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Int J Syst Evol Microbiol 54 (2004), 2019-2024; DOI  10.1099/ijs.0.02932-0
© 2004 International Union of Microbiological Societies

Geobacillus gargensis sp. nov., a novel thermophile from a hot spring, and the reclassification of Bacillus vulcani as Geobacillus vulcani comb. nov.

Tamara N. Nazina1, Elena V. Lebedeva1, Andrei B. Poltaraus2, Tatyana P. Tourova1, Alexandre A. Grigoryan1, Diyana Sh. Sokolova1, Anatoliy M. Lysenko1 and George A. Osipov3

1 Institute of Microbiology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7/2, Moscow, 117312 Russia
2 Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, ul. Vavilova 32, Moscow, 117984 Russia
3 Research Group of Academician Yu. Isakov, Russian Academy of Medical Sciences, Sadovaya-Kudrinskaya 15, Moscow, 103001 Russia

Correspondence
Tamara N. Nazina
nazina{at}inmi.host.ru


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
A novel thermophilic spore-forming strain, GaT, was isolated from the Garga hot spring located in the northern part of the Transbaikal region (Russia). Strain GaT was found to be an aerobic, Gram-positive, rod-shaped, thermophilic (optimum growth temperature is 60–65 °C), chemo-organotrophic bacterium that grows on various sugars, carboxylic acids and hydrocarbons. The G+C content of its DNA is 52·9 mol%. The 16S rRNA gene sequence similarity data show that strain GaT is closely related to members of the genus Geobacillus. Relevant chemotaxonomic data (in particular, the major fatty acid profile of strain GaT, which includes iso-C15 : 0, iso-C16 : 0 and iso-C17 : 0 acids) support the assignment of this strain to the genus Geobacillus. The physiological, biochemical and DNA–DNA hybridization studies of strain GaT showed that it differs both genotypically and phenotypically from the recognized Geobacillus species. Based on these data, strain GaT belongs to a novel species, Geobacillus gargensis sp. nov. (type strain, GaT=VKM B-2300T=DSM 15378T). The analysis of the phenotypic characteristics (additional to those given in the original description) of the type strain of Bacillus vulcani (DSM 13174T) showed that they are very similar to the major phenotypic characteristics of the genus Geobacillus. The low DNA–DNA reassociation values of strain DSM 13174T with various species of this genus (from 38 to 54 %) clearly demonstrate a sufficient genomic distinction of this strain and its taxonomic status as a species. The physiological characteristics, phylogenetic position and DNA–DNA reassociation values of B. vulcani allow this species to be reclassified as Geobacillus vulcani comb. nov. The main properties that differentiate G. vulcani from the other species of the genus are its ability to produce acids from glycerol, lactose and ribose.

Published online ahead of print on 30 April 2004 as DOI 10.1099/ijs.0.02932-0.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Geobacillus gargensis GaT is AY193888.

