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Pyrobaculum Calidifontis Sp. Nov., a Novel Hyperthermophilic Archaeon That Grows in Atmospheric Air

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Pyrobaculum Calidifontis Sp. Nov., a Novel Hyperthermophilic Archaeon That Grows in Atmospheric Air Archaea 1, 113–121 © 2002 Heron Publishing—Victoria, Canada Pyrobaculum calidifontis sp. nov., a novel hyperthermophilic archaeon that grows in atmospheric air TAKU AMO,1 MARIA LUZ F. PAJE,2 AKIKO INAGAKI,1 SATOSHI EZAKI,1 HARUYUKI ATOMI1 and TADAYUKI IMANAKA1,3 1 Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering, Kyoto University,Yoshida-Honmachi, Sakyo-ku, Kyoto 606-8501, Japan, and Core Research for Evolutional Science and Technology Program of Japan Science and Technology Corporation (CREST-JST), Kawaguchi, Saitama 332-0012, Japan 2 National Institute of Molecular Biology and Biotechnology, University of the Philippines LosBaños, College Laguna 4031, Philippines 3 Author to whom correspondence should be addressed ([email protected]) Received May 10, 2001; accepted March 1, 2002; published online March 27, 2002 Summary A novel, facultatively aerobic, heterotrophic Stetter 1998). Many hyperthermophiles reported thus far are hyperthermophilic archaeon was isolated from a terrestrial hot strictly anaerobic (Amend and Shock 2001), possibly because spring in the Philippines. Cells of the new isolate, strain VA1, the availability of oxygen in hydrothermal environments is were rod-shaped with a length of 1.5 to 10 µm and a width of low as a result of the low solubility of oxygen at high tempera- 0.5 to 1.0 µm. Isolate VA1 grew optimally at 90 to 95 °C and tures. All hyperthermophilic members of the Euryarchaeota pH 7.0 in atmospheric air. Oxygen served as a final electron ac- are strict anaerobes, and respire predominantly by sulfur or ceptor under aerobic growth conditions, and vigorous shaking sulfate reduction, methanogenesis or fermentation (Huber and of the medium significantly enhanced growth. Elemental sul- Stetter 1998). In Crenarchaeota, a few hyperthermophiles have fur inhibited cell growth under aerobic growth conditions, been found that utilize oxygen as a terminal electron acceptor whereas thiosulfate stimulated cell growth. Under anaerobic (Castresana and Moreira 1999). The hyperthermophilic growth conditions, nitrate served as a final electron acceptor, archaeon Aeropyrum pernix has been shown to be an obligate but nitrite or sulfur-containing compounds such as elemental aerobe (Sako et al. 1996), and some Sulfolobus species, with sulfur, thiosulfate, sulfate and sulfite could not act as final elec- optimal growth temperatures in the range of 80 to 85 °C (Gro- tron acceptors. The G+C content of the genomic DNA was gan 1989), can also utilize oxygen (Brock et al. 1972). Further- 51 mol%. Phylogenetic analysis based on 16S rRNA se- more, a neutrophilic facultative aerobe, Pyrobaculum quences indicated that strain VA1 exhibited close relationships oguniense (Sako et al. 2001), and a few acidophilic facultative to species of the genus Pyrobaculum. A DNA–DNA hybridiza- aerobes, such as Acidianus infernus (Segerer et al. 1986) and tion study revealed a low level of similarity (≤ 18%) between Sulfurisphaera ohwakuensis (Kurosawa et al. 1998), have strain VA1 and previously described members of the genus been identified. There have also been reports on the isolation Pyrobaculum. Physiological characteristics also indicated that strain VA1 was distinct from these Pyrobaculum species. Our of facultative microaerobes, including Pyrobaculum aero- results indicate that isolate VA1 represents a novel species, philum (Völkl et al. 1993), Pyrolobus fumarii (Blöchl et al. named Pyrobaculum calidifontis. 1997) and Aquifex pyrophilus (Huber et al. 1992), which grow optimally at oxygen concentrations below 5% (v/v) in the gas Keywords: aerobic respiration, hyperthermophile, nitrate res- phase (Adams and Kelly 1998). piration. At present, the genus Pyrobaculum comprises five species: Pyrobaculum islandicum (Huber et al. 1987), P. organotroph- um (Huber et al. 1987), P. aerophilum (Völkl et al. 1993), Introduction P. arsenaticum (Huber et al. 2000) and P. oguniense (Sako et Hyperthermophiles are defined as microorganisms that grow al. 2001). Despite the small number of species, this genus is di- optimally at temperatures above 80 °C (Stetter 1999), or as mi- verse in terms of the physiological characteristics of its mem- croorganisms that can grow at temperatures above 90 °C (Ad- bers. Pyrobaculum islandicum and P.organotrophum are strict ams and Kelly 1998). A vast number of hyperthermophiles anaerobes, growing heterotrophically with elemental sulfur or have been isolated from marine hydrothermal systems, heated oxidized sulfur-containing compounds as electron acceptors sediments, terrestrial solfataras and hot springs (Huber and (Huber et al. 1987). Pyrobaculum islandicum