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Int J Syst Evol Microbiol 57 (2007), 1554-1560; DOI  10.1099/ijs.0.64820-0
© 2007 International Union of Microbiological Societies

Pelagibacillus goriensis gen. nov., sp. nov., a moderately halotolerant bacterium isolated from coastal water off the east coast of Korea

Yoon-Gon Kim1, Chung Yeon Hwang1, Kwang Woo Yoo2, Hyung Tae Moon2, Jung-Hoon Yoon3 and Byung Cheol Cho1

1 School of Earth and Environmental Sciences and Research Institute of Oceanography, Seoul National University, San 56-1 Shillim-dong, Kwanak-gu, Seoul 151-742, Republic of Korea
2 Safety and Technology Department, Korea Hydro and Nuclear Power Co. Ltd, 167 Samseong-dong, Gangnam-gu, Seoul 135-791, Republic of Korea
3 Korea Research Institute of Bioscience and Biotechnology (KRIBB), PO Box 115, Yusong, Taejon, Republic of Korea

Correspondence
Byung Cheol Cho
bccho{at}snu.ac.kr


   ABSTRACT
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A Gram-positive, moderately halotolerant bacterium, designated CL-GR16T, was isolated from coastal water off the east coast of Korea. The strain was strictly aerobic, rod-shaped, motile by means of peritrichous flagella and produced ellipsoidal spores. Phylogenetic analysis based on 16S rRNA gene sequences revealed that the isolate represented an independent lineage within Bacillus rRNA group 1, showing 93.6–94.6 % similarity with respect to the genus Ornithinibacillus, 94.0 % with respect to Paucisalibacillus, 91.0–93.5 % with respect to Virgibacillus, 93.2–93.3 % with respect to Salinibacillus and 92.8–93.2 % with respect to Oceanobacillus. The optimum temperature and pH for growth were 30 °C and pH 7.5. Strain CL-GR16T was able to grow at NaCl concentrations from 0 to 14 %, with optimum growth occurring at 0–2 % NaCl. The strain lacked oxidase. The major fatty acids were anteiso-C15 : 0 (65.6 %), anteiso-C17 : 0 (11.0 %) and iso-C15 : 0 (9.1 %). The polar lipids were diphosphatidylglycerol, phosphatidylglycerol and an unidentified glycolipid. The predominant menaquinone was MK-7. The G+C content of the DNA was 43 mol%. On the basis of the results of the polyphasic analysis, strain CL-GR16T represents a novel genus and species, for which the name Pelagibacillus goriensis gen. nov., sp. nov. is proposed. The type strain is strain CL-GR16T (=KCCM 42329T=DSM 18252T).

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain CL-GR16T is DQ519571.

The whole-cell fatty acid composition of strain CL-GR16T and related species, and a two-dimensional thin-layer chromatogram of the polar lipids of strain CL-GR16T are available as supplementary data with the online version of this paper.


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Gram-positive, endospore-forming bacteria that have halophilic/halotolerant/alkaliphilic and/or alkalitolerant properties have often been isolated from various saline habitats. Most of these bacteria were originally classified as belonging to the genus Bacillus, e.g. Bacillus halophilus, Bacillus marinus, Bacillus marismortui, Bacillus salexigens, Bacillus dipsosauri and Bacillus pantothenticus (Arahal et al., 1999Go; Claus & Berkeley, 1986Go; Garabito et al., 1997Go; Ventosa et al., 1989Go). On the basis of 16S rRNA gene sequence comparisons and phenotypic data, however, they have been reclassified as members of novel genera such as Halobacillus (Spring et al., 1996Go), Gracilibacillus (Wainø et al., 1999Go), Virgibacillus (Heyndrickx et al., 1999Go), Salibacillus (Wainø et al., 1999Go; Arahal et al., 2000Go) and Alkalibacillus (Jeon et al., 2005aGo). In addition, novel genera whose members have halophilic/halotolerant/alkaliphilic and/or alkalitolerant properties have been proposed, such as Oceanobacillus (Lu et al., 2001Go), Filobacillus (Schlesner et al., 2001Go), Lentibacillus (Yoon et al., 2002Go), Paraliobacillus (Ishikawa et al., 2002Go), Tenuibacillus (Ren & Zhou, 2005aGo), Pontibacillus (Lim et al., 2005Go), Salinibacillus (Ren & Zhou, 2005bGo), Thalassobacillus (García et al., 2005Go), Halolactibacillus (Ishikawa et al., 2005Go), Ornithinibacillus (Mayr et al., 2006Go) and Paucisalibacillus (Nunes et al., 2006Go). In particular, these bacteria constitute a considerably large phylogenetic group within Bacillus rRNA group 1 (Ash et al., 1991Go), which is a phyletic assemblage of bacteria classically defined as the genus Bacillus. Most of the species of this phylogenetic group were isolated from saline or hypersaline environments, e.g. mud from a deep-sea ridge, beach sediment, salt fields, salt lakes, solar salterns, hypersaline soils and decaying marine algae. We isolated a Gram-positive, endospore-forming, moderately halotolerant bacterial strain, CL-GR16T, from coastal water off the east coast of Korea. According to the results of a phylogenetic analysis, the novel isolate was found to belong to Bacillus rRNA group 1 (Bacillus sensu stricto).

