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Hyperthermophilic Microorganisms FEMS Microbiology Reviews 75 (1990) 117-124 Published by Elsevier FEMSRE 00133 Hyperthermophilic microorganisms K.O. Steuer, G. Fiala, G. Huber, R. Huber and A. Segerer Lehrstuhl für Mikrobiologie, Universität Regensburg, Regensburg, F.R.G. Key words: Hyperthermophiles; Taxonomy 1. INTRODUCTION 7 to 9) rich in NaCl. Also man-made hot environ• ments such as the boiling outflows of geothermal The most extremely thermophilic living beings power plants are suitable environments for hyper• known to date are bacteria growing at tempera• thermophiles [9]. Submarine hydrothermal systems tures between 80 and 110 °C [1-3]. Some of them are slightly acidic to alkaline (pH 5 to 8.5) and are so well adapted to the high temperatures that normally contain high amounts of NaCl and SO4 ~ they do not even grow below 80 ° C [4]. As a rule, due to the presence of sea water (Table 1). Due to non of these hyperthermophilic bacteria are able the low solubility of oxygen at high temperatures to grow at 60 ° C or below. Hyperthermophiles are and the presence of reducing gases, most biotopes occurring mainly within the archaebacterial king• of hyperthermophiles are anaerobic. Within con• dom [5]; some of them are also present within the tinental solfataric fields, oxygen is only present eubacteria [6,7]. Due to their existence within within the upper acidic layer which appears phylogenetically highly divergent groups, the lack ochre-coloured due to the existence of ferric iron of closely related mesophiles, and their biotopes [8]. existing already since the Archean age, hyperther• Although not growing below 60 °C, hyperther• mophiles may have adapted to the hot environ• mophiles are able to survive at low temperatures ment already billions of years ago. at least for years. Some of the anaerobic hyper• thermophiles are able to tolerate oxygen much better at low (non-growth) temperatures than at 2. BIOTOPES high (growth) temperatures. This property may be essential for dispersal of these organisms through The hyperthermophilic bacteria known at pre• oxygen-rich low-temperature areas. sent have been isolated from submarine hydro- thermal areas and from continental solfataras. The surface of the solfataras is usually rich in sulfate 3. TAXONOMY OF HYPERTHERMOPHILIC and exhibits an acidic pH (0.5 to 6; [1,2]). In the BACTERIA depth, solfataras are less acidic or even neutral Up to now, about 35 different species of hyper• (pH 5 to 7; [8]). Sometimes, solfataric fields may thermophilic bacteria are known. They belong to also contain some weakly alkaline hot springs (pH different taxa within the eu- and archaebacteria (Table 2). Within the eubacteria, hyperthermo• philes are within the Thermotogales order, which Correspondence to: K.O. Steuer, Lehrstuhl für Mikrobiologie, is the deepest phylogenetic branch-off based on Institute for Biochemistry, Genetics and Microbiology, Univer• sity of Regensburg, Universitätsstr. 31, P.O. Box 397, D-8400 16S rRNA sequences within this kingdom [7]. The Regensburg, F.R.G. phylogenetic tree within the archaebacterial king- 0168-6445/90/S03.50 © 1990 Federation of European Microbiological Societies dorn exhibits two main branches: the branch con• S° and S2", forming sulfuric acid (Table 3, 4). taining methanogens and halophiles and the Many Sulfolobus isolates are facultative hetero- branch of the sulfur metabolizing archaebacteria trophs and a few, still unnamed, are even strict [7]. The latter consists almost exclusively of hyper• heterotrophs (Stetter, unpublished). The type thermophiles [3,7] while there are only a few groups strain of Sulfolobus acidocaldarius (DSM 639) of hyperthermophiles within the other branch shows excellent growth on organic matter [11]. (Archaeoglobales, Thermococcales, Methano- Autotrophically cultured on S2~ and S°, however, thermaceae, Mc. jannaschii). Within the sulfur this strain shows only extremely weak growth and metabolizers, acidophilic (e.g. Sulfolobus, Metal- sulfuric acid formation [12-14]. Some members of losphaera, Acidianus) and neutrophilic (e.g. Pyro- the Sulfolobales like Metallosphaera sedula are dictium, Desulfurococcus, Staphylothermus, Ther- able to oxidize sulfidic ores like pyrite, chal- mococcus) genera were discovered during the last copyrite and sphalerite, forming sulfuric acid and years. Therefore, the old designation "Thermo- solubilizing the heavy metal ions (Table 3,4; [15]). acidophiles" which was primarily used to char• Under microaerophilic conditions, Sulfolobus is acterize the genera Sulfolobus and Thermoplasma able to reduce ferric iron and molybdate, which [1] is not suitable anymore for the designation of therefore act as electron acceptors under these this branch. conditions [16,17]. Members of the genus Sulfolo• bus grow