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Ferroplasma Acidiphilum Gen. Nov., Sp. Nov., an Acidophilic, Autotrophic, Ferrous-Iron-Oxidizing, Cell-Wall-Lacking, Mesophilic Member of the Ferroplasmaceae Fam

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Ferroplasma Acidiphilum Gen. Nov., Sp. Nov., an Acidophilic, Autotrophic, Ferrous-Iron-Oxidizing, Cell-Wall-Lacking, Mesophilic Member of the Ferroplasmaceae Fam International Journal of Systematic and Evolutionary Microbiology (2000), 50, 997–1006 Printed in Great Britain Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea Olga V. Golyshina,1,2 Tatiana A. Pivovarova,2 Grigory I. Karavaiko,2 Tamara F. Kondrat’eva,2 Edward R. B. Moore,1 Wolf-Rainer Abraham,1 Heinrich Lu$ nsdorf,1 Kenneth N. Timmis,1 Michail M. Yakimov1 and Peter N. Golyshin1 Author for correspondence: Peter N. Golyshin. Tel: j49 531 6181498. Fax: j49 531 6181411. e-mail: pgo!GBF.de 1 Division of Microbiology, An isolate of an acidophilic archaeon, strain YT, was obtained from a GBF National Research bioleaching pilot plant. The organism oxidizes ferrous iron as the sole energy Centre for Biotechnology, Mascheroder Weg 1, source and fixes inorganic carbon as the sole carbon source. The optimal pH for 38124 Braunschweig, growth is 17, although growth is observed in the range pH 13to22. The cells Germany are pleomorphic and without a cell wall. 16S rRNA gene sequence analysis 2 Institute of Microbiology, showed this strain to cluster phylogenetically within the order Russian Academy of ‘Thermoplasmales ’ sensu Woese, although with only 899 and 872% sequence Sciences, Prosp. 60-letiya Oktyabrya, Moscow, Russia identity, respectively, to its closest relatives, Picrophilus oshimae and Thermoplasma acidophilum. Other principal differences from described species of the ‘Thermoplasmales ’ are autotrophy (strain YT is obligately autotrophic), the absence of lipid components typical of the ‘Thermoplasmales ’ (no detectable tetraethers) and a lower temperature range for growth (growth of strain YT occurs between 15 and 45 SC). None of the sugars, amino acids, organic acids or other organic compounds tested was utilized as a carbon source. On the basis of the information described above, the name Ferroplasma acidiphilum gen. nov., sp. nov. is proposed for strain YT within a new family, the Ferroplasmaceae fam. nov. Strain YT is the type and only strain of F. acidiphilum. This is the first report of an autotrophic, ferrous-iron- oxidizing, cell-wall-lacking archaeon. Keywords: Archaea,‘Thermoplasmales’, acidophilic, chemolithoautotrophic, ferrous- iron-oxidizing INTRODUCTION proposed (Woese, 1987; Woese et al., 1990; Segerer & Stetter, 1992b), but has not been validly published, and Acidophilic aerobic or facultatively anaerobic Archaea the order Sulfolobales (Segerer & Stetter, 1992a). These that colonize biotopes such as pyrite ores, solfatara groups of acidophiles differ with respect to their fields etc., where sulfur and iron are typically in phenotypic properties; first of all, with respect to the reduced forms, generally represent two different phylo- carbon and energy sources utilized. Some repre- genetic groups of the Archaea, the order ‘Thermo- sentatives of the Sulfolobales, e.g. Acidianus brierleyi plasmatales’or‘Thermoplasmales’, which has been (Segerer & Stetter, 1992a), members of the genus ................................................................................................................................................. Metallosphaera (Fuchs et al., 1995; Huber et al., 1989) Abbreviations: CID, collision-induced dissociation; FAB, fast-atom bom- and Sulfolobus hakonensis (Takayanagi et al., 1996), bardment; MS, mass spectrometry. obtain energy by oxidizing sulfur, sulfide minerals and The EMBL accession number for the 16S rRNA gene sequence of Ferro- ferrous iron. Other species of the genus Sulfolobus, e.g. plasma acidiphilum strain YT is AJ224936. Sulfolobus acidocaldarius (Brock et al., 1972) and 01229 # 2000 IUMS 997 O. V. Golyshina and others Sulfolobus solfataricus (Brierley & Brierley, 1973), Anaerobic growth was assayed in closed vessels with or utilize sulfur and reduced sulfur compounds. Sul- without FeSO% in the presence of acetic acid (0n2%). The folobus metallicus (Huber & Stetter, 1991) exploits atmosphere consisted of 180 kPa CO# with or without the sulfidic ores, such as pyrite, sphalerite and chalco- addition of 40 kPa H#. Growth was monitored by the determination of the protein content of the culture using the pyrite, and elemental sulfur as energy sources. Al- # $ Bio-Rad protein assay. The concentrations of Fe + and Fe + though other members of the Sulfolobales are able to were determined by trilonometric titration (Reznikov et al., grow chemolithoautotrophically, S. metallicus (Huber 1970). Elemental sulfur and minerals containing reduced & Stetter, 1991) and Acidianus ambivalens (Fuchs et sulfur, Fe#S, ZnS, PbS