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Department of Biological Sciences, Korea Advanced Institute of Science and Technology, 373-1 Guseong-dong, Yuseong-gu, Daejeon 305-701, Republic of Korea
Correspondence
Sung-Taik Lee
e_stlee{at}kaist.ac.kr
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ABSTRACT |
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7c, C16 : 0 and either summed feature 4 (C16 : 17c/C15 : 0 iso 2-OH) or C19 : 0 cyclo 8c as the major fatty acids. Phylogenetic analysis, based on 16S rRNA gene sequencing, showed that the ten isolates formed four separate lineages in the genus Halomonas. Combined phenotypic data and DNA–DNA hybridization data supported the conclusion that they represent four novel species in the genus Halomonas, for which the names Halomonas gomseomensis sp. nov. (type strain M12T=KCTC 12662T=DSM 18042T), Halomonas janggokensis sp. nov. (type strain M24T=KCTC 12663T=DSM 18043T), Halomonas salaria sp. nov. (type strain M27T=KCTC 12664T=DSM 18044T) and Halomonas denitrificans sp. nov. (type strain M29T=KCTC 12665T=DSM 18045T) are proposed.
Transmission electron micrographs of cells of strains M12T, M24T, M27T and M29T, detailed DNA–DNA hybridization results and results of API ZYM tests are available as supplementary material in IJSEM Online.
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, b; Franzmann et al., 1988). Nearly one-third of the species within the family Halomonadaceae have undergone taxonomic changes (Arahal et al., 2001, 2002a; Dobson & Franzmann, 1996; Mellado et al., 1995) and, recently, [Pseudomonas] beijerinckii has been reclassified as Chromohalobacter beijerinckii (Peçonek et al., 2006). Nevertheless, the taxonomic status of some taxa, e.g. Cobetia marina and Halomonas marisflavi, is still in doubt.
The members of genus Halomonas are moderately halophilic bacteria, and the genus contains 35 recognized species. The type species is Halomonas elongata. Recently, Halomonas almeriensis (Martínez-Checa et al., 2005), Halomonas campaniensis (Romano et al., 2005) and Halomonas taeanensis (Lee et al., 2005) have been described. During the screening of salt-loving bacteria that might be applied to the bioremediation of saline environments, we isolated 34 Halomonas strains from saline samples of sea and solar salterns in Anmyeondo, ten strains of which were considered to belong to novel species in the genus Halomonas and were subjected to a polyphasic taxonomic investigation.
Strains M12T and M59 were isolated from saline water of Gomseom solar saltern, strains M24T and M58 were isolated from saline water of Janggok solar saltern and strains M27T, M66, M67, M29T, M69 and M70 were isolated from seawater in Anmyeondo. For most experiments, strains were cultured on marine agar or broth (Difco) containing 10 % NaCl at 28 °C for 48 h. When strains were cultured on other complex media for phenotypic tests, the final NaCl concentration was adjusted to 10 %.
The Gram reaction was performed as described by Gerhardt et al. (1994). Cell morphology and motility was observed under a phase-contrast microscope (Nikon Optiphot; x1000 magnification) with cells grown for 1–7 days, and the presence of flagella was determined by transmission electron microscopy (JEM-10111; JEOL) after negative staining with 2 % (w/v) uranyl acetate. Oxidase activity was tested using 1 % tetramethyl-p-phenylenediamine (Tarrand & Groschel, 1982) and catalase activity was tested using 3 % H2O2. Growth was investigated at temperatures ranging from 5 to 55 °C at intervals of 5 °C and at pH 4–11 at intervals of 1 pH unit. Requirement for and tolerance of NaCl were determined in nutrient broth (Difco) supplemented with modified artificial seawater [containing (l–1): 0–30 (0, 0.5, 1, 2, 4, 6, 8, 10, 12, 15, 20, 25 and 30) % NaCl, 5.94 g MgSO4.7H2O, 4.53 g MgCl2.6H2O, 0.64 g KCl and 1.3 g CaCl2; Lee et al., 2005]. Hydrolysis of casein and starch was tested on casein agar and starch agar (Difco). The H2S production test was performed on triple-sugar-iron agar (BBL). Carbon source utilization tests, acid production tests and additional physiological tests were performed using API 20NE, API 32GN, API 50CH and API ZYM galleries according to the instructions of the manufacturer (bioMérieux).
For the analysis of fatty acids, strains were cultured on tryptic soy agar (TSA; Difco) containing 10 % NaCl at 28 °C for 48 h. Halomonas anticariensis LMG 22089T, Halomonas cupida DSM 4740T, Halomonas desiderata DSM 9502T, Halomonas hydrothermalis DSM 15725T, Halomonas maura DSM 13445T, Halomonas sulfidaeris DSM 15722T, Halomonas ventosae DSM 15911T, Halomonas venusta DSM 4743T and Chromohalobacter marismortui DSM 6770T were used as reference strains under the same conditions.