A coastal water sample was incubated with sand sediment in a glass Petri dish for 5 months at room temperature. Without disturbing the sediment, 100 µl of surficial seawater was spread on a plate containing R2A agar (Difco) supplemented with 3 % (w/v) NaCl; the plate was then incubated at 25 °C for 5 days. The strain was able to grow on marine agar 2216 (MA; Difco) and subsequently purified four times on MA at 30 °C. The strain was maintained both on MA at 4 °C and in marine broth 2216 (Difco) supplemented with 30 % (v/v) glycerol at –80 °C.

The almost complete 16S rRNA gene was amplified from a single colony by performing a PCR with Taq DNA polymerase (Bioneer) and primers 27F and 1492R (Lane, 1991Go). The PCR product was purified using an AccuPrep PCR purification kit (Bioneer). Sequencing of the 16S rRNA gene was performed with an Applied Biosystems automatic sequencer (ABI3730XL) at Macrogen Corp. (Seoul, Korea). The almost-complete 16S rRNA gene sequence of the strain (1433 bp) obtained was compared with 16S rRNA gene sequences available in GenBank by using BLASTN searches (Altschul et al., 1990Go). The 16S rRNA gene sequence was manually aligned against those of members of the family Bacillaceae by using the JPHYDIT program (Jeon et al., 2005bGo). Phylogenetic trees were obtained by using the neighbour-joining (Saitou & Nei, 1987Go), maximum-parsimony (Fitch, 1971Go) and maximum-likelihood (Felsenstein, 1981Go) methods. An evolutionary distance matrix for the neighbour-joining method was generated according to the model of Jukes & Cantor (1969)Go. The robustness of the tree topologies obtained was assessed by performing bootstrap analyses based on 1000 replications (neighbour-joining and maximum-parsimony) or 100 replications (maximum-likelihood). Phylogenetic analyses were carried out using MEGA3 (Kumar et al., 2004Go) and PAUP* 4.0 (Swofford, 1998Go). Likelihood parameters were estimated by using the hierarchical ratio tests in MODELTEST, version 3.04 (Posada & Crandall, 1998Go). The phylogenetic analysis of the 16S rRNA gene sequences revealed that the isolate represented an independent lineage within Bacillus rRNA group 1, showing 93.6–94.6 % similarity with respect to the genus Ornithinibacillus, 94.0 % with respect to Paucisalibacillus, 91.0–93.5 % with respect to Virgibacillus, 93.2–93.3 % with respect to Salinibacillus and 92.8–93.2 % with respect to Oceanobacillus (Fig. 1Go). The DNA G+C content, determined at the Korean Culture Center of Microorganisms (Seoul, Korea) by performing HPLC analysis (Tamaoka & Komagata, 1984Go), was found to be 43 mol%.