Electron micrographs showing the flagellation of strain GaT and thin sections of vegetative cells of this strain are available as supplementary material in IJSEM Online. Data pertaining to the cellular fatty acid composition of strain GaT, and G+C content and DNA–DNA hybridization values are also available in IJSEM Online.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
In 2001, thermophilic bacilli of phylogenetic group 5 (Ash et al., 1991Go) were classified in a new genus, Geobacillus (Nazina et al., 2001Go). The bacteria of this genus with growth temperatures ranging from 35 to 78 °C are widespread in various geographical areas on Earth (Claus & Berkeley, 1986Go; White et al., 1993Go; Manachini et al., 2000Go; Markossian et al., 2000Go; Nazina et al., 2000Go, 2001Go; Maugeri et al., 2002Go). The genus includes the species Geobacillus stearothermophilus, Geobacillus thermocatenulatus, Geobacillus thermoleovorans, Geobacillus kaustophilus, Geobacillus thermoglucosidasius, Geobacillus thermodenitrificans, Geobacillus subterraneus, Geobacillus uzenensis, Geobacillus caldoxylosilyticus and Geobacillus toebii (Logan & Berkeley, 1984Go; Claus & Berkeley, 1986Go; Golovacheva et al., 1975Go; Suzuki et al., 1983Go; Priest et al., 1988Go; White et al., 1993Go; Zarilla & Perry, 1987Go; Manachini et al., 2000Go; Ahmad et al., 2000Go; Nazina et al., 2001Go; Fortina et al., 2001aGo; Sung et al., 2002Go). Many thermophilic bacilli that have not yet been included in recognized species (‘Bacillus caldolyticus’, ‘Bacillus caldotenax’, ‘Bacillus caldovelox’ and ‘Geobacillus uralicus’), and the recognized species Bacillus thermantarcticus, Saccharococcus thermophilus and Bacillus vulcani belong to genetic group 5, which is close to the genus Geobacillus both phenotypically and phylogenetically (Ash et al., 1991Go; Rainey et al., 1994Go; Caccamo et al., 2000Go; Heinen & Heinen, 1972Go; Rainey & Stackebrandt, 1993Go; Nystrand, 1984Go; Nicolaus et al., 1996Go; Popova et al., 2002Go). Members of the genus Geobacillus contain iso-branched saturated fatty acids (iso-C15 : 0, iso-C16 : 0 and iso-C17 : 0) as the major fatty acids and exhibit high intrageneric similarity of their 16S rRNA gene sequences (96·5–99·2 %) (Nazina et al., 2001Go; Fortina et al., 2001aGo).

When studying the microbial communities of the Garga hot spring located in the north-eastern part of the Transbaikal region, we isolated several dominant aerobic, thermophilic, spore-forming bacteria in pure cultures. The Garga spring is characterized by a maximum temperature of 75 °C and pH 7·8–8·5. When the water temperature decreases to about 60 °C, the microbial mats that occur in this spring begin to develop. The colour of the mats varies from orange on the surface to green in deeper layers. The mats contain oxygenic cyanobacteria and non-oxygenic green filamentous photosynthetic bacteria, for example Chloroflexus (V. M. Gorlenko, personal communication). The material used for the isolation of bacilli was taken from the upper layer of a microbial mat. The preliminary phenotypic and genotypic characterization of one of the isolates (strain GaT) suggested its affiliation with the genus Geobacillus. In this study, we report the relevant characteristics of strain GaT and the phenotypic and genotypic characteristics of the species B. vulcani (Caccamo et al., 2000Go), which allow strain GaT to be classified as a novel species, Geobacillus gargensis sp. nov., and B. vulcani to be reclassified as Geobacillus vulcani comb. nov.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Bacterial strains, maintenance and characterization.
Strain GaT was isolated from the upper layer of a microbial mat by using the technique of serial dilutions and inoculation of an agar medium containing sucrose (Adkins et al., 1992Go). The agar plates were incubated at 60 °C. The colonies that grew within a few days were transferred to a liquid medium of the same composition. The purity of the isolate was tested microscopically.

Cell morphology, physiological characteristics, common DNA characteristics, 16S rRNA gene sequences, phylogenetic properties and cellular fatty acid profile were studied as described previously (Nazina et al., 2001Go).

The reference strains used in this study were obtained from the DSMZ (Deutsche Sammlung von Mikroorganismen und Zellkulturen) (G. uzenensis DSM 13551T, G. subterraneus DSM 13552T, Bacillus vulcani DSM 13174T and G. kaustophilus DSM 7263T), from the All-Russian Collection of Microorganisms (G. uzenensis B-2228, ‘G. uralicus’ B-2276, G. thermocatenulatus B-1259T and Bacillus subtilis B-4537) and from Christian Jeanthon (Laboratory of Marine Microbiology, Station Biologique, CNRS UPR9042, Roscoff, France) (G. stearothermophilus DSM 22T, G. thermoleovorans DSM 5366T and G. thermodenitrificans DSM 466).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
The morphological and chemical characteristics of strain GaT are consistent with its affiliation with the genus Geobacillus. Strain GaT produced small, round, mucous, small, non-pigmented colonies with a diameter of about 1 mm. Vegetative cells were motile (in the exponential phase) peritrichously flagellated rods with rounded ends (Fig. A, available as supplementary material in IJSEM Online). The cells were 1·0–1·5 µm wide and 6–12 µm long. The endospore was terminal and ellipse-shaped, and slightly distended the mother cell. Cell division was usually symmetric. The electron microscopic examination of cells showed that they are likely to be Gram-positive (Fig. B, available as supplementary material in IJSEM Online), since their cell wall did not have the external lipoprotein layer. The Gram-positive staining of the cell wall was also demonstrated by light microscopy. The cell wall had a complex structure, namely, it was composed of three to five layers. The outermost layer exhibited the presence of regularly arranged structures that are typical of S layers. The immature spores located within the sporangium contained the cytoplasm, polyribosomes, the coat and the cortex.

