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1 Winogradsky-Institute of Microbiology, Russian Academy of Sciences, Prospekt 60-letiya Oktyabrya 7/2, Moscow, 117811 Russia
2 Moscow State University, Biological Faculty, Department of Microbiology, Vorob'evy Gory, Moscow, 119992 Russia
Correspondence
Grigorii I. Karavaiko
gregor{at}inmi.host.ru
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-alicyclic fatty acids) and the major isoprenoid quinone (menaquinone MK-7) of strain K1, supported the affiliation of strains K1 and SD-11T to the genus Alicyclobacillus. Physiological and molecular biological tests allowed genotypic and phenotypic differentiation of strains K1 and SD-11T from the nine Alicyclobacillus species with validly published names. The G+C content of the DNA of strain K1 was 48·7±0·6 mol%; that of strain SD-11T was 53±1 mol%. DNA–DNA reassociation studies showed low relatedness (22 %) between strains K1 and SD-11T, and even lower relatedness (3–5 %) between these strains and Alicyclobacillus acidocaldarius subsp. acidocaldarius ATCC 27009T, DSM 446T. DNA reassociation of strains K1 and SD-11T with Alicyclobacillus cycloheptanicus DSM 4006T gave values of 15 and 21, respectively. Based on the phenotypic and phylogenetic characteristics of strains K1 and SD-11T, Alicyclobacillus tolerans sp. nov. (type strain, K1T=VKM B-2304T=DSM 16297T) and Alicyclobacillus disulfidooxidans comb. nov. (type strain, SD-11T=ATCC 51911T=DSM 12064T) are proposed.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Alicyclobacillus tolerans K1T is AF137502.
Graphs showing the growth of and oxidation of ferrous iron and glucose consumption by strains VKM B-1269T and K1T, and tables listing the DNA base compositions of various sulfobacilli and alicyclobacilli and the 14CO2 fixation by cell suspensions of strain K1T are available as supplementary material in IJSEM Online.
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). However, the assignment of the strain to a subspecies of S. thermosulfidooxidans was questionable as its genotypic and chemotaxonomic characteristics were not studied. A comparative analysis of the number and size of restriction fragments generated from the chromosomal DNA of strain K1 and of the type strain of S. thermosulfidooxidans (VKM B-1269T=DSM 9293T) attested to the lack of intraspecies similarity between the two strains (Kondrat'eva et al., 1998). In addition, phylogenetic analysis based on partial 16S rRNA gene sequencing (500 bp) showed that strain K1 was more closely related to the genus Alicyclobacillus than to the genus Sulfobacillus (Karavaiko et al., 2000). Strain SD-11T was isolated from a mixed culture obtained after enrichment of waste water sludge of Blake Lake City, Quebec, Canada (Dufresne et al., 1993). On the basis of its ability to use elemental sulfur and pyrite as sole energy sources, the strain was described as the type strain of Sulfobacillus disulfidooxidans (Dufresne et al., 1996). Strain SD-11T is phylogenetically related to strain K1 (Karavaiko et al., 2000) and to Alicyclobacillus cycloheptanicus DSM 4006T (Dufresne et al., 1996); 16S rRNA gene sequence similarity values were 92·6 and 95·5 %, respectively. Phenotypically, strains of the genus Alicyclobacillus are spore-forming, thermoacidophilic, Gram-positive bacteria. In common with most alicyclobacilli, strains K1 and SD-11T contained -alicyclic fatty acids as the major cell-membrane lipid component (Tsaplina et al., 1994; Dufresne et al., 1996). In this report, we propose the classification of ‘S. thermosulfidooxidans subsp. thermotolerans’ strain K1 as the type strain (K1T) of Alicyclobacillus tolerans sp. nov. and the reclassification of S. disulfidooxidans as Alicyclobacillus disulfidooxidans comb. nov.