Figure 1
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  		Fig. 1. Neighbour-joining phylogenetic tree, based on 16S rRNA gene sequences, showing the position of strain CL-GR16T with respect to related taxa. Only bootstrap values above 60 % (based on 1000 resamplings) are shown at the branching points. Solid circles indicate that the corresponding nodes were also obtained in the maximum-likelihood and maximum-parsimony trees. Alicyclobacillus acidoterrestris (AJ133631) was used as an outgroup. Bar, 0.01 nucleotide substitution per site.

 
For phenotypic and chemotaxonomic analyses, strain CL-GR16T was routinely cultivated on PYA medium (1 % peptone, 0.5 % yeast extract, 0.1 % K2HPO4, 0.02 % MgSO4.7H2O, 1.5 % Bacto agar, pH 7.5; Lu et al., 2001Go). Gram-staining was performed as described by Smibert & Krieg (1994)Go. Cell morphology was examined by performing phase-contrast microscopy and transmission electron microscopy (EX2; JEOL) with cells grown in a 2-day culture at 30 °C on a PYA agar plate. Anaerobic growth was checked on PYA using the GasPak anaerobic system (BBL) for 40 days. Strain CL-GR16T was unable to grow under anaerobic conditions. The hydrolysis of casein, DNA and Tweens 40, 60 and 80, and catalase and oxidase activities were determined according to the protocols described in Cowan & Steel's manual (Barrow & Feltham, 1993Go). Other enzyme activities were assayed by using the API 20NE and API 20E kits (bioMérieux) according to the manufacturer's instructions. Acid production from different carbohydrates was determined by employing the API 50CH system (bioMérieux) according to the manufacturer's instructions. For the API 20NE, API 20E and API 50CH system analyses, Oceanobacillus iheyensis KCTC 3954T was employed as a reference strain. Growth-temperature experiments were performed using PYA broth (the same composition as PYA but without the agar). PYA broth and PYA broth containing 100 mM NaHCO3/Na2CO3 were used for growth experiments performed at pH 5.0–8.5 and pH 9.0–10.5, respectively. Final pHs were adjusted with HCl or NaOH solution. The NaCl concentrations allowing growth of strain CL-GR16T were determined by using PYA broth supplemented with NaCl at various concentrations (0, 1, 2, 3, 5, 7, 8, 10, 13, 15, 18, 20, 21, 22 and 25 %, w/v; pH 7.5). All media (irrespective of pH value and NaCl concentration) were sterilized with sterile 0.22 µm pore-size syringe filters (Advantec MFS). Growth at different pHs, NaCl concentrations and temperatures was measured by monitoring changes in the OD600 over time. Carbon-source utilization was tested on basal agar medium supplemented with yeast extract (NaCl, 23.6 g; KCl, 0.64 g; MgCl2.6H2O, 4.53 g; MgSO4.7H2O, 5.94 g; CaCl2.2H2O, 1.3 g; NaNO3, 0.2 g; NH4Cl, 0.2 g; Bacto agar 15 g; yeast extract, 0.05 g; distilled water, 1 l; Choi & Cho, 2006Go) and containing 0.2 % carbon source. Growth was scored as negative when it was equal to, or less than, that in the negative control (which lacked any carbon source), after 15 days incubation at 30 °C. All of the experiments were performed under aerobic conditions. Electron microscopy revealed that the cells of strain CL-GR16T were peritrichously flagellated rods approximately 0.4–0.7 µm wide and 1.5–4 µm long. The cells of strain CL-GR16T were revealed to be Gram-positive and to produce ellipsoidal spores positioned subterminally and centrally within swollen sporangia.

Isoprenoid quinones were investigated according to Minnikin et al. (1984)Go and analysed by HPLC as described by Collins (1985)Go. The fatty acid methyl esters present in whole cells grown on MA at 30 °C for 2 days were analysed by GC, according to the instructions of the Microbial Identification System (MIDI), at the Korean Culture Center of Microorganisms. Polar lipids were extracted using the procedures described by Minnikin et al. (1984)Go and identified by two-dimensional TLC followed by spraying with appropriate detection reagents (Komagata & Suzuki, 1987Go). The major isoprenoid quinone in strain CL-GR16T was MK-7. The major fatty acids were anteiso-C15 : 0 (65.6 %), anteiso-C17 : 0 (11.0 %) and iso-C15 : 0 (9.1 %) (see supplementary Table S1, available with the online version of this paper). The cellular polar lipids found in strain CL-GR16T were diphosphatidylglycerol, phosphatidylglycerol and an unidentified glycolipid (see supplementary Fig. S1, available with the online version of this paper).

