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Int J Syst Evol Microbiol 56 (2006), 45-49; DOI  10.1099/ijs.0.63835-0
© 2006 International Union of Microbiological Societies

Jannaschia seosinensis sp. nov., isolated from hypersaline water of a solar saltern in Korea

Dong Han Choi1, Hana Yi2, Jongsik Chun2 and Byung Cheol Cho1

1 School of Earth and Environmental Sciences and Research Institute of Oceanography, Seoul National University, 56-1 Shillim-dong, Kwanak-gu, Seoul 151-742, Republic of Korea
2 School of Biological Sciences, Seoul National University, 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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A slightly halophilic alphaproteobacterium, designated CL-SP26T, was isolated from hypersaline water of a solar saltern located in Seosin, Korea. 16S rRNA gene sequence analysis revealed an affiliation with the genus Jannaschia. Sequence similarities between CL-SP26T and type strains of members of the genus Jannaschia were 94·9–97·2 %. Cells were rod-shaped and motile with one or more monopolar flagella. Strain CL-SP26T grew on solid media as circular red colonies. It was able to grow in 3–10 % sea salt; however, no growth occurred in media containing NaCl as the only salt. Strain CL-SP26T grew at 5–35 °C and pH 7–10. The major fatty acids were 18 : 1{omega}7c (64 %) and 18 : 0 (12·0 %). Three fatty acids, 3-OH 14 : 0/iso 16 : 1 (3·6 %), 18 : 3{omega}6c (2·2 %) and 10-methyl 19 : 0 (1·9 %), found in minor quantities in CL-SP26T, are unique among Jannaschia species. The DNA G+C content was 63 mol%. According to physiological data, fatty acid composition and 16S rRNA gene sequence analysis, CL-SP26T was assigned to the genus Jannaschia, but could be distinguished from recognized species of the genus. Strain CL-SP26T (=KCCM 42114T=JCM 13035T) therefore represents a novel species, for which the name Jannaschia seosinensis sp. nov. is proposed.

Abbreviations: ASW, artificial sea water; p.s.u., practical salinity units

Published online ahead of print on 26 August 2005 as DOI 10.1099/ijs.0.63835-0.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain CL-SP26T is AY906862.

A table showing phenotypic characteristics of Jannaschia species is available as supplementary material in IJSEM Online.


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The genus Jannaschia was first described by Wagner-Döbler et al. (2003)Go. To date, three species, Jannaschia helgolandensis (type species; Wagner-Döbler et al., 2003Go), Jannaschia cystaugens (Adachi et al., 2004Go) and Jannaschia rubra (Macián et al., 2005Go), have been isolated, from sea water collected from the North Sea, Hiroshima Bay in Japan and the Mediterranean Sea on the Spanish east coast, respectively. Recently, J. cystaugens has been transferred to the genus Thalassobacter (Pujalte et al., 2005Go).

A hypersaline water sample [salinity of 318 practical salinity units (p.s.u.)] from a solar saltern in Seosin, Korea, was spread on a plate containing marine agar 2216 (MA; Difco) and the plate was incubated at 30 °C for 2 weeks. A reddish colony, strain CL-SP26T, was isolated on the plate and subsequently purified four times on MA at 30 °C. The strain was maintained both on MA at 4 °C and in marine broth (MB; Difco) supplemented with 30 % (v/v) glycerol at –80 °C.

Morphological and physiological tests were performed. Gram-staining was performed as described by Smibert & Krieg (1994)Go. Cell morphology and motility were examined by phase-contrast microscopy with cells grown at 30 °C in MB. The presence of flagella was observed using TEM (JEOL EX2) after cells had been negatively stained with uranyl acetate (2 %). Anaerobic growth was checked on MA using the GasPak anaerobic system (BBL). Bacteriochlorophyll production was determined in acetone extracts using a spectrophotometer (Ultraspec 2000; Pharmacia Biotech) for cells that had been grown in the dark. Catalase and oxidase activities were determined according to the protocols described by Smibert & Krieg (1994)Go. Gelatinase, amylase, DNase, nitrate reductase and degradation of Tween 80 were examined as described by Hansen & Sørheim (1991)Go. Cells were rod-shaped and motile by one or more monopolar flagella (Fig. 1Go). Chain formation was rarely observed in CL-SP26T. Bright granules were not seen on wet mounts of cells of different ages. Colonies on MA were red-coloured, circular, smooth and shiny. They could be dispersed well in MB and artificial sea water (ASW), unlike J. rubra (Macián et al., 2005Go). Other morphological characteristics are shown in Table 1Go.



