful transfer of the strains required a 5–10 % mid-exponential-growth-phase inoculum.
The isolate is phylogenetically most closely related to the uncultivated Aquificales environmental 16S rDNA sequence SRI-40 (Fig. 4) obtained from Icelandic hot springs (Skirnisdottir et al., 2000; 0·2 % phylogenetic distance), although its closest relative in culture is Sulfurihydrogenibium subterraneum (Takai et al., 2003; 2·0 % distance). Furthermore, the Az-Fu1T 16S rDNA sequence is 3·1 % distant from its Yellowstone relative, strain YNP-SS1 (Reysenbach et al., 2002b) and only about 18 % distant from Aquifex pyrophilus. Az-Fu1T is also 7·7 and 6·8 % distant from the recently described lineages Persephonella marina and Hydrogenothermus marinus, respectively, and differs significantly from these lineages in their physiological growth requirements (Table 2). The G+C content of the DNA of strain Az-Fu1T is 33·6 mol%. Two mismatches were detected in the 16S rRNA gene sequence which were confirmed to be real by RT-PCR and by cloning. These are located at Escherichia coli 16S rRNA positions 818 and 888. Furthermore, two 16S rRNA genes were detected in the Sulfurihydrogenibium strain Az-Fu1T genome sequence (A.-L. Reysenbach & J. F. Heidelberg, unpublished data).
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). The flagella were unsheathed and had a diameter of 
15 nm, which is typical for many bacteria (Wilson & Beveridge, 1993). Endospores were not observed. Thin sections showed a typical Gram-negative cell envelope complete with outer and plasma membranes (Fig. 2) although, like Persephonella marina (Götz et al., 2002), it was difficult to differentiate the peptidoglycan layer as a distinct entity. When grown with H2 the cells tended to cluster, forming macrofilaments (clumps of filaments), even while agitated. Under iron-oxidizing and iron-reducing conditions, Az-Fu1T cells were often found attached to minerals. Thin sections of samples grown under H2-oxidizing conditions, in the presence of S°, revealed unidentified structures that resembled internal stacked membranes with a particle periodicity on them (Fig. 3). Similar, but smaller membranous structures, have previously been reported for another member of the Aquificales, i.e. Persephonella (Götz et al., 2002). Such structures were not reported for Sulfurihydrogenibium subterraneum (Takai et al., 2002, 2003). Although internal membranes are often used to align enzymes for complex metabolic reactions, the function of these membranous structures is not yet known. Alternatively, these structures may resemble cytoplasmic axial filaments as have been reported for Escherichia coli (Okada et al., 1994); however, this is speculative without purification and extensive characterization of these structures.
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as electron acceptor. Strain Az-Fu1T grew with up to 9·0 % oxygen, with optimal growth between 1·8 and 2·0 % (v/v). There was no growth in the presence of 12·0 % (v/v) oxygen. Growth under hydrogen-oxidizing conditions was enhanced by the presence of sulfur compounds (S°, 
or 
) as reported for Hydrogenobacter (Bonjour & Aragno, 1986). Az-Fu1T is able to use ferrous iron (Fe2+) as electron donor in the presence of O2 or S°, and like Sulfurihydrogenibium subterraneum (Takai et al., 2002, 2003) ferric iron (Fe3+) can be used as electron acceptor in the presence of H2 and S°. Sulfurihydrogenibium subterraneum was also tested for iron oxidation and, like Az-Fu1T, it is capable of using ferrous iron (Fe2+) as electron donor in the presence of O2.
Comparison with related genera and species
Together with Sulfurihydrogenibium subterraneum, Az-Fu1T forms a distinct bacterial lineage within the Aquificales (Fig. 4
), with a similar low G+C content. Both strains share many characteristics with the rest of the Aquificales, such as microaerophilic growth. However, their distinct ability to use heavy metals and iron compounds as electron donors or acceptors (Tables 1 and 2) distinguish them from other members of the Aquificales.
There are several distinguishing features that set Az-Fu1T apart from Sulfurihydrogenibium subterraneum, such as salt tolerance and pH growth optima (Table 2). These differences may reflect their different habitats; Az-Fu1T has been obtained from terrestrial hot springs whereas Sulfurihydrogenibium subterraneum was obtained from a warm subterranean gold mine. Furthermore, unlike Sulfurihydrogenibium subterraneum, Az-Fu1T cannot grow aerobically, nor can it use nitrate as an electron acceptor. With the exception of Hydrogenothermus marinus and ‘Aquifex aeolicus’ (Table 2), all marine Aquificales isolates described to date are able to grow with O2 and 
as electron acceptors and H2 as an electron donor, suggesting that perhaps Sulfurihydrogenibium subterraneum is more marine in origin. Furthermore, based on a conservative estimate and comparing only homologous nucleotides, Az-Fu1T is 2 % different from Sulfurihydrogenibium subterraneum in the 16S rRNA sequence. Based on the phylogenetic position and distinct physiological characteristics of Az-Fu1T, we propose that this isolate be named Sulfurihydrogenibium azorense.
Description of Sulfurihydrogenibium azorense sp. nov.
Sulfurihydrogenibium azorense (a.zo.ren'se. N. L. neut. adj. azorense from the Azores, the place of isolation).
Motile rods, 0·4–0·5x0·9–2·0 µm. Cells can occur singly, in pairs or in filamentous clumps. Colonies are translucent. Grows best in the presence of sulfur compounds. Optimal growth occurs at 68 °C and growth occurs from 55 to 73 °C. The optimal pH for growth is 6·0, with a range from 5·5 to 7·0. Grows fastest with 0·1 % (w/v) NaCl; growth is inhibited with NaCl concentrations above 0·25 %. Not capable of growth at 12 % (v/v) O2 final concentration. Doubling time of 2·5 h with O2 as electron acceptor and H2 as electron donor. Cells utilize H2, thiosulfate, S° or Fe2+ as electron donors and O2, S° and Fe3+ as electron acceptors, but cannot use nitrate as electron acceptor. The G+C content is 33·6 mol%. Isolated from a terrestrial hot spring (68·4 °C, pH 5·9) in the Água do Caldeirão area, Furnas, on São Miguel Island, Azores. The type strain is Az-Fu1T (=DSM 15241T=OCM 825T). The GenBank accession number for the 16S rRNA sequence of Az-Fu1T is AF528192.
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+O2, S°+Fe3+ and H2+Fe3+, but could not grow with O2+
or H2+
. Data for Sulfurihydrogenibium subterraneum are taken from Takai et al. (2003)
