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1 Japan Collection of Microorganisms, RIKEN (Institute of Physical and Chemical Research), Wako-shi, Saitama 351-0198, Japan
2 Biological Resource Center, Biotechnology Center, National Institute of Technology and Evaluation, Kazusa-Kamatari, Kisarazu, Chiba 292-0812, Japan
3 Museum of Natural History, University of the Philippines Los Baños College, Laguna 4031, Philippines
4 Laboratory of Microbiology, Department of Applied Biology and Chemistry, Faculty of Applied Bioscience, Tokyo University of Agriculture, Sakuragaoka, Setagaya-ku, Tokyo 156-8502, Japan
Correspondence
T. Itoh
ito{at}jcm.riken.go.jp
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession number for the 16S rDNA sequence of strain IC-154T is AB087499.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). Until now, all Crenarchaeota species that have been isolated are either hyperthermophilic or extremely thermophilic, although the existence of mesophilic and psychrophilic Crenarchaeota is suggested by culture-independent molecular phylogenetic analyses (Hershberger et al., 1996). The phylum Crenarchaeota currently comprises the orders Sulfolobales, Thermoproteales and Desulfurococcales, which are well-supported by 16S rDNA sequence data and by phenotypic properties, such as cell morphology and lipid composition (Burggraf et al., 1997; Reysenbach, 2001). Members of the order Desulfurococcales are coccoid or disc-shaped, strictly anaerobic [except for Aeropyrum pernix (Sako et al., 1996)] and neutrophilic or weakly acidophilic, growing optimally at pH 5·5–7·5 (Huber & Stetter, 2001). Two families, Desulfurococcaceae and Pyrodictiaceae, are known in the order Desulfurococcales. On the 16S rDNA-based phylogenetic tree, members of the family Pyrodictiaceae (with optimal growth at 
100 °C) form a coherent cluster, whereas members of the family Desulfurococcaceae, with optimal growth at 85–95 °C, are more diverse. At present, there are three and seven genera with validly published names, respectively, in these families [i.e. Pyrodictium, Hyperthermus and Pyrolobus in the family Pyrodictiaceae, and Desulfurococcus, Aeropyrum, Ignicoccus, Staphylothermus, Stetteria, Sulfophobococcus and Thermosphaera in the family Desulfurococcaceae (Huber & Stetter, 2001)]. In addition, the recently described species Acidilobus aceticus (Prokofeva et al., 2000) and crenarchaeote strain NC12 (‘Caldococcus noboribetus’; Aoshima et al., 1996) seem to be distantly affiliated to the order Desulfurococcales.
During the course of a search for novel thermophilic archaea from a hot spring named ‘Mud Spring’ on the side of Mt Maquiling, Philippines, we have isolated a number of thermophilic Archaea (unpublished data). Among the four rod-shaped isolates, two strains were identified as Caldivirga maquilingensis, a member of the family Thermoproteaceae (Itoh et al., 1999). In the present study, we characterize another group of the archaeal isolates, which are cocci distantly related to the genus Acidilobus and strain NC12 (based on phylogenetic analysis of 16S rDNA), and propose the name Caldisphaera lagunensis gen. nov., sp. nov.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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), were incubated in an enrichment medium under the following growth conditions. Gas phase: air, N2 or H2/CO2 (4 : 1, v/v; 100 kPa); temperature, 70 or 85 °C; pH, 2·5 or 5·0 (adjusted at room temperature). The enrichment medium was composed of Sulfolobus medium (Brock et al., 1972) supplemented with yeast extract (Difco) (1·0 g l-1 for aerobes and 0·5 g l-1 for anaerobes) and 10 g sulfur l-1. For the isolation of anaerobic strains in N2 or H2/CO2 (4 : 1, v/v; 100 kPa), the enrichment medium was further supplemented with 1·0 mg resazurin l-1 and reduced with 0·5 g Na2S.9H2O l-1. After 1 week of cultivation, cultures were diluted serially (1 : 10) and incubated under the same conditions as for the enrichment cultivation. Following the serial dilution–cultivation method (three times), the highest dilution that showed growth was again diluted serially (1 : 10) and each dilution was divided equally into five tubes/vials and cultivated. This step was repeated for one grown culture at the highest dilution. Finally, one grown culture at the highest dilution was assigned an IC number, as shown in Table 1. Two isolates (IC-154T and IC-163) were cultivated routinely in modified TCD medium (Itoh et al., 1999) in an atmosphere of N2 at 75 °C.