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  		Fig. 1. TEM of negatively stained cells of strain CL-SP26T. Bars, 0·5 µm.

 

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  		Table 1. Selected phenotypic characteristics of Jannaschia seosinensis sp. nov. and other Jannaschia species

Strains: 1, J. seosinensis CL-SP26T (data from this study); 2, J. helgolandensis Hel 10T (Wagner-Döbler et al., 2003Go), 3, J. rubra CECT 5088T (Macián et al., 2005Go). ND, No data available. All strains are Gram-negative.

 
The temperature range for growth was determined on the basis of colony formation on MA plates that were incubated at 5–45 °C. The pH range for growth (tested at pH 5–11) was determined by changes in OD600 with time in MB. The final pH was adjusted using NaOH and HCl solutions. Growth of CL-SP26T in sea salt was determined using synthetic ZoBell broth (Bacto peptone, 5 g; yeast extract, 1 g; ferric citrate, 0·1 g; distilled water, 1 l) with various concentrations of sea salt (0, 1, 3, 5, 7, 10, 15, 20, 25 %, w/v). Nitrate reductase, indole production, acid production from glucose, arginine dihydrolase, urease, aesculin hydrolysis, gelatinase, {beta}-galactosidase and carbon source utilization were tested using the API 20NE kit (bioMérieux) according to the manufacturer's instructions, except that cell suspensions were prepared using ASW (NaCl, 24 g; MgCl2, 5·1 g; Na2SO4, 4 g; CaCl2, 1·1 g; KCl, 0·7 g; NaHCO3, 0·2 g; KBr, 0·1 g; H3BO3, 0·027 g; SrCl2, 0·024 g; NaF, 0·003 g; distilled water, 1 l; Lyman & Fleming, 1940Go) as a suspension medium and cell suspensions for carbon assimilation were prepared using an AUX medium containing 2·8 ml 10 % sea salt. Other enzyme activities were assayed using the API ZYM kit (bioMérieux) and ASW as a suspension medium. Carbon utilization by CL-SP26T was tested on basal medium agar [BMA: Tris/HCl, 50 mM, pH 7·5; NH4Cl, 190 mM; K2HPO4.3H2O, 0·33 mM; FeSO4.7H2O, 0·1 mM; and 1·5 % Bacto agar (Difco) in half-strength ASW; Baumann & Baumann, 1981Go] containing 0·2 % carbon source. BMA was supplemented with 0·01 % yeast extract. In addition, carbon utilization was investigated using Biolog GN plates. Four kinds of suspension media, ASW, basal medium (BM; Baumann et al., 1971Go) and BM supplemented with 0·01 and 0·1 % yeast extract, were used in the Biolog tests.

For API 20NE, API ZYM and Biolog analyses, J. helgolandensis Hel 10T and J. rubra CECT 5088T were used as reference strains. DNA G+C content was determined using the thermal denaturation method (Mandel & Marmur, 1968Go). CL-SP26T grew optimally at 30–35 °C and pH 10, differentiating it from other species in the genus Jannaschia (Table 1Go). CL-SP26T was unable to grow at 1 % (w/v) salinity, unlike J. helgolandensis Hel 10T and J. rubra CECT 5088T (Table 1Go). Although CL-SP26T was isolated from hypersaline water of 318 p.s.u., the upper salinity limit for growth was 10 %, suggesting that the strain might have survived in highly saline water. The strain was positive for nitrate reductase, gelatinase and amylase, but negative for the presence of cytochrome oxidase, whereas other species in genus Jannaschia gave contrasting results (Table 2Go).