For experiments, strain K1T was grown at 40 °C on modified Manning medium (Manning, 1975) containing 50–70 mM Fe2+, 0·2 g yeast extract l–1 and mineral salts [g l–1: (NH4)2SO4, 6·0; KCl, 0·2; K2HPO4, 0·2; MgSO4.7H2O, 1·0; Ca(NO3)2.7H2O, 0·1; pH 2·5–2·7]. There was no growth on the BAM agar of Deinhard et al. (1987a). Strain K1T grew organotrophically in liquid and solid modified BAM that contained less yeast extract and glucose (to 0·2 and 0·5 g l–1, respectively).
The preliminary screening for 16S rRNA gene sequences similar to that of strain K1T was carried out by using BLAST (http://www.ncbi.nlm.nih.gov/blast). Then, the 16S rRNA gene sequence of strain K1T was aligned with a representative set of 16S rRNA gene sequences obtained from recent GenBank releases by using CLUSTAL W. Positions of sequence and alignment uncertainties were omitted; in total 1308 nucleotides were used in the analysis. Phylogenetic trees were constructed by using various algorithms implemented in TREECON (Van de Peer & De Wachter, 1994). The almost-complete 16S rRNA gene sequence of strain K1T (1409 bp) was used in the analyses, corresponding to positions 15 to 1435 of Escherichia coli numbering. The comparative phylogenetic analysis showed that strain K1T clustered with species of the genus Alicyclobacillus. However, in this cluster, the similarity levels between the 16S rRNA gene sequence of strain K1T and those of strains (including the type strains) of species of the genus Alicyclobacillus with validly published names did not exceed 94·5 %. Therefore, according to current concepts (Stackebrandt & Goebel, 1994), strain K1T could not be assigned to any known species of the genus Alicyclobacillus. The 16S rRNA gene sequence of strain K1T also showed a high degree of similarity to sequences of the following unidentified strains that have been tentatively assigned to the genus Alicyclobacillus (Fig. 1): Alicyclobacillus sp. AGC-2 (99·6 %); two strains of halophilic, acidophilic, iron-oxidizing bacteria, Alicyclobacillus sp. 5C (98·9 %) and Alicyclobacillus sp. CLG (98·6 %); and bacterium GSM (99·1 %), a moderately thermophilic strain that oxidizes elemental sulfur and pyrite (in the presence organic C) and is capable of oxidizing and reducing iron (Johnson et al., 2001a, 2003; A. Yahya, K. B. Hallberg & D. B. Johnson, unpublished data). Within the genus Alicyclobacillus, these unclassified strains formed a separate phylogenetic cluster with an intraspecies similarity level of 98·6–99·6 %. Based on the results of the phylogenetic analysis, it may be concluded that strain K1T, together with several as-yet-unclassified strains, composes a new species of the genus Alicyclobacillus. The 16S rRNA gene sequences of strains K1T and SD-11T exhibited a low level of similarity (83·3–87·7 %) to the sequences of strains belonging to the genus Sulfobacillus and a high level of similarity (92·2–95·5 %) to the sequences of strains belonging to the genus Alicyclobacillus (Dufresne et al., 1996; Karavaiko et al., 2000).
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the main phenotypic and genomic properties of strains K1T and SD-11T and alicyclobacilli are compared.
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; Karavaiko et al., 2000; Goto et al., 2003). The G+C content of the DNA of strain K1T, determined by the methods of Marmur (1961) and Owen et al. (1969), and that of bacterium GSM were 48·7±0·6 and 50·5 mol% (Johnson et al., 2001a), respectively, i.e. less than the minimum G+C values determined for identified alicyclobacilli (Table 1
). The G+C content of the DNA of strain SD-11T was 52·7 mol% (our data) and 53±1 mol% (Dufresne et al., 1996) and close to the value for Alicyclobacillus acidoterrestris DSM 3922T (52·2 mol%) (Wisotzkey et al., 1992). DNA–DNA hybridization was performed by using the optical reassociation method (De Ley et al., 1970). The results confirmed the interspecies level of relatedness between strain K1T and the tested sulfobacilli strains (S. thermosulfidooxidans, Sulfobacillus acidophilus and ‘Sulfobacillus sibiricus’) and a very low reassociation level (3–5 %) between strains K1T and SD-11T and A. acidocaldarius subsp. acidocaldarius ATCC 27009T, DSM 446T grown on medium described by Darland & Brock (1971) at 63 °C and pH 3·5 (see Table A, available as supplementary material in IJSEM Online). Higher levels of DNA reassociation were determined for strains K1T and SD-11T with A. cycloheptanicus DSM 4006T (15 and 21 %, respectively).
