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Ignicoccus Gen. Nov., a Novel Genus of Hyperthermophilic, Chemolithoautotrophic Archaea, Represented by Two New Species, Ignicoccus Islandicus Sp

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Ignicoccus Gen. Nov., a Novel Genus of Hyperthermophilic, Chemolithoautotrophic Archaea, Represented by Two New Species, Ignicoccus Islandicus Sp International Journal of Systematic and Evolutionary Microbiology (2000), 50, 2093–2100 Printed in Great Britain Ignicoccus gen. nov., a novel genus of hyperthermophilic, chemolithoautotrophic Archaea, represented by two new species, Ignicoccus islandicus sp. nov. and Ignicoccus pacificus sp. nov. Harald Huber, Siegfried Burggraf, Thomas Mayer, Irith Wyschkony, Reinhard Rachel and Karl O. Stetter Author for correspondence: Karl O. Stetter. Tel: j49 941 943 3160. Fax: j49 941 943 2403. e-mail: Karl.Stetter!biologie.uni-regensburg.de Lehrstuhl fu$ r Mikrobiologie Two species of novel, chemolithoautotrophic, sulfidogenic micro-organisms und Archaeenzentrum, were isolated from submarine hydrothermal systems in the Atlantic (at the Universita$ t Regensburg, Universita$ tsstrasse 31, Kolbeinsey Ridge north of Iceland) and in the Pacific (at 9 SN, 104 SW). The 93053 Regensburg, coccoid cells grew within a temperature range of 70–98 SC (optimum around Germany 90 SC). They gained energy by reduction of elemental sulfur using molecular hydrogen as the electron donor. 16S rDNA-based sequence comparisons revealed that the organisms are members of the crenarchaeal branch of the Archaea. They represent a new, deeply branching lineage within the family of the Desulfurococcaceae. In DNA–DNA hybridization experiments both strains exhibited low levels of hybridization to each other and to further representatives of this family. Therefore, they represent a new genus, for which the name Ignicoccus gen. nov. is proposed. At present it consists of two new species, Ignicoccus islandicus sp. nov. (type strain is Kol8T l DSM 13165T l ATCC 700957T ) and Ignicoccus pacificus sp. nov. (type strain is LPC33T l DSM 13166T l ATCC 700958T ). Keywords: Archaea, Crenarchaeota, hyperthermophilic, marine, chemolithoautotrophic INTRODUCTION consisting of lobed or coccoid-shaped thermoacido- philes, Thermoproteales, which harbours all rod- Within the Archaea, hyperthermophilic micro- shaped organisms of the kingdom, and the recently organisms growing optimally at temperatures between described order Desulfurococcales (Huber & Stetter, 80 and 110 mC are found in both kingdoms, the 2000). Desulfurococcales is composed of two families: Euryarchaeota and the Crenarchaeota (Stetter, 1988, the Pyrodictiaceae, members of which grow optimally 1996; Woese et al., 1990). Within the Euryarchaeota above 100 mC, and the representatives of the Desulfuro- they are represented by deep-branching organisms coccaceae, which exhibit optimal growth between 85 like Methanopyrus kandleri and members of the and 100 mC (Burggraf et al., 1997). The representatives genera Thermococcus, Pyrococcus, Methanothermus, of the Desulfurococcaceae are usually regular to Methanococcus and Archaeoglobus. So far, the cul- irregular cocci, which occur singly or in pairs. Some tivated Crenarchaeota are exclusively extremely species form chains or aggregates in addition. With the thermophilic or hyperthermophilic (Huber & Stetter, exception of the aerobic Aeropyrum pernix, all 1999). 16S rRNA-based sequence comparisons have members of the Desulfurococcaceae are obligate revealed that three orders are evident within the anaerobes, growing heterotrophically by sulfur res- Crenarchaeota (Burggraf et al., 1997): Sulfolobales, piration of various organic compounds (producing H#S) or by fermentation. In both cases, yeast extract, ................................................................................................................................................. peptides or sugars serve as substrates. Organic acids or The EMBL accession numbers for the 16S rDNA sequences of Ignicoccus alcohols are found as metabolic products (Huber & islandicus and Ignicoccus pacificus are X99562 and AJ271794, respectively. Stetter, 1999). 01444 # 2000 IUMS 2093 H. Huber and others In this study we describe the isolation and properties For quantitative determinations, H#S was analysed by of novel, chemolithoautotrophic members of the titration (Williams et al., 1979). Desulfurococcaceae which grow by sulfur reduction Lipid analysis. Core lipids were analysed according to with molecular hydrogen as electron donor. Trincone et al. (1992). DNA isolation and DNA base composition. DNAs were METHODS prepared as described previously (Wildgruber et al., 1982). The GjC content of genomic DNAs was determined by Sources of samples. At the Kolbeinsey Ridge, north of melting point analysis (Marmur & Doty, 1962) and by direct Iceland, eight samples of submarine sandy sediments and analysis of the nucleotides after digestion of the DNA with venting water (original temperatures around 90 mC) were nuclease P1 and separation by HPLC chromatography taken by the research submersible ‘Geo’ at depths between (Vo$ lkl et al., 1993). Calf thymus DNA was used as reference. 