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  		Table 2. Selected phenotypic characteristics that differentiate J. seosinensis sp. nov. from other Jannaschia species

Strains: 1, J. seosinensis CL-SP26T (data from this study); 2, J. helgolandensis Hel 10T (Wagner-Döbler et al., 2003Go), 3, J. rubra CECT 5088T (Macián et al., 2005Go). ND, No data available; +, positive; –, negative; W, weak. API 20NE and API ZYM data were obtained in this study. All species are positive for catalase.

 
CL-SP26T could grow on BMA plates containing D-glucose, salicin, pyruvic acid, Casamino acids, DL-aspartate, succinate, urea and L-glutamate (see Supplementary Table available in IJSEM Online). However, no visible growth could be observed in Biolog GN plate tests or in carbon assimilation tests in API 20NE. The different results from each of the tests might result from differences in methods used and the composition of suspension media. Other results of biochemical and physiological tests are given in Tables 1 and 2GoGo and the species description.

Isoprenoid quinones were isolated according to Minnikin et al. (1984)Go and analysed by HPLC as described by Collins (1985)Go. The major isoprenoid quinone was UQ-10. Fatty acid methyl esters in whole cells were analysed by GC according to the Microbial Identification System (MIDI) at the Korean Culture Center of Microorganisms, Seoul, Korea. The fatty acid profile for CL-SP26T was dominated by 18 : 1{omega}7c (64 %) and 18 : 0 (12 %), which is a characteristic common to all species in the genus Jannaschia (Table 3Go). However, 3-OH 14 : 0 and/or iso 16 : 1 (3·6 %), 18 : 3{omega}6c (2·2 %) and 10-methyl 19 : 0 (1·9 %) were found in minor quantities in CL-SP26T; these fatty acids are unique among Jannaschia species. Therefore, the fatty acid pattern of strain CL-SP26T differs distinctly from those of the other species of Jannaschia.


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  		Table 3. Fatty acid compositions (%) of J. seosinensis sp. nov. and other Jannaschia species

Strains: 1, J. seosinensis CL-SP26T (data from this study); 2, J. helgolandensis Hel 10T (Wagner-Döbler et al., 2003Go), 3, J. rubra CECT 5088T (Macián et al., 2005Go). –, Not detected or <1 %.

 
The 16S rRNA gene was amplified from a single colony by PCR with Taq DNA polymerase (Bioneer) and primers 27F and 1492R (Lane, 1991Go). The PCR product was purified using the AccuPrep PCR Purification kit (Bioneer) and cloned using the pCR2.1 TOPO TA Cloning kit (Invitrogen). Sequencing of the 16S rRNA gene was performed with an Applied Biosystems automatic sequencer (ABI3730XL) at Macrogen Corporation, Seoul, Korea. The sequence of strain CL-SP26T was compared with 16S rRNA gene sequences available in GenBank using the BLAST (Altschul et al., 1990Go) search. The sequence of strain CL-SP26T was manually aligned with sequences from other species of the genus Jannaschia and type species of other genera belonging to the family Rhodobacteraceae obtained from GenBank and the Ribosomal Database Project (Cole et al., 2003Go) using known 16S rRNA secondary structure information. Phylogenetic trees were obtained by 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 tree topologies was assessed by bootstrap analyses based on 1000 replications for neighbour-joining and maximum-parsimony methods and 100 replications for the maximum-likelihood method. Alignment analysis was carried out using the program jPHYDIT (version 1.0; available at http://chunlab.snu.ac.kr/jphydit/) and phylogenetic analysis was carried out using MEGA3 (Kumar et al., 2004Go) and PAUP* 4.0 (Swofford, 1998Go). Likelihood parameters were estimated by the hierarchical ratio tests in MODELTEST version 3.04 (Posada & Crandall, 1998Go). The almost complete 16S rRNA gene sequence of strain CL-SP26T (1384 bp) was obtained. Sequence similarity analysis indicated that the closest relatives of strain CL-SP26T were J. rubra (97·2 %), J. helgolandensis (96·9 %) and Thalassobacter stenotrophicus (94·9 %). Phylogenetic analyses based on the 16S rRNA gene sequence showed that strain CL-SP26T formed a robust cluster with species of the genus Jannaschia (Fig. 2Go). Thus, it is clear that this isolate belongs to the genus Jannaschia. Although the similarities between strain CL-SP26T and two species (J. rubra and J. helgolandensis) were close to general guidelines (97 %) for species designation at the 16S rRNA gene level (Stackebrandt & Goebel, 1994Go), a dendrogram of 16S rRNA gene relationships showed that CL-SP26T is phylogenetically distant from these two species, forming a distinct branch. Furthermore, phenotypic features (salt, temperature and pH ranges for growth, presence of nitrate reductase, amylase and gelatinase activities, absence of oxidase activity) and fatty acid profiles clearly differentiated CL-SP26T from J. rubra and J. helgolandensis. In conclusion, physiological features, fatty acid profiles and phylogenetic analyses based on 16S rRNA gene sequences suggest that strain CL-SP26T represents a novel species of the genus Jannaschia, for which the name Jannaschia seosinensis sp. nov. is proposed.