The membrane lipid composition of cells of strain K1T organotrophically grown in liquid modified BAM medium and in liquid modified Manning medium (with Fe2+/FeS2) was determined after acid methanolysis. To 10 mg of a cell pellet dried in a nitrogen flow was added 400 µl of absolute methanol containing 2·6 M HCl for 4 h at 70 °C. Methyl esters of fatty acids and dimethylacetals, formed as a result of methanolysis, were twice extracted with 100 µl hexane, dried, and treated with 30 µl N,O-bis(trimethylsilyl)-trifluoroacetamide for 15 min at 80 °C to obtain trimethylsilyl esters of hydroxyl acids. The obtained mixture (2–5 µl) was fed into the injector of an HP-5973 gas chromatograph mass spectrometer (Hewlett Packard). Regular software supplied with a quadruple mass-analyser was used for control of the apparatus and data processing. The mass spectrometer used electrons with energy of 70 eV for ionization and had a resolution of 0·5 amu and a working mass range of 2–100 amu; the sensitivity threshold was 0·01 ng of methylstearate. Chromatographic separation of the mixture was performed on an HP-5ms methyl silica capillary column (Hewlett Packard) (30 m; inner diameter, 0·2 mm, coated with immobile methylsilicone, 0·2 µm – width phase). Helium, the carrier gas, passed through the column at a flow rate of 1·5 ml min–1. The initial temperature was set at 120 °C for 2 min and then increased to 300 °C at a rate of 5 °C min–1. Separated substances were identified on known features of their mass spectra and relative retention times using the mass-spectral databases nbs75k and wiley275. Simple -cyclohexane acids were also identified from the published data (Oshima & Ariga, 1975) and oxyacids by specific fragmentation of Me-TMS derivatives (methyl-O-trimethylsilyl derivatives) and methyl esters (without silylation). It was shown that strain K1T differed only slightly from A. acidocaldarius, A. acidoterrestris, Alicyclobacillus acidiphilus, Alicyclobacillus sendaiensis, Alicyclobacillus hesperidum (Wisotzkey et al., 1992; Goto et al., 2003; Matsubara et al., 2002; Tsuruoka et al., 2003; Albuquerque et al., 2000), S. disulfidooxidans (Dufresne et al., 1996) and strains of S. thermosulfidooxidans (Tsaplina et al., 1994). All these strains contained -alicyclic (cyclohexanoic) fatty acids as the major lipid component. Under heterotrophic conditions, the percentage of particular -alicyclic acids in the total fatty acid content of strain K1T comprised: -cyclohexane-C17 : 0, from 27·5 (under auototrophic conditions) to 60 %; -cyclohexane-C19 : 0, from 2·1 (under mixotrophic conditions) to 7·9 %; -cyclohexane-C17 : 0 2OH (never before revealed in alicyclobacilli), from 8·2 (under autotrophic and mixotrophic conditions) to 11·3 %; and -cyclohexane-C18 : 0, from 0·7 (under mixotrophic conditions) to 1·2 %. When grown organotrophically, strain K1T could be differentiated from other species of the genus Alicyclobacillus by the amounts of -cyclohexane-C17 : 0 (60·0 %) and -cyclohexane-C19 : 0 (7·9 %) present: values for A. acidocaldarius were 47·6–52·8 % and 25·2–42·6 %, respectively; values for strains of A. acidoterrestris were 62·6–68·4 % and 18·9–23·9 %, respectively (Goto et al., 2003); values for A. hesperidum were 56·8 and 13·3 %, respectively; and values for A. sendaiensis were 44·1 and 30·2 %, respectively.