Fatty acid methyl esters were prepared and analysed as described previously (Klatte et al., 1994) using the standard Microbial Identification System (MIDI Inc.) for automated gas chromatographic analysis (Sasser, 1990; Kämpfer & Kroppenstedt, 1996). Isoprenoid quinones were extracted and purified as described previously (Tindall, 1990); dried preparations were dissolved in 200 µl 2-propanol and 1–10 µl samples were separated by HPLC without further purification.
Extraction of genomic DNA, PCR-mediated amplification of the 16S rRNA genes and sequencing of purified PCR products were carried out according to Rainey et al. (1996). The 16S rRNA gene sequences were aligned with published sequences retrieved from EMBL using CLUSTAL X (Thompson et al., 1997) and edited using BioEdit (Hall, 1999). Phylogenetic trees were constructed on the basis of the neighbour-joining (Saitou & Nei, 1987) and maximum-parsimony (Fitch, 1971) methods; distances were estimated by the method of Jukes & Cantor (1969) using MEGA version 2.1 (Kumar et al., 2001). The resultant tree topologies were evaluated by bootstrap analysis (Felsenstein, 1985) based on 1000 resampled datasets. DNA G+C contents were determined by HPLC after hydrolysis as described by Tamaoka & Komagata (1984) and non-methylated 
DNA (Sigma) was used as a standard. DNA–DNA hybridization to determine genomic relatedness was performed fluorometrically by the method of Ezaki et al. (1989) using DNA probes labelled with photobiotin (Sigma; A1935) and microdilution wells (Greiner Bio-one; 96-well microplate).
The novel Halomonas strains formed visible colonies (0.5–1.5 mm diameter) on marine agar with 10 % NaCl at 28 °C within 48 h. Good growth occurred at temperatures ranging from 15 to 40 °C. The colonies were convex, translucent and circular with entire edges. Cells were aerobic, Gram-negative, catalase-positive, non-spore-forming rods and were motile with peritrichous or lateral/polar flagella. Transmission electron micrographs of cells of strains M12T, M24T, M27T and M29T are available as Supplementary Fig. S1 in IJSEM Online. Detailed physiological and biochemical characteristics are summarized in Table 1 and in the species descriptions.
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7c, C16 : 0 and summed feature 4 (C16 : 17c/C15 : 0 iso 2-OH) were predominant. Strain M27T showed a slightly different profile; C18 : 17c, C16 : 0 and C19 : 0 cyclo 8c were predominant. Detailed fatty acid compositions are shown in Table 2.
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Combined phenotypic and genotypic data support that the ten novel strains represent four novel species in the genus Halomonas, for which the names Halomonas gomseomensis sp. nov., Halomonas janggokensis sp. nov., Halomonas salaria sp. nov. and Halomonas denitrificans sp. nov. are proposed.
Description of Halomonas gomseomensis sp. nov.
Halomonas gomseomensis (gom.se.om.en'sis. N.L. fem. adj. gomseomensis referring to Gomseom in Anmyeondo, from where the first strains were isolated).
Cells are aerobic, Gram-negative, non-spore-forming rods (0.6–0.8x1.8–2.4 µm). Colonies are cream–beige, smooth, translucent and circular with entire edges and stick slightly to solid media. Cells are motile with peritrichous flagella. Oxidase-negative and catalase-positive. Growth occurs at 5–45 °C (optimum 25–30 °C) and at pH 6–10 (optimum pH 7–8). Growth occurs at salinities of 1–20 % NaCl (optimum 8–12 % NaCl). Indole and H2S are not produced. Voges–Proskauer test is negative. Nitrate and nitrite are not reduced. Aesculin and DNA are hydrolysed, but casein, gelatin, starch, Tween 80 and urea are not. Acid is produced from glycerol, D-arabinose, L-arabinose, D-xylose, galactose, glucose, fructose, mannose, inositol, arbutin, aesculin, maltose, sucrose, trehalose, D-turanose, D-fucose and L-fucose, but not from erythritol, ribose, L-xylose, adonitol, methyl 
-D-xylose, sorbose, rhamnose, dulcitol, mannitol, sorbitol, methyl 
-D-mannoside, methyl -D-glucoside, N-acetylglucosamine, amygdalin, salicin, cellobiose, lactose, melibiose, inulin, melezitose, raffinose, starch, glycogen, xylitol, gentiobiose, D-lyxose, D-tagatose, D-arabitol, L-arabitol, gluconate, 2-ketogluconate and 5-ketogluconate. The following compounds are utilized as sole carbon sources: D-glucose, N-acetylglucosamine, salicin, inositol, L-fucose, sucrose, maltose, L-arabinose, gluconate, propionate, malate, malonate, valerate, acetate, citrate, DL-lactate, histidine, L-alanine, 2-ketogluconate, 3-hydroxybutyrate, 4-hydroxybenzoate and L-proline. The following carbon sources are not utilized: mannitol, rhamnose, D-ribose, D-melibiose, mannose, D-sorbitol, itaconate, suberate, adipate, caprate, phenylacetate, 5-ketogluconate, glycogen, 3-hydroxybenzoate and L-serine. Results from API ZYM tests are available in Supplementary Table S2 in IJSEM Online. The predominant quinone is ubiquinone Q-9; a small amount of Q-8 is also present. The fatty acids C18 : 17c, C16 : 0 and C16 : 17c/C15 : 0 iso 2-OH are predominant. The G+C content of the DNA is 62.0–63.6 mol% (62.0 mol% for the type strain).
