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Int J Syst Evol Microbiol 56 (2006), 1631-1634; DOI  10.1099/ijs.0.64305-0
© 2006 International Union of Microbiological Societies

Halorubrum lipolyticum sp. nov. and Halorubrum aidingense sp. nov., isolated from two salt lakes in Xin-Jiang, China

Heng-Lin Cui1,2, Dilbr Tohty3, Pei-Jin Zhou1 and Shuang-Jiang Liu1

1 State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, ZhongGuanCun, Haidian, Beijing 100080, People's Republic of China
2 Graduate University of Chinese Academy of Sciences, Beijing 100049, People's Republic of China
3 College of Life Sciences, Xin-Jiang Normal University, Urumqi 830053, People's Republic of China

Correspondence
Shuang-Jiang Liu
liusj{at}sun.im.ac.cn


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Two extremely halophilic archaea, strains 9-3T and 31-hongT, were isolated from Aibi salt lake and Aiding salt lake in Xin-Jiang, China. Their morphology, physiology, biochemical features, polar lipid compositions and 16S rRNA gene sequences were characterized in order to elucidate their taxonomic status. The results from this study indicated that strains 9-3T and 31-hongT are members of the genus Halorubrum. Their physiological properties and polar lipid compositions are clearly different from those of the currently described species of Halorubrum. DNA–DNA relatedness values for strain 9-3T with respect to its closely related neighbours Halorubrum saccharovorum JCM 8865T and Halorubrum lacusprofundi JCM 8891T were 51.6 and 25.1 %, respectively, DNA–DNA relatedness values for strain 31-hongT with respect to its closely related neighbours Hrr. saccharovorum JCM 8865T and Hrr. lacusprofundi JCM 8891T were 29.4 and 44.9 %, respectively, and DNA–DNA relatedness between strains 9-3T and 31-hongT was 54 %. Thus, two novel species of the genus Halorubrum are proposed, Halorubrum lipolyticum sp. nov. (type strain 9-3T=CGMCC 1.5332T=JCM 13559T) and Halorubrum aidingense sp. nov. (type strain 31-hongT=CGMCC 1.2670T=JCM 13560T).

The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains 9-3T and 31-hongT are DQ355814 and DQ355813, respectively.

A thin-layer chromatogram showing the glycolipids/phospholipids of strains 9-3T and 31-hongT and members of the genus Halorubrum is available as a supplementary figure in IJSEM Online.


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To date, the genus Halorubrum contains 12 species with validly published names: Halorubrum lacusprofundi (Franzmann et al., 1988Go), Hrr. saccharovorum (Tomlinson & Hochstein, 1976Go), Hrr. coriense (Kamekura & Dyall-Smith, 1995Go; McGenity & Grant, 1995Go), Hrr. distributum (Zvyagintseva & Tarasov, 1987Go; Oren & Ventosa, 1996Go), Hrr. sodomense (Oren, 1983Go; Oren & Ventosa, 1996Go), Hrr. tebenquichense (Lizama et al., 2002Go), Hrr. terrestre (Ventosa et al., 2004Go), Hrr. trapanicum (McGenity & Grant, 1995Go), Hrr. xinjiangense (Feng et al., 2004Go), Hrr. alkaliphilum (Feng et al., 2005Go), Hrr. tibetense (Fan et al., 2004Go) and Hrr. vacuolatum (Mwatha & Grant, 1993Go; Kamekura et al., 1997Go). A phylogenetic tree based on the 16S rRNA gene sequences of these species indicates that the 12 species belonged to three distinct clusters (Fig. 1Go). Cluster 1 contains neutrophilic species, including Hrr. coriense, Hrr. distributum, Hrr. sodomense, Hrr. tebenquichense, Hrr. terrestre, Hrr. trapanicum and Hrr. xinjiangense. Cluster 2 consists of two other neutrophilic species, Hrr. lacusprofundi and Hrr. saccharovorum. Cluster 3 contains three alkaliphilic species, Hrr. alkaliphilum, Hrr. tibetense and Hrr. vacuolatum. During our surveys on the halophilic archaeal diversity of two salt lakes in the Xin-Jiang region of China (Cui et al., 2006Go), two strains that clustered tightly with members of cluster 2 were obtained. In this paper, we present the taxonomy of the two strains, strains 9-3T and 31-hongT.


Figure 1
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  		Fig. 1. Phylogenetic tree, based on 16S rRNA gene sequences, showing the relationships between the members of the genus Halorubrum and related genera within the family Halobacteriaceae. Bootstrap values (%) are based on 1000 replicates and are shown for branches with more 80 % bootstrap support. Bar, 0.02 expected changes per site.

 
Strains 9-3T and 31-hongT were isolated from sediments of Aibi salt lake and Aiding salt lake, respectively. The isolation procedure was as described previously (Xin et al., 2000Go; Feng et al., 2004Go). Characterization of strains 9-3T and 31-hongT was performed according to the proposed minimal standards for the description of novel taxa in the order Halobacteriales (Oren et al., 1997Go). The morphology and growth characteristics were assessed, miscellaneous biochemical and nutrition tests were performed, sensitivity to antimicrobial agents was determined, lipids were analysed and nucleic acid characterization and DNA–DNA hybridization (thermal denaturation and renaturation method) were performed as described and cited by Feng et al. (2004Go, 2005)Go.