The main isoprenoid quinone in strain K1T, as determined by the method of Collins (1985), was menaquinone with seven isoprene units, MK-7 (90 % from common sum), while MK-6 was a minor component. Standard mixtures of menaquinones were used for identification purposes.
Morphologically, strains K1T and SD-11T differed from species of Alicyclobacillus and Sulfobacillus by a slightly larger cell size [3·0–6·0x0·9–1·0 µm (K1T) and 1·0–6·0x0·6–1·0 µm (SD-11T)], the lack of flagella and the thermal resistance of their spores (remain viable after 30 min heating at 110 °C) (Kovalenko & Malakhova, 1983; Bogdanova et al., 1990). The cell wall consists of a thin murein layer (50–60 Å in thickness); cells exhibited a surface S-layer comprising large hexagonally packed (p6-symmetry) rod-shaped subunits of 150–160 Å in diameter and 180–200 Å in height (unpublished data). On a solid medium containing 0·5 % (w/v) agarose, strain K1T grew slowly: small colonies of 0·3–0·5 mm in diameter were observed after 7–10 days incubation.
Strain K1T grew optimally at 37–42 °C, differing from the known thermophilic bacteria of the genus Alicyclobacillus, which are characterized by optimal growth at 42–60 °C and an inability to grow at 25 °C (Wisotzkey et al., 1992; Goto et al., 2003) with the exception of A. acidiphilus DSM 14558T (Matsubara et al., 2002). Bacterium GSM has optimal growth at 46 °C and does not grow below 35 °C (Johnson et al., 2001a). Strain SD-11T is a mesophile with optimal growth at 35 °C (Dufresne et al., 1993, 1996); however, authors have observed spore germination at 4 °C for this strain and regard this temperature as the lower growth limit. Strain K1T grew between pH 1·5 and 5·0, with the optimum at pH 2·5–2·7, while the alicyclobacilli with validly published names grew in the range pH 2·0–6·5, with the optimum at pH 3·0–5·5. Growth of strain SD-11T was optimal at pH 1·5–2·5 (Table 1).
Physiological characteristics of strain K1T studied with the use of the API 50 CH system (BioMérieux), described by Deinhard et al. (1987a, b) for the biochemical profiling of Alicyclobacillus species, are compared with the respective data reported for several species of sulfobacilli and alicyclobacilli (Table 1). The growth of strain K1T and acidification of the medium were monitored every 2 days for 10 days. All tests were repeated in triplicate. Compared with S. thermosulfidooxidans VKM B-1269T, strain K1T utilized a greater number of organic substrates (Tsaplina et al., 1991) and accumulated 1·5–2 times greater biomass (up to 20 mg protein l–1, as determined by the Lowry method). Mannose, ribose, fructose, galactose, sucrose, trehalose, starch, glycine, cysteine, aspartic acid and glutamic acid could support rapid growth. Mannitol, glucose, xylose, sorbose, melezitose, amygdalin, methyl 
-D-glucoside, aesculin and glycogen could support slower growth. Weak growth was observed on glycerol, lactose, raffinose, turanose, arabinose and maltose. Acidification of the medium did not exceed 0·2 of a pH unit. All other carbohydrates tested did not support growth. Strain K1T and all other strains except Alicyclobacillus herbarius do not reduce nitrate to nitrite. Alicyclobacillus pomorum and A. cycloheptanicus were oxidase-positive; strain K1T was weakly oxidase-positive. A. pomorum was catalase-positive; strain K1T was weakly catalase-positive. Gelatin was hydrolysed by A. acidiphilus, A. cycloheptanicus and A. herbarius. Starch was hydrolysed by A. acidocaldarius, A. hesperidum, strain K1T and strain SD-11T. Most noticeable growth of strain K1T (up to 30 mg protein l–1) was observed in the presence of 0·1 % (w/v) complex organic substrates – peptone, yeast extract and casein hydrolysate – which was accompanied by the excretion of 0·5–1·2x10–3 units proteolytic enzymes ml–1, determined according to Nomoto & Narahashi (1956). Much like with the sulfobacilli (Wood & Kelly, 1983; Zakharchuk et al., 1994, 2003; Tsaplina et al., 1994, 2000), mixotrophic growth conditions were optimal for strain K1T; the most active growth and the highest biomass yield were observed under these conditions (see Fig. A, available as supplementary material in IJSEM Online). The specific growth rate reached values of 0·28 h–1 with glucose (1·2 mM), yeast extract (0·02 %) and 70 mM Fe2+ present in the medium. Fe2+ oxidation (determined by method of Reznikov et al., 1970) occurred at a rate of 0·62 mM h–1 and the amount of glucose consumed was 80 % (by the method of Ashwell, 1957) of its initial content (see Fig. B, available as supplementary material in IJSEM Online).