The type strain is M12T (=KCTC 12662T=DSM 18042T), isolated from saline water of Gomseom solar saltern in Anmyeondo, Korea.
Description of Halomonas janggokensis sp. nov.
Halomonas janggokensis (jang.gok.en'sis. N.L. fem. adj. janggokensis referring to Janggok in Anmyeondo, from where the first strains were isolated).
Cells are aerobic, Gram-negative, non-spore-forming rods (0.5–0.7x1.6–2.0 µm). Colonies are white, smooth, translucent and circular with entire edges. Cells are motile with peritrichous flagella. Oxidase-negative and catalase-positive. Growth occurs at 5–45 °C (optimum 25–30 °C) and at pH 6–10 (optimum pH 7–8). Growth occurs at salinities of 1–20 % NaCl (optimum 10–15 % NaCl). Indole and H2S are not produced. Voges–Proskauer test is negative. Nitrate and nitrite are not reduced. DNA is hydrolysed, but aesculin, casein, gelatin, starch, Tween 80 and urea are not. Acid is produced from glycerol, L-arabinose, adonitol, galactose, glucose, fructose, mannitol, sorbitol, maltose, sucrose, trehalose, xylitol, D-turanose, D-fucose, D-arabitol and L-arabitol, but not from erythritol, D-arabinose, ribose, D-xylose, L-xylose, methyl -D-xylose, mannose, sorbose, rhamnose, dulcitol, inositol, methyl -D-mannoside, methyl -D-glucoside, N-acetylglucosamine, amygdalin, arbutin, aesculin, salicin, cellobiose, lactose, melibiose, inulin, melezitose, raffinose, starch, glycogen, gentiobiose, D-lyxose, D-tagatose, L-fucose, gluconate, 2-ketogluconate and 5-ketogluconate. The following compounds are utilized as sole carbon sources: mannitol, D-glucose, inositol, sucrose, maltose, D-sorbitol, L-arabinose, gluconate, propionate, malate, malonate, valerate, acetate, adipate, citrate, DL-lactate, L-alanine, 2-ketogluconate, 3-hydroxybutyrate and L-proline. The following carbon sources are not utilized: rhamnose, N-acetylglucosamine, salicin, D-ribose, D-melibiose, L-fucose, mannose, itaconate, suberate, caprate, histidine, phenylacetate, 5-ketogluconate, glycogen, 4-hydroxybenzoate, 3-hydroxybenzoate and L-serine. Results from API ZYM tests are available as Supplementary Table S2. The predominant quinone is ubiquinone Q-9; a small amount of Q-8 is also present. The fatty acids C18 : 17c, C16 : 0 and C16 : 17c/C15 : 0 iso 2-OH are predominant. The G+C content of the DNA is 60.2–61.0 mol% (61.0 mol% for the type strain).
The type strain is M24T (=KCTC 12663T=DSM 18043T), isolated from saline water of Janggok solar saltern in Anmyeondo, Korea.
Description of Halomonas salaria sp. nov.
Halomonas salaria (sa.la'ri.a. L. fem. adj. salaria of or belonging to salt).