Although strain CL-GR16T was most closely related to the genera Ornithinibacillus (93.6–94.6 %), Paucisalibacillus (94.0 %), Virgibacillus (91.0–93.5 %), Salinibacillus (93.2–93.3 %) and Oceanobacillus (92.8–93.2 %), the phylogenetic analysis of the 16S rRNA gene sequences revealed that the isolate did not form a robust clade with these closely related species (Fig. 1Go). There was a difference between the DNA G+C content of strain CL-GR16T (43 mol%) and that for the genus Paucisalibacillus (38 mol%). Furthermore, the presence of an unidentified glycolipid distinguished strain CL-GR16T from the genera Virgibacillus and Ornithinibacillus (Table 1Go). The fatty acid profile of strain CL-GR16T also differed from that of the genus Ornithinibacillus in terms of the proportions of the major fatty acids (iso-C15 : 0 and anteiso-C15 : 0) (see Table S1). The NaCl concentrations associated with optimal growth clearly distinguished strain CL-GR16T from the closely related genera Virgibacillus, Salinibacillus and Oceanobacillus (Table 1Go). For the genera Virgibacillus, Salinibacillus and Oceanobacillus, optimal growth occurs at NaCl concentrations 3–10, 10–15 and 3–10 %, respectively; for strain CL-GR16T, optimal growth was maintained at 0–2 % NaCl, was reduced by the further addition of NaCl, and did not occur at all at 15 % NaCl (Table 1Go). Furthermore, strain CL-GR16T can be differentiated from the genus Ornithinibacillus with reference to some phenotypic traits (hydrolysis of aesculin and starch, acid production from D-mannose and utilization of D-xylose); in addition, acid production from D-melibiose distinguishes strain CL-GR16T from the genera Ornithinibacillus, Paucisalibacillus and Virgibacillus. The utilization patterns for some carbon sources (D-glucose, D-fructose and sucrose) also serve to differentiate strain CL-GR16T from the genera Paucisalibacillus and Salinibacillus (Table 1Go). In conclusion, on the basis of the polyphasic data presented, strain CL-GR16T represents a novel genus and species, for which the name Pelagibacillus goriensis gen. nov., sp. nov. is proposed.


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  		Table 1. Differential phenotypic characteristics of strain CL-GR16T and related species

Taxa: 1, strain CL-GR16T; 2, Ornithinibacillus bavariensis (Mayr et al., 2006Go); 3, Ornithinibacillus californiensis (Mayr et al., 2006Go); 4, Paucisalibacillus globulus (Nunes et al., 2006Go); 5, Virgibacillus koreensis (Lee et al., 2006Go); 6, Virgibacillus carmonensis (Heyrman et al., 2003Go); 7, Virgibacillus halodenitrificans (Yoon et al., 2004Go); 8, Virgibacillus marismortui (Arahal et al., 1999Go, 2000Go; Heyrman et al., 2003Go); 9, Virgibacillus proomii (Heyndrickx et al., 1999Go; Heyrman et al., 2003Go); 10, Virgibacillus pantothenticus (Heyndrickx et al., 1999Go; Heyrman et al., 2003Go); 11, Virgibacillus dokdonensis (Yoon et al., 2005Go); 12, Virgibacillus necropolis (Heyrman et al., 2003Go); 13, Virgibacillus salexigens (Garabito et al., 1997Go; Wainø et al., 1999Go; Heyrman et al., 2003Go); 14, Salinibacillus aidingensis (Ren & Zhou, 2005bGo); 15, Salinibacillus kushneri (Ren & Zhou, 2005bGo); 16, Oceanobacillus iheyensis (Lu et al., 2001Go; Mayr et al., 2006Go); 17, Oceanobacillus picturae (Heyrman et al., 2003Go; Lee et al., 2006Go); 18, Oceanobacillus oncorhynchi (Yumoto et al., 2005Go). The cells of all of the species are rod-shaped, motile and positive for catalase. +, Positive; –, negative; V, variable; W, weakly positive; ?, unclear result; ND, not determined.