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). Unless otherwise stated, modified TCD medium (Itoh et al., 1999) was used as the basal medium for phenotypic studies, and cultures were incubated at 75 °C in an atmosphere of N2. For electron microscopy, cells were placed on a collodion-coated grid, shadowed with platinum–palladium and examined with a transmission electron microscope (H-300; Hitachi). To determine the pH range for growth, the pH was adjusted at room temperature; it was almost the same at 75 °C in the presence of 10 mM trisodium citrate as buffer. To test tolerance of O2, the strains were inoculated into sulfur-free, non-reduced TCD medium in an atmosphere of N2 that contained various levels of air, and incubated on a reciprocal shaker (80 r.p.m.). Possible electron acceptors were identified by using test medium (Itoh et al., 1998) reduced with 0·5 g Na2S.9H2O l-1 in an atmosphere of N2. Utilization of O2 as an electron acceptor was examined in the same test medium, but not reduced, in an atmosphere of N2 that contained 1 % O2. Growth was estimated by fluorescence intensity after treatment with NanoOrange dye (Molecular Probes) following the supplier's protocol, or by direct counting with a Petroff–Hauser counting chamber (0·02 mm in depth). A good correlation between the two methods was obtained. Metabolic products were detected by using a gas chromatograph (GC-7A, Shimadzu) equipped with a 2 m glass column (FAL-M 25 %, 80/100 mesh) and a flame-ionization detector. Likewise, H2 and CO2 were detected by GLC with a thermal conductivity detector [column: H2 with MS-5A, and CO2 with PoraPak Q (both from Supelco)]. 16S rDNA was amplified with primers A-20F (5'-TCCGGTTGATCCTGCCG-3', corresponding to positions 8–24 in the Escherichia coli numbering system) and A-1530R (5'-GGAGGTGATCCAGCCG-3', positions 1540–1525). Initially, partial 16S rDNA sequences of all isolates were determined by using a sequencing primer, A-520R (5'-GTATTACCGCGGCGGCTG-3', positions 536–519), and almost-whole 16S rDNA sequences of the representative strains (IC-154T and IC-163) were determined as described previously (Itoh et al., 1999). The 16S rDNA sequences were first aligned with the CLUSTAL X program (Thompson et al., 1997) and edited manually with the aid of the SSU rRNA database (Van de Peer et al., 2000). Evolutionary distances were calculated after gaps, ambiguous bases and unalignable regions had been eliminated. The phylogenetic tree was constructed by using the neighbour-joining method (Saitou & Nei, 1987) and was evaluated by bootstrap resampling (Felsenstein, 1985). |
RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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. Three Metallosphaera strains were obtained under one set of growth parameters (air, 70 °C, pH 5·0) and ten strains related to Sulfolobus yangmingensis, Sulfurisphaera ohwakuensis and Sulfolobus tokodaii were obtained under several sets of growth conditions [i.e. air or H2/CO2 (4 : 1, v/v; 100 kPa), 70 or 85 °C, pH 2·5 or 5·0]. On the other hand, four strains (IC-154T, IC-158, IC-163 and IC-165), isolated under N2 or H2/CO2 (4 : 1, v/v; 100 kPa), at 70 °C, pH 5·0, showed low similarity values to Acidilobus aceticus (Prokofeva et al., 2000) and strain NC12 [representing ‘Caldococcus noboribetus’ (Aoshima et al., 1996)], suggesting that they represent a novel taxon related to the genus Acidilobus. Of these four isolates, strains IC-154T and IC-163, isolated under H2/CO2 (4 : 1, v/v; 100 kPa) and N2, respectively, were selected for further characterization.