Cells are aerobic, Gram-negative, non-spore-forming rods (0.8–0.9x1.3–1.7 µm). Colonies are yellow, smooth, translucent and circular with entire edges. Cells are motile with lateral/polar flagella. Oxidase-positive and catalase-positive. Growth occurs at 10–45 °C (optimum 25–30 °C) and at pH 5–10 (optimum pH 7–8). Growth occurs at salinities of 0–25 % NaCl (optimum 10–20 % NaCl). Indole and H2S are not produced. Voges–Proskauer test is negative. Nitrate is reduced, but nitrite is not reduced. Casein and DNA are hydrolysed, but aesculin, gelatin, starch, Tween 80 and urea are not. Acid is produced from glycerol, erythritol, L-arabinose, ribose, D-xylose, galactose, glucose, fructose, mannose, rhamnose, mannitol, cellobiose, maltose, lactose, melibiose, trehalose, D-lyxose, D-fucose and D-arabitol, but not from D-arabinose, L-xylose, adonitol, methyl -D-xylose, sorbose, dulcitol, inositol, sorbitol, methyl -D-mannoside, methyl -D-glucoside, N-acetylglucosamine, amygdalin, arbutin, aesculin, salicin, sucrose, inulin, melezitose, raffinose, starch, glycogen, xylitol, gentiobiose, D-turanose, D-tagatose, L-fucose, L-arabitol, gluconate, 2-ketogluconate and 5-ketogluconate. The following compounds are utilized as sole carbon sources: mannitol, D-glucose, D-ribose, L-fucose, maltose, mannose, L-arabinose, itaconate, gluconate, propionate, malate, valerate, acetate, adipate, citrate, DL-lactate, 2-ketogluconate, 5-ketogluconate, L-proline and L-serine. The following carbon sources are not utilized: rhamnose, N-acetylglucosamine, salicin, D-melibiose, inositol, sucrose, D-sorbitol, suberate, caprate, malonate, phenylacetate, histidine, L-alanine, 3-hydroxybutyrate, glycogen, 4-hydroxybenzoate and 3-hydroxybenzoate. Results from API ZYM tests are available as Supplementary Table S2. The predominant quinone is ubiquinone Q-9; a small amount of Q-8 is also present. The fatty acids C18 : 17c, C16 : 0 and C19 : 0 cyclo 8c are predominant. The G+C content of the DNA is 58.8–60.1 mol% (58.8 mol% for the type strain).
The type strain is M27T (=KCTC 12664T=DSM 18044T), isolated from seawater in Anmyeondo, Korea.
Description of Halomonas denitrificans sp. nov.
Halomonas denitrificans (de.ni.tri'fi.cans. N.L. v. denitrifico to denitrify; N.L. part. adj. denitrificans denitrifying).
Cells are aerobic, Gram-negative, non-spore-forming rods (0.6–0.8x1.2–1.6 µm). Colonies are brown–yellow, smooth, translucent and circular with entire edges. Cells are motile with peritrichous flagella. Oxidase-positive and catalase-positive. Growth occurs at 5–50 °C (optimum 25–35 °C) and at pH 7–10 (optimum pH 8–9). Growth occurs at salinities of 2–20 % NaCl (optimum 8–10 % NaCl). Indole and H2S are not produced. Voges–Proskauer test is negative. Nitrate and nitrite are reduced. Aesculin, casein, DNA, gelatin, starch, Tween 80 and urea are not hydrolysed. Acid is produced from fructose, but not from glycerol, erythritol, D-arabinose, L-arabinose, ribose, D-xylose, L-xylose, adonitol, methyl -D-xylose, galactose, glucose, mannose, sorbose, rhamnose, dulcitol, inositol, mannitol, sorbitol, methyl -D-mannoside, methyl -D-glucoside, N-acetylglucosamine, amygdalin, arbutin, aesculin, salicin, cellobiose, maltose, lactose, melibiose, sucrose, trehalose, inulin, melezitose, raffinose, starch, glycogen, xylitol, gentiobiose, D-turanose, D-lyxose, D-tagatose, D-fucose, L-fucose, D-arabitol, L-arabitol, gluconate, 2-ketogluconate and 5-ketogluconate. The following compounds are utilized as sole carbon sources: propionate, malate, valerate, malonate, acetate, citrate, DL-lactate, L-alanine, 3-hydroxybutyrate, L-proline and L-serine. The following carbon sources are not utilized: mannitol, D-glucose, rhamnose, N-acetylglucosamine, salicin, D-ribose, D-melibiose, inositol, L-fucose, sucrose, D-sorbitol, maltose, mannose, L-arabinose, itaconate, suberate, adipate, caprate, gluconate, phenylacetate, histidine, 2-ketogluconate, 5-ketogluconate, glycogen, 4-hydroxybenzoate and 3-hydroxybenzoate. Results from API ZYM tests are available as Supplementary Table S2. The predominant quinone is ubiquinone Q-9; a small amount of Q-8 is also present. The fatty acids C18 : 17c, C16 : 0 and C16 : 17c/C15 : 0 iso 2-OH are predominant. The G+C content of the DNA is 53.8–55.2 mol% (53.8 mol% for the type strain).
The type strain is M29T (=KCTC 12665T=DSM 18045T), isolated from seawater in Anmyeondo, Korea.
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ACKNOWLEDGEMENTS |
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