The cells of strains 9-3T and 31-hongT are motile, Gram-negative rods. Both strains are able to grow in a wide range of salinities (1.7–4.3 M salt; optimal growth at 2.6 M). The cells lyse in distilled water. Colonies on agar medium are red-pigmented. Details of the morphology, growth characteristics, nutrition, antibiotic sensitivity and biochemistry of strains 9-3T and 31-hongT are given in the species descriptions. Differences between strains 9-3T and 31-hongT and other members of the genus Halorubrum are shown in Table 1Go.


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  		Table 1. Differentiation of Halorubrum lipolyticum sp. nov. 9-3T and Halorubrum aidingense sp. nov. 31-hongT from other Halorubrum species

Taxa: 1, strain 9-3T; 2, strain 31-hongT; 3, Hrr. lacusprofundi JCM 8891T; 4. Hrr. saccharovorum JCM 8865T; 5, Hrr. coriense JCM 9275T (data from McGenity & Grant, 2001Go); 6, Hrr. distributum JCM 9100T (McGenity & Grant, 2001Go); 7, Hrr. sodomense ATCC 33755T (McGenity & Grant, 2001Go); 8, Hrr. tebenquichense ALT6-92T (Lizama et al., 2002Go); 9, Hrr. terrestre VKM B-1739T (Ventosa et al., 2004Go); 10, Hrr. trapanicum JCM 10477T (McGenity & Grant, 2001Go); 11, Hrr. xinjiangense AS 1.3527T (Feng et al., 2004Go); 12, Hrr. alkaliphilum AS 1.3528T (Feng et al., 2005Go); 13, Hrr. tibetense AS 1.3239T (Fan et al., 2004Go); 14, Hrr. vacuolatum JCM 9060T (McGenity & Grant, 2001Go). Symbols: +, positive; –, negative; W, weakly positive; ND, not determined. Data for strains 9-3T, 31-hongT, JCM 8891T and ATCC 29252T were obtained in this study.

 
Phylogenetic analyses based on the 16S rRNA gene sequences of strain 9-3T and strain 31-hongT indicated that they were most closely related to those of Hrr. lacusprofundi ACAM 34T (98.2 and 98.5 %, respectively) and Hrr. saccharovorum JCM 8865T (98.1 and 97.3 %, respectively). The 16S rRNA gene sequence similarity between strains 9-3T and 31-hongT was 97.6 %.

Polar lipid analysis indicated that both strains contained C20–C20 derivatives of phosphatidylglycerol, phosphatidylglycerol phosphate methyl ester and phosphatidylglycerol sulfate. Glycolipids of strain 9-3T migrated with the same RF values as those of Hrr. saccharovorum and Hrr. lacusprofundi, but not those of strain 31-hongT (see Supplementary Fig. S1 available in IJSEM Online). The DNA G+C contents of strains 9-3T and 31-hongT are 65.9 and 64.2 mol% (Tm), respectively. The DNA–DNA relatedness values for strain 9-3T with respect to Hrr. saccharovorum JCM 8865T and Hrr. lacusprofundi JCM 8891T were 51.6 and 25.1 %, and those for strain 31-hongT with respect to Hrr. saccharovorum JCM 8865T and Hrr. lacusprofundi JCM 8891T were 29.4 and 44.9 %, respectively. The DNA–DNA relatedness between strains 9-3T and 31-hongT was 54 %.

On the basis of these results, it is concluded that strains 9-3T and 31-hongT represent two novel species of the genus Halorubrum, for which the names Halorubrum lipolyticum sp. nov. and Halorubrum aidingense sp. nov. are proposed.

Description of Halorubrum lipolyticum sp. nov.
Halorubrum lipolyticum (li.po.ly'ti.cum. Gr. n. lipos fat; N.L. neut. adj. lyticum from Gr. adj. lutikos able to loosen, able to dissolve; N.L. neut. adj. lipolyticum fat-dissolving, referring to the property of being able to hydrolyse lipids).