Morphology and phenotypic characteristics
Cells of strains IC-154T and IC-163 were mostly regular cocci, 0·8–1·1 µm in diameter (Fig. 1). Cells 2·0–2·5 µm in diameter were occasionally observed. They usually occurred singly or in pairs, and sometimes in aggregates of several cells. Of the two strains characterized, only IC-163 had pili attached to its cells (up to three pili). The two strains were non-motile and grew under strictly anaerobic conditions with N2, N2/CO2 (4 : 1, v/v; 100 kPa) or H2/CO2 (4 : 1, v/v; 100 kPa) as the gas phase. They also grew in a low-oxygen atmosphere (up to 2 % O2), but not in 5 % O2 or higher. They grew at 45–80 °C, and at pH 2·3–5·4 in the presence of 10 mM trisodium citrate as buffer. No growth was observed at 40 or 82 °C (at pH 4·0), or at pH 2·0 or 6·0 (at 75 °C). In buffered medium, strain IC-154T grew optimally at 70–78 °C and at pH 3·5–4·0. The doubling time under optimal conditions (75 °C, pH 3·7) was 5 h and, at stationary phase, the cultures contained approximately 1·4–1·5x107 cells ml-1. The two strains did not grow under autotrophic conditions: medium with no yeast extract under H2/CO2 (4 : 1, v/v; 100 kPa). They utilized starch, glycogen, gelatin, beef extract, yeast extract and peptone as carbon and energy sources, but not D-arabinose, D-fructose, D-galactose, D-glucose, lactose, maltose, mannose, D-ribose, sucrose, D-xylose, acetate, butyrate, citrate, formate, fumarate, lactate, L-malate, propionate, pyruvate, succinate, methanol, formamide, methylamine or trimethylamine (final concentrations: 0·05 % for proteinaceous substances, 0·5 % for sugars and 0·2 % for other compounds). Only strain IC-154T could utilize casamino acids (weakly). Addition of a vitamin mixture (Balch et al., 1979) to the medium weakly promoted growth of the two strains. Both strains tolerated up to 1·5 % NaCl in the growth medium (no growth occurred at 1·75 % NaCl). Growth was significantly enhanced by the presence of sulfur as an electron acceptor in the medium. Likewise, growth was slightly promoted by the presence of fumarate, sulfate (only for IC-163) and O2 (1 %, only for IC-154T), but not by thiosulfate, cystine, oxidized glutathione, malate, nitrate or FeCl3. Hydrogen sulfide was detected from cultures grown with sulfur. Acetate, propionate, isobutyrate, butyrate and isovalerate, as well as H2 and CO2, were detected as metabolic products from cultures grown with or without sulfur. Both strains were sensitive to erythromycin, novobiocin and rifampicin, but resistant to ampicillin, chloramphenicol, kanamycin, oleandomycin, streptomycin and vancomycin (100 µg ml-1). The core lipid fractions contained cyclic and acyclic tetraethers.
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. The almost-entire 16S rDNA sequences (1466 bases) determined for the two strains were identical. The G+C ratio was 61·8 %. The 16S rDNA sequence of IC-154T was free from chimeric artefacts, according to the CHECK_CHIMERA program of the Ribosomal Database Project (Maidak et al., 2001). It contained all of the small-subunit rRNA signature bases that define the crenarchaeotes (Woese et al., 1993), except for two bases at positions 34 and 1335 (see Table 2). Phylogenetic analysis was conducted with other crenarchaeote species by comparing 1066 bases in order to construct a phylogenetic tree (Fig. 2). The analysis revealed that the two strains were most closely associated with the order Desulfurococcales within the phylum Crenarchaeota. However, they formed an independent lineage that was related distantly to Acidilobus aceticus and strain NC12, which is tentatively named ‘Caldococcus noboribetus’ (sequence similarity, 91·5–92·6 %). Sequence similarity to members of the orders Desulfurococcales (except for Acidilobus aceticus and strain NC12), Sulfolobales and Thermoproteales was 88·8–91·4, 84·8–86·9 and 86·2–88·1 %, respectively. On the phylogenetic tree, strain IC-154T, Acidilobus aceticus and strain NC12 clustered together with a relatively high bootstrap value (94 %), thereby this group of strains is tentatively named the Acidilobus group. As shown in Table 2, signature sequence analysis revealed that the Acidilobus group had five sequence positions (i.e. positions 34, 321 : 332, 1308 : 1329, 1335 and 1393) that are unique to this group among the phylum Crenarchaeota, and only two positions (i.e. positions 784 : 798 and 1364) that are shared with the remaining members of the order Desulfurococcales.