After a change in the cultivation conditions from mixotrophic to heterotrophic in the presence of glucose and yeast extract in the medium (first culture transfer), strain K1T used 60 % of the glucose initially present (1·2 mM) in the medium (see Fig. B, available in IJSEM Online). The specific growth rate reached values of 0·13 h–1. After a change in the cultivation conditions from mixotrophic to autotrophic without organic compounds, strain K1T exhibited lower growth rates in the first culture transfer (µ=0·035 h–1). The rate of iron oxidation was 0·27 mM h–1. Strain K1T oxidized only 15 % of the ferrous iron (70 mM) added to the medium. Chemo-organoheterotrophic and chemolithoautotrophic growth ceased after six and two culture transfers, respectively. Yeast extract is needed as growth factor for strain SD-11T (Dufresne et al., 1996).
Of all the alicyclobacilli, only A. cycloheptanicus, phylogenetically most closely related to strains K1T and SD-11T, required growth factors (certain vitamins and amino acids), but growth of all alicyclobacilli was stimulated by the addition of yeast extract to the medium (Wisotzkey et al., 1992). As with alicyclobacilli, ammonium served as the best source of nitrogen for strain K1T.
In cells of strain K1T grown mixotrophically in the presence of glucose, yeast extract and Fe2+, the activities of the key enzymes of carbohydrate metabolism were several times higher than in organotrophically grown cells (Karavaiko et al., 2001). The activity of almost all enzymes sharply decreased under autotrophic and heterotrophic conditions. Moreover, only enzymes of the Embden–Meyerhof–Parnas pathway could be detected in the cells grown autotrophically, whereas the key enzymes of the Entner–Doudoroff and pentose-phosphate pathways could not. The activity of pentose-phosphate-pathway enzymes was not detected under organotrophic growth (Karavaiko et al., 2001). The highest protein yield observed in cells of strain K1T under mixotrophic conditions, together with the highest activity for most carbohydrate metabolism enzymes under these conditions, allows an assumption to be made: that strain K1T can use additional energy derived from glucose oxidation during mixotrophic growth. Under the mixotrophic conditions the growth was stable. A higher capacity for glucose utilization was characteristic of the thermotolerant strain K1T (as compared with S. thermosulfidooxidans VKM B-1269T) (see Fig. B, available in IJSEM Online) and of the mesophilic strain SD-11T (Dufresne et al., 1996).
A significant biochemical characteristic of strain K1T that distinguishes it from sulfobacilli is its complete TCA cycle (Karavaiko et al., 2002). In sulfobacilli, the TCA cycle is blocked at the level of 2-oxoglutarate dehydrogenase, thus merely fulfilling a biosynthetic role (Zakharchuk et al., 1994, 2003; Tsaplina et al., 2000). Some strains of sulfobacilli are capable of oxidoreduction of iron (Bridge & Johnson, 1998). Similar to the phylogenetically related bacteria bacterium GSM, A. acidocaldarius and Alicyclobacillus-like strain Y004 (Johnson et al., 2001a, b, 2003), strain K1T was able also to reduce Fe3+: 10 mM for 7–10 days. Similar to bacterium GSM (Johnson et al., 2001a), strain K1T could weakly assimilate 14CO2 under different conditions with Fe2+ or S0 as the electron donors (see Table B, available as supplementary material in IJSEM Online). Thus, strains K1T and SD-11T differ from strains of the genus Sulfobacillus by a more-efficient organotrophic growth and from Alicyclobacillus strains by the requirement for inorganic electron donors. Judging from a number of the foregoing features, strain K1T occupies an intermediate position between the genera Sulfobacillus and Alicyclobacillus. Presumably, the well described bacilli GSM and SD-11T (Johnson et al., 2001a, 2003; Dufresne et al., 1996) and some unclassified strains may also group together with strain K1T.