can also reduce Stetter 1998). They are diverse with respect to their phylogeny ferric iron under organotrophic growth conditions (Vargas et and physiological and biochemical properties (Huber and al. 1998), and was found to grow chemolithoautotrophically 114 AMO, PAJE, INAGAKI, EZAKI, ATOMI AND IMANAKA with hydrogen, carbon dioxide and elemental sulfur (Huber et Na2SO4; 10 mg KCl; 2.5 mg MnSO4·5H2O; 0.8 mg al. 1987). Pyrobaculum aerophilum is a marine facultative ZnSO4·7H2O; 0.4 mg CuSO4·5H2O; 0.3 mg Na2SO3; and microaerobe that can grow aerobically at oxygen concentra- 0.2 mg CoCl2·6H2O. The pH of the enrichment medium was tions up to 5% (v/v) in the gas phase (Völkl et al. 1993), anaer- adjusted to 7.0 with NaOH at room temperature before obically by dissimilatory nitrate or nitrite reduction (Völkl et autoclaving. The enrichment was performed in test tubes al. 1993), and chemolithoautotrophically with hydrogen or (180 mm × 18 mm; Iwaki, Tokyo, Japan) with silicone plugs thiosulfate as electron donors coupled with the reduction of (Top, Kyoto, Japan) containing 10 ml of medium and incu- oxygen or nitrate (Völkl et al. 1993). Pyrobaculum arsen- bated at 85 °C in atmospheric air without shaking. For isola- aticum is a strict anaerobe, growing chemolithoautotroph- tion, the enrichment medium was solidified with 0.8% Gelrite ically with carbon dioxide as carbon source, hydrogen as in slanted media bottles (Iwaki). The medium was supple- electron donor, and arsenate, thiosulfate or elemental sulfur as mented with 5 mM MgSO4 and 1.25 mM CaCl2 for solidifica- the electron acceptor (Huber et al. 2000). Pyrobaculum arsen- tion of the medium. After applying the samples, the slants aticum can also grow organotrophically in the presence of an were incubated at 85 °C. inorganic electron acceptor such as sulfur, selenate or arsenate (Huber et al. 2000). Pyrobaculum oguniense is a facultative Growth experiments with strain VA1 aerobe, growing aerobically and microaerobically with oxy- Unless otherwise stated, routine liquid cultivations were per- gen as an electron acceptor (Sako et al. 2001). Under aerobic formed in medium containing 10 g of tryptone and 1.0 g of conditions, growth is inhibited by elemental sulfur, but under yeast extract per liter of deionized water (TY medium) at anaerobic conditions, elemental sulfur, thiosulfate, L-cystine 90 °C in an appropriate gas phase. Aerobic cultures in atmo- and oxidized glutathione can be utilized as electron acceptors spheric air were performed in 100 or 1000 ml media bottles (Sako et al. 2001). (Iwaki) with silicone plugs (Top) containing 50 or 200 ml of Here, we report the isolation and characterization of a novel medium, respectively, without shaking, or in 500-ml shaking facultatively aerobic, hyperthermophilic archaeon that dis- flasks (Iwaki) with silicone plugs (Top) containing 200 ml of plays vigorous growth in atmospheric air. medium with vigorous shaking (120 rpm). Anaerobic culture conditions were maintained as described by Balch et al. (1979). Vial bottles (20 ml volume, Maruemu, Osaka, Japan) Materials and methods containing 10 ml medium were autoclaved and transferred to an anaerobic chamber (Tabai Espec, Osaka, Japan) filled with Strains an anoxic gas mixture (N2:CO2:H2, 90:5:5). In the chamber, T Pyrobaculum aerophilum JCM 9630 , P.organotrophum JCM trace oxygen was reduced by adding 0.5 mM Na2S and then T T 9190 and Thermoproteus tenax JCM 9277 were purchased the bottle was sealed with a butyl rubber stopper (Maruemu) from the Japan Collection of Microorganisms (JCM; Wako, and an aluminum cap (Maruemu). Resazurin (1 mg l–1)was T Japan). Pyrobaculum islandicum DSM 4184 was a gift from used as a redox indicator. Microaerobic growth conditions Prof. Toshihisa Ohshima (Tokushima University, Tokushima, were obtained by omitting the addition of Na2S. The presence T T Japan). Pyrobaculum oguniense TE7 (= JCM 10595 )was of oxygen was confirmed by the color of resazurin. kindly provided by Prof. Yoshihiko Sako (Kyoto University, Kyoto, Japan). Light and electron microscopy Cells were observed with an Eclipse E800 light microscope Collection of samples (Nikon, Tokyo, Japan) with immersion oil. For scanning elec- Water and mud samples were collected from various hot tron microscopic observation, samples were prepared as fol- springs in Los Baños and Calamba, Laguna, the Philippines. A lows. Diluted cultures were applied to thin glass coated with hyperthermophilic archaeon, Caldivirga maquilingensis,was poly-L-lysine (Sigma, St. Louis, MO). Cells were fixed with previously isolated from this field (Itoh et al. 1999). The in situ 2.5% glutaraldehyde solution in potassium phosphate buffer temperatures ranged from 45 to 85 °C. Mud samples were (pH 7.2) and washed five times with the potassium phosphate acidic (pH 1.8 to 3.2) and water samples were near neutral buffer. Samples
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