The physiological characteristics of strain GaT are given in Table 1Go and in the species description. Strain GaT was found to be a thermophilic bacterium, since it could grow within the temperature range 45–70 °C, with an optimum growth temperature of 60–65 °C. The isolate grew well within the pH range 5·5–8·5, with an optimum pH for growth of 6·5–7·0. The isolate was able to utilize a variety of sugars, carboxylic acids and hydrocarbons aerobically. The bacterium was able to grow in synthetic media and did not require any growth factors, vitamins, NaCl or KCl. Significant culture turbidity was observed in a medium with sucrose as the sole carbon and energy source, with the generation time being 2·5 h.


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  		Table 1. Characteristics that differentiate Geobacillus gargensis sp. nov. from the closely related species of the genus Geobacillus

Taxa: 1, G. gargensis strain GaT; 2, G. stearothermophilus; 3, G. thermocatenulatus; 4, G. thermoglucosidasius; 5, G. thermoleovorans; 6, G. kaustophilus; 7, G. thermodenitrificans; 8, G. uzenensis; 9, G. subterraneus; 10, G. caldoxylosilyticus; 11, G. toebii; 12, G. vulcani. Symbols: +, growth/activity observed; –, no growth/activity observed; W, weak growth; ND, not determined; V, variable within group. Data are from the present study (G. gargensis) or from Logan & Berkeley (1984)Go, Claus & Berkeley (1986)Go and Priest et al. (1988)Go (G. stearothermophilus); Golovacheva et al. (1975)Go, Nazina et al. (2001)Go and data from the present study (G. thermocatenulatus); Suzuki et al. (1983)Go (G. thermoglucosidasius); Zarilla & Perry (1987)Go and Nazina et al. (2001)Go (G. thermoleovorans); Priest et al. (1988)Go and White et al. (1993)Go (G. kaustophilus); Manachini et al. (2000)Go (G. thermodenitrificans); Nazina et al. (2001)Go (G. uzenensis; G. subterraneus); Ahmad et al. (2000)Go and Fortina et al. (2001a)Go (G. caldoxylosilyticus); Sung et al. (2002)Go (G. toebii); Caccamo et al. (2000)Go and data from the present study (B. vulcani=G. vulcani). Strain GaT and all other strains are negative for indole production and are catalase-positive, and produce acid from glucose, fructose, maltose, mannose, sucrose and trehalose (in the description of G. toebii, most of these characteristics are absent).

 
16S rRNA gene sequence analysis
The analysis of the almost-complete 16S rRNA gene sequence (1459 nucleotides) of strain GaT, corresponding to Escherichia coli positions (Brosius et al., 1978Go) 37–1479, showed that this strain has sequence similarity values of 94·6–99·3 % to the recognized species of the genus Geobacillus (Fig. 1Go). The strain formed a separate phylogenetic cluster, which was closely related to G. kaustophilus (99·3 % sequence similarity), G. thermoleovorans (99·1 % similarity), G. thermocatenulatus (99·0 % similarity) and B. vulcani (98·8 % similarity). The analysis also showed that B. vulcani was closely related to G. kaustophilus (99·4 % sequence similarity). The phylogenetic clustering of B. vulcani with members of the genus Geobacillus, with 95·3–99·4 % sequence similarity values, suggested that B. vulcani may actually represent a species of the genus Geobacillus. In order to verify the taxonomic positions of strain GaT and B. vulcani DSM 13174T, they were subjected to DNA–DNA hybridization analysis with the type strains of most of the known Geobacillus species.