 
Description of Pelagibacillus gen. nov.
Pelagibacillus (Pe.la'gi.ba.cil'lus. L. n. pelagus the sea; L. dim. n. bacillus small rod; N.L. masc. n. Pelagibacillus bacillus pertaining to the sea).

Cells are Gram-positive, obligately aerobic, spore-forming rods and are motile by means of peritrichous flagella. Moderately halotolerant. Negative for oxidase. The predominant menaquinone is MK-7. The major fatty acids are anteiso-C15 : 0, anteiso-C17 : 0 and iso-C15 : 0. The cellular polar lipids are diphosphatidylglycerol, phosphatidylglycerol and an unidentified glycolipid. The type species is Pelagibacillus goriensis.

Description of Pelagibacillus goriensis sp. nov.
Pelagibacillus goriensis (go.ri.en'sis. N.L. masc. adj. goriensis from Gori, where the type strain was isolated).

Exhibits the following properties in addition to those given in the genus description. Cells are 0.4–0.7 µm wide and 1.5–4.0 µm long. Cells produce ellipsoidal spores subterminally or centrally positioned within swollen sporangia. Colonies are circular, creamy white in colour and 3–5 mm in diameter on PYA plates after cultivation for 1 day. The optimum NaCl concentration for growth is 0–2 % (w/v), with a range of 0–14 % (at pH 7.5). Growth is observed within the temperature range 15–43 °C (optimum, 30 °C), at pH values between 5.5 and 9 (optimum, pH 7.5). Hydrolyses casein, Tweens 40, 60 and 80 and starch and is catalase- and DNase-positive. According to the API 20NE system, hydrolysis of aesculin, gelatin and PNPG (beta-galactosidase activity) occur, but indole is not produced and urease, arginine dihydrolase and nitrate reductase activities are absent. According to the API 20E system, hydrolysis of gelatin and ONPG (beta-galactosidase activity) occur, but arginine dihydrolase, lysine decarboxylase, citrate utilization, H2S production, urease, tryptophan deaminase, indole production and acetoin production (Voges–Proskauer reaction) are absent. According to the API 50 CH system, acids are produced from D-cellobiose, D-fructose, D-galactose, D-glucose, D-lactose, D-mannitol, D-mannose, D-melibiose, D-raffinose, D-trehalose, aesculin, glycerol, L-rhamnose, N-acetylglucosamine, amygdalin, salicin, arbutin, gentiobiose, D-tagatose and sucrose, but not from erythritol, adonitol, methyl beta-D-xyloside, L-sorbose, dulcitol, methyl {alpha}-D-mannoside, methyl {alpha}-D-glucoside, melezitose, starch, glycogen, xylitol, D-turanose, L-lyxose, DL-fucose, gluconate, 2-ketogluconate, 5-ketogluconate, DL-arabinose, D-ribose, DL-xylose, inositol, D-sorbitol, D-maltose or inulin. Utilizes citrate, D-cellobiose, D-galactose, D-mannose, D-raffinose, D-salicin, D-trehalose, D-xylose, lactose, L-ascorbate, L-rhamnose, N-acetylglucosamine and pyruvic acid as sole carbon sources, but not acetate, {alpha}-ketobutyric acid, benzoate, DL-cysteine, D-fructose, D-glucose, D-mannitol, D-ribose, D-sorbitol, glycerol, glycine, glycogen, myo-inositol, inulin, L-arabinose, L-arginine, L-asparagine, L-lysine, L-ornithine, L-proline, succinate, sucrose or tartrate. The DNA G+C content is 43 mol%.

The type strain, CL-GR16T (=KCCM 42329T=DSM 18252T), was isolated from coastal water off the east coast of Korea.


   ACKNOWLEDGEMENTS
 
This work was supported, in part, by the BK21 project of the Korean Government and a project (A04NJ08) of the Korea Hydro & Nuclear Power Co. Ltd.


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