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  		Fig. 2. Neighbour-joining tree showing the relationship between strain CL-SP26T and members of the genus Jannaschia and other related genera belonging to the Rhodobacteraceae. Only bootstrap values above 70 % are shown (1000 resamplings) at the branching points. Solid circles indicate that the corresponding nodes are also recovered in maximum-likelihood and maximum-parsimony trees. Sequence accession numbers are given in parentheses. Paracoccus denitrificans IAM 12479T (Y17512) was used as an outgroup (not shown). Bar, 0·01 nucleotide substitutions per site.

 
Description of Jannaschia seosinensis sp. nov.
Jannaschia seosinensis (se.o.sin.en'sis. N.L. fem. adj. seosinensis referring to the Seosin region in Korea, where the type strain was found).

Gram-negative, strictly aerobic and straight rods, approximately 0·7–1·2 µm wide and 1·1–2·3 µm long. Cells are motile by one or more monopolar flagella. On MA solid medium, colonies are dark red, entire, circular, convex and shiny. Bacteriochlorophyll is not detected. After 4 days on MA at 30 °C colonies are approximately 0·8–1·5 mm in diameter. Grows at 5–35 °C (optimum of 30–35 °C) and pH 7–10. Growth occurs in sea salt concentrations of 3–10 % (w/v) (optimum of 3–5 %), but no growth occurs in media containing only NaCl as a salt. Positive for catalase, amylase, gelatinase and nitrate reductase, but negative for oxidase, DNase and degradation of Tween 80. Major fatty acids are 18 : 1{omega}7c (64 %) and 18 : 0 (12·0 %); 3-OH 14 : 0 and/or iso 16 : 1 (3·6 %), 18 : 3{omega}6c (2·2 %) and 10-methyl 19 : 0 (1·9 %) are found in minor quantities. In API 20NE tests, the type strain is negative for nitrate reductase, gelatinase, arginine dihydrolase, urease, indole production and acid production from glucose, but positive for hydrolysis of aesculin and {beta}-galactosidase. In API ZYM tests, the type strain is positive for alkaline phosphatase, esterase (C4 and C8), leucine arylamidase, valine arylamidase, {alpha}-galactosidase, {beta}-galactosidase and {alpha}-glucosidase, but negative for lipase (C14), cystine arylamidase, trypsin, {alpha}-chymotrypsin, acid phosphatase, naphthol-AS-BI-phosphohydrolase, {beta}-glucuronidase, {beta}-glucosidase, N-acetyl-{beta}-glucosaminidase, {alpha}-mannosidase and {alpha}-fucosidase. The following substrates are utilized: D-glucose, salicin, pyruvic acid, Casamino acids, DL-aspartate, succinate, urea and L-glutamate.

The type strain is CL-SP26T (=KCCM 42114T=JCM 13035T), isolated from a hypersaline water sample from a solar saltern. The DNA G+C content of the type strain is 63 mol%.


   ACKNOWLEDGEMENTS
 
This work was supported in part by the Special Grants Research Program in Fisheries (MOMAF) to B. C. C. (20000039) and by the BK21 project of the Korean Government.


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