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  		Fig. 1. Phylogenetic tree showing the positions of strain GaT and B. vulcani among Geobacillus species. The scale bar represents the expected number of changes per sequence position (the Jukes–Cantor distance). Bootstrap values (expressed as percentage of 100 replications) are shown at branch points; values greater than 95 % were considered significant. G., Geobacillus; B., Bacillus; S., Saccharococcus. The GenBank/EMBL/DDBJ accession numbers of the reference strains are shown in parentheses.

 
DNA base composition and DNA–DNA similarity
The G+C content of the DNA of strain GaT was found to be 52·9±0·2 mol%. The DNA–DNA reassociation values of strain GaT with B. vulcani DSM 13174T and the nine type or reference strains of the genus Geobacillus varied from 31 to 55 % (see Table A available in IJSEM Online). These values are within the range that is typical of a genospecies (30–70 %) (Wayne et al., 1987Go). The DNA–DNA reassociation values indicate that both strain GaT and B. vulcani DSM 13174T belong to the genus Geobacillus as separate species. The DNA–DNA hybridization values between the thermophilic Geobacillus strains and a mesophilic strain of B. subtilis, taken as an outgroup, varied from 3 to 10 %.

Our earlier (Nazina et al., 2001Go) and present data contradict the results of the hybridization experiments of Sunna et al. (1997)Go, who reported a very high value of DNA–DNA reassociation (more than 75 %) between Bacillus thermocatenulatus, Bacillus kaustophilus and Bacillus thermoleovorans. This disagreement may be due to the absence of adequate hybridization controls at inter- and intraspecies levels in the experiments of Sunna et al. (1997)Go. The DNA–DNA reassociation values obtained by Caccamo et al. (2000)Go for B. kaustophilus, Bacillus thermodenitrificans and Bacillus stearothermophilus were within a range of 40·4–61·4 %, which is in agreement with our data.

Fatty acids
The fatty acid profile of strain GaT (see Table B and Fig. C in IJSEM Online) was largely composed of iso-C15 : 0 (25·84 %), iso-C16 : 0 (25·91 %) and iso-C17 : 0 (19·79 %). In the fatty acid composition, strain GaT and the bacterium B. vulcani were clustered with the species of the genus Geobacillus, but not with the thermophilic species of the genera Bacillus and Ureibacillus or Thermobacillus and Aneurinibacillus (data not shown) (Kämpfer, 1994Go; Nazina et al., 2001Go; Manachini et al., 2000Go; Ahmad et al., 2000Go; Fortina et al., 2001aGo, bGo; Caccamo et al., 2000Go; Andersson et al., 1995Go).

Strain GaT differed both genotypically and phenotypically from the recognized species of the genus Geobacillus. The strain utilized acetate and lactate, but not citrate, and hydrolysed casein and aesculin, but not gelatin. The strain was also able to produce acids from glycerol and ribose, but not from inositol, lactose or xylose. The methyl red and the urea decomposition tests were negative. All these properties allowed us to differentiate strain GaT from B. vulcani and the representatives of the genus Geobacillus. Based on the results of the phenotypic and genotypic analyses, we conclude that strain GaT is a member of a novel Geobacillus species, for which we propose the name Geobacillus gargensis sp. nov.

