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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
Correspondence
Byung Cheol Cho
bccho{at}snu.ac.kr
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ABSTRACT |
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7c (48.5 %), C16 : 0 (14.8 %), C17 : 0 (12.2 %), C19 : 0 cyclo 8c (6.3 %) and summed feature 3 (C16 : 17c and/or iso-C15 : 0 2-OH, 6.0 %). Among the phylogenetically related genera, the fatty acid C17 : 0 was found only in strain CL-GR58T. The DNA G+C content of the novel strain was 68.0 mol%. According to phylogenetic analyses of the 16S rRNA gene sequence, fatty acid content and the physiological data, strain CL-GR58T represents a novel species in a new genus of the family Rhodospirillaceae, for which the name Thalassobaculum litoreum gen. nov., sp. nov. is proposed. The type strain of the type species is CL-GR58T (=KCCM 42674T=DSM 18839T).
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) of the class Alphaproteobacteria, currently comprises 14 genera (http://www.bacterio.cict.fr). Members of the family Rhodospirillaceae exhibit a variety of modes of growth: the genera Rhodovibrio and Phaeospirillum and some species in three other genera (i.e. Rhodocista centenaria, Rhodospirillum photometricum and Roseospira marina) are capable of both photo- and chemo-heterotrophic growth under anoxic conditions in the light and under microoxic to oxic conditions in the dark, respectively (Nissen & Dundas, 1984; Mack et al., 1993; Garrity et al., 2005). The other species in the genera Rhodospirillum and Roseospira (i.e. Rhodospirillum rubrum, Roseospira mediosalina and Roseospira navarrensis) are capable of photolithoautotrophic growth (with hydrogen or sulfide as an electron donor) as well as the above growth modes (Guyoneaud et al., 2002; Garrity et al., 2005). Other species in the genus Rhodocista (i.e. Rhodocista pekingensis) can grow photo- and chemolitho-heterotrophically (with hydrogen as an electron donor) under anoxic conditions in the light and under oxic conditions in the dark, respectively (Zhang et al., 2003). The genus Rhodospira is capable of photolitho- (with sulfide as an electron donor) and chemo-heterotrophic growth under anoxic conditions in the light and under microoxic conditions in the dark, respectively (Pfennig et al., 1997). The genus Telmatospirillum is capable of chemoheterotrophic growth under anoxic to microoxic conditions and both chemolithoheterotrophic and lithoautotrophic growth (with hydrogen as an electron donor), under microoxic conditions (Sizova et al., 2007). Furthermore, chemoheterotrophic genera, Azospirillum (except Azospirillum oryzae which can grow chemolithoheterotrophically utilizing hydrogen as an electron donor; Xie & Yokota, 2005), Skermanella, Inquilinus, Tistrella, Thalassospira, Defluviicoccus and Magnetospirillum have been reported (Sly & Stackebrandt, 1999; Coenye et al., 2002; López-López et al., 2002; Shi et al., 2002; Garrity et al., 2005; Maszenan et al., 2005).
Most species in the family Rhodospirillaceae have been isolated from various non-marine habitats such as freshwater, activated sludge biomass, soil and roots of plants and cystic fibrosis patients (Coenye et al., 2002; Garrity et al., 2005). Only limited numbers of members in the family Rhodospirillaceae have been discovered in marine environments (López-López et al., 2002): only five species affiliated with the genera Rhodovibrio (Rhodovibrio salinarum and Rhodovibrio sodomensis; Nissen & Dundas, 1984; Mack et al., 1993) and Thalassospira (Thalassospira lucentensis, Thalassospira profundimaris and Thalassospira xiamenensis, López-López et al., 2002; Liu et al., 2007) in the family Rhodospirillaceae have been isolated from seawater samples.
Here, we describe a chemoheterotrophic bacterium, strain CL-GR58T, isolated from coastal seawater in Gori, Korea. In August 2005, coastal seawater and sediment samples were brought back to the laboratory and incubated in a 150 mm diameter glass Petri dish for around 15 months at room temperature. Without disturbing the sediment, a 100 µl sample of seawater was removed from the surface and spread on a marine agar 2216 (MA; Difco) plate, which was then incubated at 30 °C for 1 week. Strain CL-GR58T was isolated and subsequently purified on MA at 30 °C four times. The strain was maintained both on MA at 30 °C and in marine broth 2216 (MB; Difco) supplemented with 30 % (v/v) glycerol at –80 °C.