Cells are motile, rod-shaped (0.9–1.2x1.8–5.5 µm) and Gram-negative. Colonies on agar plates containing 2.6 M NaCl are red, elevated and round. Chemo-organotrophic and aerobic. Growth occurs at NaCl concentrations of 1.7–4.8 M, at pH 7.0–9.0 and temperatures of 25–58 °C. Optimal NaCl concentration, pH and temperature for growth are 2.6 M, pH 7.5 and 45–48 °C, respectively. Catalase- and oxidase-positive. Anaerobic growth with nitrate, arginine or DMSO does not occur. Nitrate reduction to nitrite is observed. H2S is not produced from Na2S2O3. Negative for indole formation. Tweens 20, 40, 60 and 80 are hydrolysed. Caseinase-negative. Amylase- and gelatinase-positive. Glucose, fructose, galactose, mannose, sucrose and maltose are utilized and acids are produced. No growth or acid production is observed on sorbose, xylose, lactose, D-ribose, mannitol or sorbitol. Sensitive to rifampicin, bacitracin and novobiocin. Resistant to erythromycin, neomycin, chloramphenicol, ampicillin, penicillin G, norfloxacin, ciprofloxacin, streptomycin, kanamycin, tetracycline and vancomycin. Cells contain C20–C20 derivatives of phosphatidylglycerol, phosphatidylglycerol phosphate methyl ester, phosphatidylglycerol sulfate and sulfated mannosyl-glucosyl glycerol diether. The DNA G+C content of the type strain is 65.9 mol% (Tm).

The type strain, 9-3T (=CGMCC 1.5332T=JCM 13559T), was isolated from Aibi salt lake in Xin-Jiang, China.

Description of Halorubrum aidingense sp. nov.
Halorubrum aidingense (ai.ding.en'se. N.L. neut. adj. aidingense from Aiding salt lake in China, where the type strain was isolated).

Cells are motile, rod-shaped (0.9–1.0x3.6–6.4 µm) and Gram-negative. Colonies on agar plates containing 2.6 M NaCl are red, elevated and round. Chemo-organotrophic and aerobic. Growth occurs at NaCl concentrations of 1.7–4.3 M, at pH 7.0–9.0 and at temperatures of 25–52 °C. Optimal NaCl concentration, pH and temperature for growth are 2.6 M, pH 7.5 and 40–42 °C, respectively. Catalase- and oxidase-positive. Anaerobic growth with nitrate, arginine or DMSO does not occur. Nitrate reduction to nitrite is observed. H2S is not produced from Na2S2O3. Positive for indole formation. Tweens 20, 40, 60 and 80 are hydrolysed. Casein and starch are not hydrolysed. Gelatin is not liquefied. Glucose, fructose, galactose, mannose, sucrose, maltose and mannitol are utilized and acids are produced. No growth or acid production is observed on sorbose, xylose, lactose, D-ribose or sorbitol. Sensitive to rifampicin, bacitracin and novobiocin. Resistant to erythromycin, neomycin, chloramphenicol, ampicillin, penicillin G, norfloxacin, ciprofloxacin, streptomycin, kanamycin, tetracycline and vancomycin. Cells contain C20–C20 derivatives of phosphatidylglycerol, phosphatidylglycerol phosphate and phosphatidylglycerol phosphate sulfate. Sulfated mannosyl-glucosyl glycerol diether was not detected. The DNA G+C content of the type strain is 64.2 mol% (Tm).

The type strain, 31-hongT (=CGMCC 1.2670T=JCM 13560T), was isolated from Aiding salt lake in Xin-Jiang, China.


   ACKNOWLEDGEMENTS
 
This work was supported by the grants from the Ministry of Science and Technology (2004CB719601) and from the Chinese Academy of Sciences (KJCX1-SW-07).


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Feng, J., Zhou, P., Liu, S.-J. & Warren-Rhodes, K. (2005). Halorubrum alkaliphilum sp. nov., a novel haloalkaliphile isolated from a soda lake in Xinjiang, China. Int J Syst Evol Microbiol 55, 149–152.[Abstract/Free Full Text]

Franzmann, P. D., Stackebrandt, E., Sanderson, K., Volkman, J. K., Cameron, D. E., Stevenson, P. L., McMeekin, T. A. & Burton, H. R. (1988). Halobacterium lacusprofundi sp. nov., a halophilic bacterium isolated from Deep Lake, Antarctica. Syst Appl Microbiol 11, 20–27.

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Kamekura, M., Dyall-Smith, M. L., Upasani, V., Ventosa, A. & Kates, M. (1997). Diversity of alkaliphilic halobacteria: proposals for transfer of Natronobacterium vacuolatum, Natronobacterium magadii, and Natronobacterium pharaonis to Halorubrum, Natrialba, and Natronomonas gen. nov., respectively, as Halorubrum vacuolatum comb. nov., Natrialba magadii comb. nov., and Natronomonas pharaonis comb. nov., respectively. Int J Syst Bacteriol 47, 853–857.[Abstract/Free Full Text]

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McGenity, T. J. & Grant, W. D. (1995). Transfer of Halobacterium saccharovorum, Halobacterium sodomense, Halobacterium trapanicum NRC 34021, and Halobacterium lacusprofundi to the genus Halorubrum gen. nov., as Halorubrum saccharovorum comb. nov., Halorubrum sodomense comb. nov., Halorubrum trapanicum comb. nov., and Halorubrum lacusprofundi comb. nov. Syst Appl Microbiol 18, 237–243.

McGenity, T. J. & Grant, W. D. (2001). Genus VII. Halorubrum McGenity and Grant 1996, 362VP. In Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 1, pp. 320–324. Edited by D. R. Boone, R. W. Castenholz & G. M. Garrity. New York: Springer.

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