only at very low ionic strength and were 3.1. Extremely acidophilic hyperthermophiles therefore not found within the marine environ• Extremely acidophilic hyperthermophiles were ment ([11]; Segerer and Stetter, unpublished). found up to now exclusively within continental Members of the genus Acidianus similar to solfataric fields. The organisms are coccoid-shaped Sulfolobus are able to grow by oxidation of S°, strict and facultative aerobes. They are extreme forming sulfuric acid [18,19]. Some strains grow acidophiles due to their requirement of acidic pH also on sulfidic ores, but much less efficient than (opt. approx. pH 3). Phylogenetically, they belong Metallosphaera (Table 4; [14]). In addition, mem• to the archaebacterial genera Sulfolobus, Metal- bers of Acidianus are able to grow by anaerobic losphaera, Acidianus, and Desulfurolobus. The less oxidation of H2, using S° as electron donor (Table extremely thermophilic archaebacterium Thermo• 4; [18]). A thermoacidophilic isolate, which had plasma is an extreme acidophile, too. It is a facul• been tentatively named "Sulfolobus ambiualens" tative anaerobe occurring both in smoldering coal [20] was later described as Desulfurolobus am- refuse piles and continental solfataric fields [1,10]. bivafens, representing a new genus [21]. By Members of the genus Sulfolobus are strict DNA : DNA hybridization, however, Desulfurolo• aerobes growing autotrophically by oxidation of bus ambivalens shows a close relationship to the Table 1 Biotopes of hyperthermophilic bacteria Characteristics Type of thermal area Solfataric fields Submarine hydrothermal systems Sites Steam-heated mud holes. Hot sediments and vents soils and surface waters; deep hot springs; geo- thermal power plants Temperatures Up to 100°C Up to about 374 °C pH 0.5 to 9 5 to 8.5 Presence of 02 Surface oxic; depth anoxic Anoxic 2_ + 2 Major gases and C02, CO, CH4, S04 , NH4 H2, H2S,S°,S03 - sulfur compounds 3.2. Slightly acidophilic and neutrophilic hyperther• Taxonomy of hyperthermophilic archaebäcteria mophiles Order Genus Species Slightly acidophilic and neutrophilic hyperther• mophiles were found both in continental solfataric I. Eubacteria! kingdom Thermotogales Thermotoga T. maritima fields and in submarine hydrothermal systems and T. neapolitana they show specific adaptations to their environ• T. thermarum ments. All of them are strict anaerobes. Solfataric Thermosipho 8 T. africanus fields contain members of the genera Thermopro• 8 Fervidobacterium F. nodosum teus, Pyrobaculum, Thermofilum, Desulfurococcus, F. islandicum and Methanothermus (Table 3; [9,23-26]). Cells of II. Archaebacterial kingdom members of the genera Thermoproteus, Pyrobacu• Sulfolobales Sulfolobus S. acidocaldarius lum, and Thermofilum are characteristically stiff S. solfataricus rods with protruding spheres ("golf clubs") mainly Metallosphaera M. sedula Acidianus A. infernus at their ends, possibly due to a mode of budding. A. brierleyi 8 Cells of Thermofilum are only about 0.17 to 0.35 Desulfurolobus D. ambiualens /im in width and are therefore different from Thermoproteales Thermoproteus T. tenax Thermoproteus and Pyrobaculum. Thermoproteus T. neutrophifus tenax, Thermoproteus neutrophilus and Pyrobacu• Pyrobaculum P. islandicum P. organotrophum lum islandicum are able to grow autotrophically by Thermofilum T. pendens anaerobic reduction of S° with H2 as electron T. librum donor [9,27]. Strains of Thermofilum and Pyro• Desulfurococcus D. mobilis baculum organotrophum are obligate heterotrophs. D. mucosus They are growing by sulfur respiration, using dif• D. saccharovorans Staphylothermus • S. marinus ferent organic substrates (Table 4). Thermofilum Pyrodictialcs Pyrodictium P. occultum pendens shows an obligate requirement for a lipid P. brockii fraction of Thermoproteus tenax. Thermoproteus P. abyssum tenax and Pyrobaculum islandicum are also able to Tliermodiscus T. maritimus grow heterotrophically by sulfur respiration (Ta• Thermococcales Thermococcus T. celer T. stetteri ble 4). Also in solfataric fields coccoid hetero• Fyrococcus P. furiosus trophic organisms occur which gain energy by P. woésii respiring organic material using sulfur as electron Archaeoglobales Archaeoglobus A. fulgidus acceptor. They belong to the genus Desulfurococ• A. profundus cus [25]. From solfataras in the southwest of Ice• Thermoplasmales 8 Thermoplasma T. acidophilum land, rod-shaped methanogens growing at temper• T. volcanium Methanobacteriales b Methanothermus M. fervidus atures up to 97 °C (Table 3) were isolated [26,28]. M. sociabilis Two species are known: Methanothermus fervidus Methanococcales Methanococcus b M. thermolitho- and Methanothermus sociabilis, cells of the latter 8 trap hi cus growing in clusters up to 3 mm. Both species are M. jannaschii strict
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