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; Huber & Stetter, 2001). Furthermore, 16S rDNA sequence analysis revealed that the two strains are most closely related to Acidilobus aceticus (Prokofeva et al., 2000) and strain NC12, a representative of ‘Caldococcus noboribetus’ (Aoshima et al., 1996), and form a cluster named the Acidilobus group, as described above. In addition to the phylogenetic analysis, members of the Acidilobus group share certain phenotypic properties: all are acidophilic cocci (optimal pH, 3·0–4·0), are strictly anaerobic and organotrophic, use sulfur as an electron acceptor and inhabit terrestrial acidic hot springs. It is noteworthy that all remaining species of the order Desulfurococcales, including the terrestrial genera Desulfurococcus (Zillig et al., 1982; Bonch-Osmolovskaya et al., 1988), Sulfophobococcus (Hensel et al., 1997) and Thermosphaera (Huber et al., 1998), favour weakly acidic to neutral pH for growth (optimal pH, 5·5–7·5). Considering the outlying position of the Acidilobus group on the phylogenetic tree (Fig. 2) and the fact that only a few signature sequences are shared with other species of the order Desulfurococcales (Table 2), inclusion of the Acidilobus group in the order Desulfurococcales may be controversial. At the moment, however, sequence analysis of 16S rDNA from more related strains, or of molecules other than 16S rDNA, is required to settle the taxonomic status of the Acidilobus group at order or family level. Strains IC-154T and IC-163 can be differentiated from Acidilobus aceticus, and even from strain NC12, by the following characteristics. Strains IC-154T and IC-163 are extreme thermophiles that grow optimally around 75 °C and not at 82 °C, whereas Acidilobus aceticus and NC12 are hyperthermophilic and grow optimally at 85 and 92 °C, respectively. Moreover, Acidilobus aceticus has a genomic DNA G+C content of 53·8 mol%, requires yeast extract when grown with starch as the carbon source and does not produce H2 during growth. On the phylogenetic tree, strains IC-154T and IC-163 occupy an independent position and show at least 7·7 % sequence dissimilarity from any other crenarchaeote strains. Therefore, these two strains represent a novel genus in the Acidilobus group. Except for a few phenotypic differences between strains IC-154T and IC-163 (e.g. presence or absence of pili and spectrum of electron acceptors), the two strains are similar to each other and their 16S rDNA sequences are identical, suggesting that they belong to a single species. Thus, we propose the name Caldisphaera lagunensis gen. nov., sp. nov. to accommodate the four strains IC-154T, IC-158, IC-163 and IC-165. The type strain of the novel species is IC-154T (=JCM 11604T=MCC-UPLB 1331T=ANMR 0165T).