Characteristics of reference strains
The phenotypic characteristics of B. vulcani DSM 13174T and G. thermocatenulatus B-1259T, additional to those available in the original description of these strains, are summarized in Table 1Go. The results of the Voges–Proskauer test and the test for the anaerobic growth of strain DSM 13174T in glucose broth were negative (as with the other species of the genus Geobacillus). Strain DSM 13174T grew on C6 hydrocarbons, but not on C14–C16 hydrocarbons; no acids were produced from adonitol, arabinose, inositol, rhamnose or sorbitol. In contrast to their original descriptions (Golovacheva et al., 1975Go; Caccamo et al., 2000Go), strain B-1259T hydrolysed starch, whereas strain DSM 13174T was catalase-positive. A comparison of B. vulcani DSM 13174T with the phylogenetically closest species G. kaustophilus DSM 7263T (99·4 % sequence similarity) indicated that they differ phenotypically in the ability to hydrolyse casein and to produce acids from glycerol, inositol, lactose and ribose. Thus, the species B. vulcani must be reclassified as Geobacillus vulcani comb. nov. on the basis of its physiological characteristics, phylogenetic position and DNA–DNA reassociation values.

Description of Geobacillus gargensis sp. nov.
Geobacillus gargensis [gar.g.en'sis. N.L. adj. gargensis of Garga, pertaining to the Garga hot spring located in Eastern Siberia (Russia), from which the type strain was isolated].

Cells are rod-shaped, motile by means of peritrichous flagella and produce terminally located ellipsoidal spores in slightly swollen sporangia. The cells are 1·0–1·5 µm wide and 6–12 µm long. Gram-positive, with the chemo-organotrophic type of metabolism. Aerobic. No acids are produced from raffinose. Utilizes hydrocarbons (C12–C16), butyrate, pyruvate, fumarate, succinate, peptone, tryptone, nutrient broth, potato agar and yeast extract as carbon and energy sources. No growth occurs on methanol, ethanol, propanol, butanol or isobutanol. Unable to grow autotrophically on H2+CO2. Unable to produce NH3 from peptone. H2S is not produced. The egg-yolk lecithinase test is negative. Growth factors, vitamins, NaCl and KCl are not required for growth. The optimum temperature for growth is 60–65 °C, with an optimum pH of 6·5–7·0. Fatty acid profile consists of iso-C15 : 0 (25·84 %), iso-C16 : 0 (25·91 %), iso-C17 : 0 (19·79 %), anteiso-C17 : 0 (8·2 %), anteiso-C15 : 0 (1·99 %), C17 : 1 (4·21 %), iso-C17 : 1 (3·91 %) and iso-C18 : 0 (1·40 %). Carbon source utilization and hydrolysis of chromogenic substrates (including differentiating characters for all Geobacillus species) are indicated in Table 1Go.

The type strain is GaT (=VKM B-2300T=DSM 15378T). Isolated from the Garga hot spring.

Description of Geobacillus vulcani comb. nov.
Basonym Bacillus vulcani Caccamo et al. 2000Go.

Geobacillus vulcani (vul.ca'ni. L. gen. m. n. vulcani of the volcano, pertaining to the Aeolian Island volcano with a shallow marine hydrothermal vent, from which the organism was isolated).

Phylogenetic and chemotaxonomic data indicate that Bacillus vulcani is more closely related to species of the genus Geobacillus than to any species of the genus Bacillus. The cultural, morphological and physiological characteristics of the species, described by Caccamo et al. (2000)Go, are valid, except that strain DSM 13174T is catalase-positive. Fatty acid profile consists of iso-C15 : 0 (16·6 %), iso-C16 : 0 (14·6 %), iso-C17 : 0 (21 %), anteiso-C17 : 0 (11·4 %) and C18 : 0 (13 %). Carbon source utilization and hydrolysis of chromogenic substrates are indicated in Table 1Go.

The type strain is 3s-1T (=DSM 13174T=CIP 106305T). Isolated from sediment of a shallow hydrothermal vent.


   ACKNOWLEDGEMENTS
 
We are grateful to V. Gorlenko from the Institute of Microbiology, Russian Academy of Sciences, Moscow, Russia for providing samples from the Garga hot spring and to L. L. Mityushina from INMI RAS for assistance. This work was supported by grants from the Russian Foundation for Basic Research (project numbers 01-04-49250, 02-04-39002) and from the Russian Ministry of Science and Technology (project no. 43.073.1.1.2515).


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INT J SYST EVOL MICROBIOL MICROBIOLOGY J GEN VIROL
J MED MICROBIOL ALL SGM JOURNALS