103 and 106 m (Fricke et al., 1989; Burggraf et al., 1990). Furthermore, black smoker samples were obtained during DNA–DNA hybridization. DNA–DNA hybridization was dive 3072 of the submersible ‘Alvin’ at the East Pacific carried out using the filter technique (Gillespie & Gillespie, Rise at 9m N, 104m W at a depth of 2500 m. The samples 1971; Birnstiel et al., 1972) as described by Pley et al. (1991). were brought to our laboratory anaerobically without Nucleic acids were hybridized under optimal conditions temperature control. (25 mC below TM in 3iSSC buffer at 65 mC) (Marmur & Doty, 1961; Brenner, 1973; Meyer & Schleifer, 1978) using Strains and culture conditions. The new isolates were the DNAs of Kol8T and LPC33T as probes. enriched and cultivated in strictly anaerobic half-strength SME medium (Stetter et al., 1983; Pley et al., 1991), prepared 16S rRNA analysis. The nearly complete 16S rRNA genes of according to Balch & Wolfe (1976). The medium contains the new isolates were PCR-amplified (Saiki et al., 1985, −" the following components (l ): NaCl, 13n85 g; MgSO%; 1988). The primers used in the amplification corresponded 7H O, 3 5 g; MgCl ;6H O, 2 75 g; KH PO ,05g; to positions 8–23 (TCYGGTTGATCCTGCC), and # n # # n # % n T CaCl#;2H#O, 0n38 g; KCl, 0n33 g; (NH%)#SO%,0n25 g; 1512–1492 (ACGGHTACCTTGTTACGACTT) for Kol8 NaBr, 0 05 g; H BO ,0015 g; SrCl ;6H O, 7 5mg; KI or 1406–1390 (ACGGGCGGTGTGTRCAA) for LPC n " $ $ n # # n (1 mg ml− ), 25 µl; elemental sulfur, 5n0 g. Reduction of the strains (Escherichia coli 16S rRNA numbering; Brosius et al., medium was carried out by addition of 20 ml Na#S(2n5%, 1981). Both strands of the PCR products were directly w\v); afterwards, the pH was adjusted at room temperature sequenced as described by Burggraf et al. (1997). The T T to 5n5 with sulfuric acid. The organisms were grown routinely sequences (Kol8 , 1465 bases; LPC33 , 1311 bases; LPC37, in 120 ml serum bottles containing 20 ml medium pres- 1297 bases) were aligned with a set of representative archaeal surized with H#\CO# (80:20, v\v; 250 kPa). Incubation was sequences using the ARB program (W. Ludwig & O. Strunk, carried out at 90 mC with shaking (100 r.p.m.). Heterotrophic 1998, http:\\www.mikro.biologie.tu-muenchen.de\pub\ growth was tested under a gas phase of N#\CO# (80:20, v\v; ARB\). Dendrograms were computed with the neighbour- 200 kPa). joining, maximum-parsimony and maximum-likelihood methods included in the ARB package. Unless otherwise stated, organic substrates and alternative electron acceptors (thiosulfate, sulfite, sulfate, nitrate and nitrite) were added at final concentrations of 0n1%. Batch RESULTS cultures were grown in a 300 l enamel-protected fermenter (HTE Bioengineering) at 90 mC with stirring (100 r.p.m.) and Enrichment and isolation −" gassing with H#\CO# (80:20; 2 l min ). To enrich chemolithoautotrophic, sulfur-reducing Light and electron microscopy. Cells were routinely observed hyperthermophiles, serum bottles with 20 ml half- with an Olympus BX 60 phase-contrast microscope with an strength SME medium supplemented with 1% (w\v) oil immersion objective, UPlanFl 100\1n3. Bacterial growth sulfur (gas phase H#\CO#) were inoculated with about was followed by direct cell counting using a Thoma chamber 1 g of the sandy sediments from the Kolbeinsey Ridge (depth 0n02 mm). Electron microscopy was performed as follows. For direct visualization, cells were chemically fixed or rocky black smoker material obtained from the by adding glutaraldehyde (2%, v\v, final concn) to the deep sea of the East Pacific Rise. The enrichment culture medium, concentrated by centrifugation, applied attempts were incubated with shaking at 90 mC. After onto a carbon-coated copper grid and shadowed with 2 d, irregular cocci had grown in 3 out of 10 samples T T 1nmPt\C (angle 15m). For ultrathin sections, cells were (Kol8 , LPC33 and LPC37) and large amounts of cultivated in cellulose capillary tubes, high-pressure frozen, H#S could be detected qualitatively in the culture freeze-substituted in acetone containing 1% OsO% and medium. The enrichment cultures were successfully embedded in Epon\Araldite (Rieger et al., 1997). Sections transferred into fresh medium and cells were first were stained with uranyl acetate and lead citrate. For freeze- purified by serial dilution carried out three times using etching, a concentrated cell suspension was frozen in liquid the same medium. In addition, the ‘optical tweezer’ nitrogen, freeze-etched for 4 min at 97 C and shadowed k m et al with 1 nm Pt\C (angle 45m) and with 10 nm C (angle 90m). technique was used for final purification (Huber ., Replicas were cleaned overnight on sulfuric acid (70%, 1995). The isolates were designated as the samples. w\v).
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