The 16S rRNA gene was amplified from a single colony by using PCR with Taq DNA polymerase (Bioneer) and primers 27F and 1492R (Lane, 1991). The PCR product was purified by using the AccuPrep PCR purification kit (Bioneer) and direct sequence determination of the purified 16S rRNA gene was performed with an Applied Biosystems automated sequencer (ABI3730XL) at Macrogen, Seoul, Korea. The almost-complete 16S rRNA gene sequence of strain CL-GR58T (1336 nucleotides) was obtained and compared with available 16S rRNA gene sequences in GenBank using BLASTN searches (Altschul et al., 1990). The sequence of strain CL-GR58T was manually aligned with all available 16S rRNA gene sequences of recognized species in the family Rhodospirillaceae obtained from GenBank and Ribosomal Database Project (Cole et al., 2003) databases using known 16S rRNA secondary structure information. Phylogenetic trees were constructed by neighbour-joining (Saitou & Nei, 1987), maximum-parsimony (Fitch, 1971) and maximum-likelihood (Felsenstein, 1981) methods. An evolutionary distance matrix for the neighbour-joining method was generated according to the model of Jukes & Cantor (1969). The robustness of the tree topologies was assessed by bootstrap analyses based on 1000 replications for the neighbour-joining and maximum-parsimony methods and 100 replications for the maximum-likelihood method. Alignment analysis was carried out using the jPHYDIT program (Jeon et al., 2005) and phylogenetic analyses were carried out using MEGA 3 (Kumar et al., 2004) and PAUP 4.0 (Swofford, 1998). Likelihood parameters were estimated by using the hierarchical ratio test in MODELTEST, version 3.04 (Posada & Crandall, 1998).
The fatty acid methyl esters in whole cells of strain CL-GR58T grown on MA at 30 °C for 5 days were analysed with gas chromatography according to the instructions of the Microbial Identification System (MIDI) at the Korean Culture Center of Microorganisms (KCCM) in Seoul, Korea. The DNA G+C content was analysed by HPLC (HP 100; Hewlett Packard) analysis of deoxyribonucleosides as described by Mesbah et al. (1989), after DNA extraction according to the method of Marmur (1961). Lambda DNA was used as a standard. The quinone system was determined according to Minnikin et al. (1984) and analysed by HPLC as described by Collins (1985).
Morphological and physiological characteristics were determined. Gram-staining was performed as described by Smibert & Krieg (1994). Cell motility was observed by the hanging drop method (Suzuki et al., 2001). Cell morphology and presence of flagella was observed using transmission electron microscopy (EX2; JEOL). Anaerobic growth was checked on MA using the GasPak anaerobic system (BBL). Poly-β-hydroxybutyrate granules were observed by epifluorescence microscopy (BX60; Olympus) after Nile blue A staining (Ostle & Holt, 1982). Bacteriochlorophyll a production was determined in 90 % acetone extracts using a spectrophotometer (Ultraspec 2000; Pharmacia Biotech) for cells that had been grown either in the light or in the dark for 7 days. The temperature range for growth was examined on the basis of colony formation on MA incubated at temperatures ranging from 5 to 40 °C, using increments of 5 °C. The pH range (pH 3–10, using increments of 1 pH unit) for growth was determined by assessing changes in OD600 over the incubation period (up to 7 days) in MB. The final pH was adjusted using 1 M NaOH and 1 M HCl solutions. The tolerance of strain CL-GR58T to sea salts was determined both on the basis of colony formation on synthetic Zobell agar (5 g Bacto peptone, 1 g yeast extract, 0.1 g ferric citrate, 15 g Bacto agar, 1 l distilled water) and assessing changes in OD600 in Zobell broth with various concentrations (0–10 % increments of 1 % and 15 %, w/v) of sea salts (Sigma). Growth in a medium containing NaCl as the sole salt was determined both on the basis of colony formation on synthetic Zobell agar and by assessing changes in OD600 in Zobell broth with different concentrations of NaCl (0–10 % increments of 1 % and 15 %, w/v). The ability to fix dinitrogen was tested, under anoxic conditions, on NFb medium (5.0 g malate, 0.5 g K2HPO4, 0.2 g MgSO4 . 7H2O, 0.1 g NaCl, 0.02 g CaCl2 . 2H2O, 2 ml 0.5 % bromothymol blue in 0.2 M KOH, 1 ml sterile filtered vitamin solution, 2 ml sterile filtered micronutrient solution, 4 ml 1.64 % FeEDTA solution, 4.5 g KOH, 1 l distilled water and 15 g l–1 Bacto agar, at pH 6.8; Eckert et al., 2001), using Azospirillum doebereinerae KCTC 12904T as the reference strain. Further, the presence of the nifH gene fragment was determined by using PCR amplification with specific primers (PolF/PolR; Poly et al., 2001) for both strain CL-GR58T and A. doebereinerae KCTC 12904T. The oxidase and catalase tests were performed according to the protocols described by Smibert & Krieg (1994). Gelatinase, amylase and nitrate reductase activities and degradation of Tween 80 were determined according to Hansen & Sørheim (1991). In addition, other enzyme activities were assayed using the API ZYM kit (bioMérieux) according to the manufacturer's instructions, except that the cell suspension was prepared using artificial seawater (24 g NaCl, 5.1 g MgCl2, 4 g Na2SO4, 1.1 g CaCl2, 0.7 g KCl, 0.2 g NaHCO3, 0.1 g KBr, 0.027 g H3BO3, 0.024 g SrCl2, 0.003 g NaF, 1 l distilled water; Lyman & Fleming, 1940).