Our attempt to isolate thermophilic organisms from an acidic hot spring in the Philippines resulted in the detection of five different crenarchaeotic species, as determined by analysis of their partial 16S rDNA sequences. Rod-shaped crenarchaeotes, Caldivirga maquilingensis and Thermoproteus sp., were isolated in an atmosphere of N2 at pH 5·0 and 85 °C, as shown previously (Itoh et al., 1999). Otherwise, coccoid crenarchaeotes, Metallosphaera and Sulfolobus–Sulfurisphaera-related strains and Caldisphaera lagunensis were obtained, as shown in this study. The growth conditions for isolation of Metallosphaera strains (air, pH 5·0, 70 °C) are consistent with the optimal growth conditions of known Metallosphaera species, except for pH (range, 1·0–4·5; Huber et al., 1989; Fuchs et al., 1995). The Sulfolobus–Sulfurisphaera isolates prevailed in enrichment cultures grown under various conditions, as shown in Table 1. Indeed, representative strains (IC-146, IC-147, IC-155, IC-156 and IC-157) of the Sulfolobus–Sulfurisphaera isolates grew aerobically and anaerobically in a H2/CO2 (4 : 1, v/v) gas atmosphere (data not shown). Sulfolobus yangmingensis is phylogenetically most closely related to our Sulfolobus–Sulfurisphaera isolates; nevertheless, Sulfolobus yangmingensis, as well as Sulfolobus tokodaii, are described as obligate aerobes (Jan et al., 1999; Suzuki et al., 2002), whereas Sulfurisphaera ohwakuensis (Kurosawa et al., 1998) is able to grow anaerobically by utilizing H2 as an electron donor and sulfur as an electron acceptor (which is the same as our isolates). The taxonomic delineation of the genera Sulfolobus and Sulfurisphaera should be re-evaluated in the near future.
Caldisphaera lagunensis was able to grow by dissimilatory fermentative sulfur reduction in an atmosphere of N2. Therefore, employment of N2 as the gas phase in enrichment cultures may be advantageous for selective isolation of strains related to the genus Caldisphaera from sample sites where Caldisphaera cohabits with anaerobically growing Sulfolobales species, such as Sulfurisphaera ohwakuensis. The isolation of two genera (Caldivirga and Caldisphaera) from a single hot spring site suggests that further undescribed archaeal genera may be isolated from unexplored geothermal habitats.
Description of Caldisphaera gen. nov.
Caldisphaera (Cal.di.sphae'ra. L. adj. caldus hot; L. fem. n. sphaera sphere; N.L. fem. n. Caldisphaera a hot spherical cell).
Cells are mostly regular cocci, 0·8–1·1 µm in diameter, and occur singly or in pairs. Pili may be present. Non-motile. Extremely high temperature (70–78 °C) and acidic conditions (pH 3·5–4·5) are preferred for growth. Grows anaerobically. Resistant to chloramphenicol, kanamycin, oleandomycin, streptomycin and vancomycin. Sensitive to erythromycin, novobiocin and rifampicin. Possesses cyclic and acyclic tetraether core lipids. DNA G+C content of the type species is 31 mol%. The 16S rDNA is typical of a crenarchaeote in sequence signature analysis. Phylogenetically, the genus represents an independent lineage related to the order Desulfurococcales. Inhabits terrestrial hot springs. The type species is Caldisphaera lagunensis.
Description of Caldisphaera lagunensis sp. nov.
Caldisphaera lagunensis (la.gu.nen'sis. N.L. fem. adj. lagunensis pertaining to Laguna, the province in the Philippines where the type strain was isolated).
Grows anaerobically and tolerates low levels of oxygen (up to 2 %). Heterotrophic. Growth occurs at 45–80 °C and pH 2·3–5·4. Under optimal growth conditions, doubling time is 5 h. Growth occurs at low salinity (
1·5 % NaCl). Chemo-organotrophic; utilizes starch, glycogen, gelatin, beef extract, yeast extract and peptone as carbon and energy sources. Forms acetate, propionate, isobutyrate, butyrate, isovalerate, H2 and CO2 as metabolic products. Growth is stimulated by the presence of sulfur. Hydrogen sulfide is formed. DNA G+C content is 31 mol%.
The type strain is IC-154T (=JCM 11604T =MCC-UPLB 1331T =ANMR 0165T). Reference strains are IC-158 (=ANMR 0169), IC-163 (=JCM 11605 =MCC-UPLB 1332 =ANMR 0174) and IC-165 (=ANMR 0176). Isolated from a hot spring on Mt Maquiling, Laguna, the Philippines.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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