On the basis of the above-mentioned morphological, physiological, chemotaxonomic and phylogenetic characteristics of strains K1T and SD-11T, two novel species are proposed, Alicyclobacillus tolerans sp. nov. and Alicyclobacillus disulfidooxidans comb. nov., respectively. Comparative characteristics of strains K1T and SD-11T and alicyclobacilli are given in Table 1.
Emended description of the genus Alicyclobacillus Wisotzkey et al. 1992 emend. Goto et al. 2003
The description of the genus Alicyclobacillus (Wisotzkey et al., 1992; Goto et al., 2003) should be supplemented with the following phenotypic characteristics. Temperature growth range is broader (<20–70 °C). Optimum growth temperature range is 35–60 °C. Species have a more diverse type of nutrition than previously thought: can also grow mixotrophically. The G+C content of the DNA ranges from 48·7 to 62·7 mol% (Tm).
The type species is Alicyclobacillus acidocaldarius (Darland and Brock 1971) Wisotzkey et al. 1992.
Description of Alicyclobacillus tolerans sp. nov.
Alicyclobacillus tolerans (tol.er'ans. L. part. adj. tolerans tolerant to changes in the growth temperature and pH).
Cells are non-motile, aerobic, Gram-positive, spore-forming rods, often occurring in short chains composed of two to four cells. Rods are either straight or slightly curved, 3–6 µm long and 0·9–1·0 µm wide. Reproduction is by binary fission with the transverse septum formation. The cytoplasm contains numerous vesicular inclusions, polyphosphate and poly-
-hydroxybutyrate granules. The location of oval spores is terminal or subterminal, enlarging the sporangium. Mixotroph, slowly oxidizing Fe2+, S0 or sulfide minerals in the presence of 0·2 g yeast extract l–1 or organic substrates (Table 1). Capable of reducing Fe3+. Facultative chemo-organoheterotroph. Organotrophic growth is supported by the substrates indicated in Table 1. The best source of nitrogen is ammonium. Thermotolerant: temperature range <20–55 °C; optimum 37–42 °C. Obligate acidophile: pH range for growth 1·5–5·0; optimum 2·5–2·7. The G+C content of the DNA is 48·7±0·6 mol%. Fatty acid profile is mainly composed of -cyclohexane-C17 : 0, -cyclohexane-C19 : 0, -cyclohexane-C17 : 0 2OH and -cyclohexane-C18 : 0. Normal and branched-chain iso- and anteiso-acids are also present. The main isoprenoid quinone is menaquinone MK-7 (90 %); minor component is MK-6. Isolated from oxidizable lead–zinc ores (Uzbekistan).
The type strain is K1T (=VKM B-2304T=DSM 16297T).
Description of Alicyclobacillus disulfidooxidans comb. nov.
Alicyclobacillus disulfidooxidans (di.sul.fi.do.ox'i.dans. L. adj. duplus double; L. n. sulfur sulfur; N.L. v. oxido oxidize; N.L. adj. disulfidooxidans disulfide-oxidizing bacterium).
Basonym: Sulfobacillus disulfidooxidans Dufresne et al. 1996.
The description is that given by Dufresne et al. (1996).
The type strain is SD-11T (=ATCC 51911T=DSM 12064T).
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ACKNOWLEDGEMENTS |
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