and Sb#S$, were sterilized by al., 1996) are the only obligately chemolithoauto- autoclaving and added to the medium. trophic species known. In contrast, species of both Antibiotic-sensitivity analysis. The sensitivity of strain YT to genera of the order ‘Thermoplasmales’ described to antibiotics was determined by their addition in controlled date, Thermoplasma (Darland et al., 1970; Segerer et concentrations into cultures that had been pre-grown for al., 1988; Segerer & Stetter, 1992b) and Picrophilus one generation in the medium outlined above. (Schleper et al., 1995, 1996), are heterotrophic archaea that probably consume the decomposition products of Growth on organic substrates. The following organic com- the primary producers in solfatara fields and coal pounds were tested as possible substrates at concentrations of 0n1–0n2%, with or without the addition of FeSO%. Growth refuse piles, such as species of the genera Acidianus, was estimated, as described above, after incubation for 48 h. Thiobacillus and Sulfolobus. Sugars and related compounds: -arabinose, fructose, su- Here, we report the isolation, phylogenetic character- crose, -sorbitol, - and -glucose, glucose 1-phosphate, ization and phenotypic characteristics of strain YT, glucose 6-phosphate, -maltose, -xylose, -mannitol, lac- isolated from a pyrite-leaching pilot plant and repre- tose, cellobiose, -galactose, mannose, -fucose, gentio- biose, m-inositol, lactulose, -melibiose, β-methyl -gluco- senting a hitherto undescribed species of a new genus side, -psicose, raffinose, -rhamnose, -sorbitol, -trehal- that represents a new family within the order ‘Thermo- T ose, turanose, xylitol, cyclodextrin, dextrin, inosine, uridine, plasmales’. Strain Y represents the only strictly thymidine and glycogen. Organic acids and their salts: autotrophic, cell-wall-deficient archaeon described to aminobutyric acid, methyl pyruvate, monomethyl succinate, date. In recognition of its ability to oxidize ferrous iron acetic acid, cis-acetic acid, citric acid, formic acid, - and the absence of a distinct cell wall, together with the galactonic acid lactone, -galacturonic acid, -gluconic acid, acidic origin of isolation, the name Ferroplasma -glucosaminic acid, -glucuronic acid, α-hydroxybutyric acidiphilum gen. nov., sp. nov., within the family acid, β-hydroxybutyric acid, γ-hydroxybutyric acid, p-hy- Ferroplasmaceae fam. nov., is proposed, and strain YT droxyphenylacetic acid, itaconic acid, α-ketobutyric acid, α- ( DSM 12658T) is designated as the type strain. ketoglutaric acid, α-ketovaleric acid, -lactic acid, malonic l acid, propionic acid, quinic acid, -saccharic acid, sebacic acid, succinic acid, bromosuccinic acid, succinamic acid, METHODS urocanic acid and -pyroglutamic acid. Amino acids: glu- T curiamide, alaninamide, -alanine, -alanyl-glycine, -as- Isolation. Strain Y was isolated by serial dilution of the paragine, -aspartic acid, -glutamic acid, glycyl--aspartic aqueous phase of a bioreactor of a pilot plant (Tula, Russia), acid, glycyl--glutamic acid, -histidine, hydroxy--proline, which was bioleaching a gold-containing arsenopyrite\ -leucine, -ornithine, -phenylalanine, -proline, -serine, pyrite ore concentrate from Bakyrtchik (Kazakhstan), in a -serine, -threonine, -carnitine, putrescine and phenyl- modified 9K medium (see below). The temperature of the ethylamine. Alcohols: 2-aminoethanol, 2,3-butanediol, isolation source was 28–30 mC and the pH was 1n6–1n9. The glycerol, -α-glycerol phosphate, adonitol, -arabitol and purity of the culture and the absence of associated micro- i-erythritol. Others: Tweens 40 and 80, N-acetyl -galacto- organisms were controlled directly by phase-contrast mi- samine and N-acetyl -glucosamine. croscopy as well as by inoculation of heterotrophic liquid media. The purity of the culture was also estimated by (i) the Electron microscopy. Vegetative cells were fixed in 2n5% inability to obtain any bacterial PCR amplicons and (ii) the glutaraldehyde solution and absorbed to Formvar-coated homogeneity of sequences of PCR amplicons obtained by copper grids (300 square mesh) for 20–90 s, depending on using Archaea-specific oligonucleotide primers. the cell density, blotted with filter paper and air-dried. T Samples were shadowed unidirectionally with Pt\Cat15m Growth conditions. If not stated otherwise, strain Y was angle of elevation and a final thickness of 4 nm in an MED cultivated in 250 ml flasks with 100 ml modified medium " 020 evaporation unit (Baltec). Negative staining, embedding 9K (Silverman & Lundgren, 1959) containing (l− ): 04g n and ultrathin sectioning were done according to methods MgSO .7H O, 0 2 g (NH ) SO ,01 g KCl, 0 1g KHPO % # n % # % n n # % described previously (Yakimov et al., 1998). and 25 g FeSO%.7H#O. The medium was supplemented with 0n02% yeast extract (Difco) and trace elements, as described Incorporation of labelled CO2.
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