Carbon utilization was tested using the basal broth medium supplemented with yeast extract (23.6 g NaCl, 0.64 g KCl, 4.53 g MgCl2 . 6H2O, 5.94 g MgSO4 . 7H2O, 1.3 g CaCl2 . 2H2O, 0.2 g NaNO3, 0.2 g NH4Cl, 0.05 g yeast extract, 1 l distilled water; Bruns et al., 2001) containing 0.4 % carbon source. Strain CL-GR58T was incubated for 4 weeks and carbon utilization was scored as negative when the growth rate was equal to, or less than, that in the negative control with no carbon source. Growth rate was measured by monitoring changes in OD600. Resistance to antibiotics was determined by the disc diffusion plate method (Bauer et al., 1966).
The 16S rRNA gene sequence of strain CL-GR58T showed 90.9 % similarity to the type strains of Azospirillum lipoferum, 89.8 % to Azospirillum oryzae, 89.7 % to Azospirillum canadense, 89.5 % to A. doebereinerae and 79.3–89.5 % to the other type species of the family Rhodospirillaceae. Although strain CL-GR58T was closely related to species of the genus Azospirillum on the basis of 16S rRNA gene sequence similarity, the novel strain was not included in the clade of the genera Azospirillum, Rhodocista or Skermanella (Fig. 1). Further, the lineage of strain CL-GR58T was not associated with any other genera of the family Rhodospirillaceae. Therefore, phylogenetically, strain CL-GR58T should be recognized as representing a distinct genus in the family Rhodospirillaceae.
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7c (48.5 %), C16 : 0 (14.8 %), C17 : 0 (12.2 %), C19 : 0 cyclo 8c (6.3 %), summed feature 3 (iso-C15 : 0 2-OH and/or C16 : 17c, 6.0 %), 11-methyl C18 : 17c (3.0 %), C18 : 0 (2.0 %), C15 : 0 (1.5 %) and an unknown fatty acid (ECL 18.814; 1.4 %) (Table 1). Fatty acid C18 : 17c was commonly found as a major component in strain CL-GR58T and related genera (Table 1); a feature shared by members of the class Alphaproteobacteria (Labrenz et al., 2000). However, a significant amount of C17 : 0 (12.2 %) was only found in strain CL-GR58T and was not found at significant levels in the related genera Azospirillum, Rhodovibrio, Tistrella or Inquilinus (Table 1). Furthermore, the absence of fatty acids C16 : 0 2-OH, C16 : 0 3-OH, C17 : 0 2-OH and C18 : 1 2-OH clearly differentiated strain CL-GR58T from the genera Azospirillum, Tistrella and Inquilinus (Table 1). A significant concentration of C18 : 1 2-OH (15.5–16.1 %) observed in the genera Tistrella and Inquilinus was not detected in strain CL-GR58T or in the genus Rhodovibrio. Absence of fatty acid C19 : 0 cyclo 8c differentiated the genus Rhodovibrio from other related genera. Therefore, the fatty acid pattern of strain CL-GR58T differs distinctly from those of related genera in the family Rhodospirillaceae. The major quinone in strain CL-GR58T was ubiquinone 10 (Q-10), which is also found in the genera Azospirillum, Tistrella and Skermanella; however in the genera Rhodocista and Rhodovibrio, Q-9, and Q-10 and MK-10 were found, respectively (Table 2). The G+C content of the DNA was 68.0 mol% (Table 2).
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- and β-glucosidases and N-acetyl-β-glucosaminidase activities were positive and were weakly positive for esterase lipase (C8), lipase (C14), - and β-galactosidases, -mannosidase and -fucosidase. No activities were found for cystine arylamidase, trypsin, -chymotrypsin and β-glucuronidase. Growth occurred on D-ribose, sucrose, L-arabinose and yeast extract. No growth occurred on acetate, -ketobutyric acid, citrate, fructose, galactose, glucose, mannitol, raffinose, salicin, trehalose, ethanol, inositol, inulin, lactose, L-lysine, L-rhamnose, N-acetylglucosamine, oxalic acid, pyruvic acid, succinate or L-proline. Strain CL-GR58T was susceptible to streptomycin, gentamicin, vancomycin, kanamycin, penicillin, erythromycin, tetracycline, chloramphenicol, ciprofloxacin and ampicillin, but resistant to mitomycin C, nalidixic acid and polymyxin B.
Strain CL-GR58T could be differentiated phenotypically from the genus Azospirillum by its inability to perform nitrogen fixation and from the genera Rhodocista and Rhodovibrio by the absence of bacteriochlorophyll a (Table 2
). Strain CL-GR58T could be differentiated from members of the genus Defluviicoccus by some phenotypic features (presence of flagella, positive activity for oxidase) and from the genus Skermanella by the positive activity for gelatinase. The growth temperature range distinguished strain CL-GR58T (10–35 °C) from members of the genus Inquilinus (25–42 °C). In addition, the salt tolerance range distinguished strain CL-GR58T (1–10 %) from the genera Azospirillum (<5 %), Tistrella (<1 %), Skermanella (<5 %) and Inquilinus (<6 %) (Table 2).
In conclusion, phylogenetic analyses based on 16S rRNA gene sequences, chemotaxonomic data (fatty acid profiles, quinones) and phenotypic traits indicated that strain CL-GR58T should be classified as a novel genus and species, for which the name Thalassobaculum litoreum gen. nov., sp. nov. is proposed.
Description of Thalassobaculum gen. nov.
Thalassobaculum (Tha.las'so.ba.cu.lum. Gr. n. Thalassa the sea; L. neut. n. baculum stick; N.L. neut. n. Thalassobaculum rod-shaped bacterium from the sea).
Cells are Gram-negative, slightly curved and straight rod-shaped and are motile by means of a polar flagellum. Growth is heterotrophic and facultatively anaerobic. Oxidase- and catalase-positive. Bacteriochlorophyll a is not detected. Unable to fix dinitrogen under anoxic conditions. Dominant cellular fatty acids are C18 : 17c, C16 : 0, C17 : 0, C19 : 0 cyclo 8c and summed feature 3 (C16 : 17c and/or iso-C15 : 0 2-OH). The isoprenoid quinone is Q-10. The G+C content of the DNA is 68.0 mol%. Phylogenetically, the genus is a member of the family Rhodospirillaceae. The type species is Thalassobaculum litoreum.
Description of Thalassobaculum litoreum sp. nov.
Thalassobaculum litoreum (li.to.re'um. L. neut. adj. litoreum of the shore).
Displays the following properties in addition to those given in the genus description. Colonies are circular, convex and cream–yellow on marine agar plates. After 10 days on MA at 30 °C, colonies are approximately 1 mm in diameter. Cells are approximately 0.3–0.5 µm wide and 1.3–1.5 µm long. Grows at between 10 and 35 °C (optimum of 30–35 °C) and pH 7–9 (optimum of pH 8). Growth occurs at sea salts concentrations of 1–10 % (w/v) (optimum 2–4 %), but no growth occurs in media containing only NaCl as a salt. Cells contain poly-β-hydroxybutyrate granules. Gelatinase and amylase are produced. Tween 80 is not hydrolysed. Nitrate is reduced to nitrite. Positive for the following enzyme activities as tested with the API ZYM system: alkaline phosphatase, esterase (C4), leucine arylamidase, valine arylamidase, acid phosphatase, naphthol-AS-BI-phosphohydrolase, - and β-glucosidases and N-acetyl-β-glucosaminidase; weakly positive for esterase lipase (C8), lipase (C14), - and β-galactosidases, -mannosidase and -fucosidase. No activities for cystine arylamidase, trypsin, -chymotrypsin and β-glucuronidase. D-ribose, sucrose, L-arabinose and yeast extract are utilized as carbon sources. Negative for utilization of the following: acetate, -ketobutyric acid, citrate, fructose, galactose, glucose, mannitol, raffinose, salicin, trehalose, ethanol, inositol, inulin, lactose, L-lysine, L-rhamnose, N-acetylglucosamine, oxalic acid, pyruvic acid, succinate and L-proline. Cells are sensitive to (µg per disc): streptomycin (10), gentamicin (10), vancomycin (30), kanamycin (30), penicillin (10), erythromycin (15), tetracycline (30), chloramphenicol (30), ciprofloxacin (5) and ampicillin (10).
The type strain, CL-GR58T (=KCCM 42674T=DSM 18839T), was isolated from coastal seawater, Korea.
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