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Int J Syst Evol Microbiol 56 (2006), 2879-2882; DOI  10.1099/ijs.0.64540-0
© 2006 International Union of Microbiological Societies

Shewanella spongiae sp. nov., isolated from a marine sponge

Sung-Hyun Yang, Kae Kyoung Kwon, Hee-Soon Lee and Sang-Jin Kim

Marine and Extreme Genome Research Center, Korea Ocean Research and Development Institute, PO Box 29, Ansan, 425-600, Republic of Korea

Correspondence
Sang-Jin Kim
s-jkim{at}kordi.re.kr


   ABSTRACT
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A psychrophilic bacterium, designated strain HJ039T, was isolated from a marine sponge collected in the East Sea of Korea (also known as the Sea of Japan). Cells were Gram-negative, motile and rod-shaped (1.8–3.54 µmx0.27–0.73 µm). Growth was observed between 5 and 26 °C (optimum 15 °C), at pH 5.0–8.5 (optimum pH 6.0–6.5) and in the presence of 0–6.0 % NaCl (optimum 2.0 %). The 16S rRNA gene sequence of strain HJ039T showed high levels of similarity (93.7–95.4 %) with members of the genus Shewanella, especially with Shewanella gaetbuli TF-27T (95.2 %), Shewanella decolorationis S12T (94.9 %), Shewanella putrefaciens LMG 26268T (94.6 %), Shewanella hafniensis P010T (94.6 %), Shewanella algae ATCC 51192T (94.5 %) and Shewanella kaireitica c931T (94.5 %). However, phylogenetic analysis revealed that strain HJ039T shared a phyletic line with S. algae and Shewanella amazonensis. The major respiratory quinone was Q-8. The DNA G+C content was 52.8 mol%. The major fatty acids were i-13 : 0 (8.5 %), 15 : 0 (4.2 %), i-15 : 0 (23.2 %), i-15 : 1 (7.9 %), 16 : 0 (8.7 %), 16 : 1{omega}7 (21.0 %) and 17 : 1{omega}8 (6.4 %). From this polyphasic taxonomic evidence, strain HJ039T is considered to represent a novel species of the genus Shewanella, for which the name Shewanella spongiae sp. nov. is proposed. The type strain is HJ039T (=KCCM 42304T=JCM 13830T).

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain HJ039T is DQ167234.

A table detailing the fatty acid content of strain HJ039T and closely related species of the genus Shewanella is available as supplementary material in IJSEM Online.


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The genus Shewanella MacDonell and Colwell 1985Go comprises a group of Gram-negative, motile, rod-shaped, oxidase-positive, non-fermentative and facultatively anaerobic aquatic and marine bacteria with genomic DNA G+C contents of 42–55 mol% (Bowman, 2005Go; Gauthier et al., 1995Go; MacDonell & Colwell, 1985Go; Venkateswaran et al., 1999Go). The genus Shewanella is a member of the Gammaproteobacteria (Anzai et al., 2000Go) and at the time of writing comprised 34 recognized species (see http://www.bacterio.cict.fr/s/shewanella.html and http://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi). Strains belonging to members of the genus Shewanella have been isolated from a variety of sources including marine environments (Bozal et al., 2002Go; Ivanova et al., 2001Go; Nealson et al., 1991Go), clinical samples (Brink et al., 1995Go; Nozue et al., 1992Go; Venkateswaran et al., 1999Go), sediments (Myers & Nealson, 1988Go; Zhao et al., 2005Go) and oilfield fluids (Semple & Westlake, 1987Go). They have also been strongly implicated as opportunistic pathogens of humans and aquatic animals (Aguirre et al., 1994Go; Brink et al., 1995Go) and as the causal agents of proteinaceous food spoilage (Jorgensen & Huß, 1989Go). Shewanella species have also been known to be important in the context of bioremediation, because of their considerable potential for co-metabolic bioremediation of halogenated organic pollutants (Petrovskis et al., 1994Go), destructive souring of crude petroleum (Semple & Westlake, 1987Go), and dissimilatory reduction of manganese and iron oxides (Myers & Nealson, 1988Go), uranium (Lovley & Phillips, 1988Go) and other compounds (Kostka et al., 1996Go; Perry et al., 1993Go). In this study, we report the taxonomic properties of a novel psychrophilic species of Shewanella isolated from marine sponge.

Strain HJ039T was isolated from a marine sponge living at 20 m water depth of the East Sea, Korea (also known as the Sea of Japan). A sponge sample was homogenized and diluted with sterilized seawater, spread onto solid marine agar 2216 (MA; Difco) and then incubated at 10 °C for 1 week. Individual colonies were isolated from MA and the morphologically distinct strain HJ039T was selected for further characterization.

Unless otherwise stated, physiological and morphological characterization was conducted according to the methods of Sohn et al. (2004)Go and Kwon et al. (2005)Go. The bacterial suspension used to inoculate the API 20E, API ZYM (bioMérieux) and Microlog GN2 (Biolog) systems was prepared in a 2 % sea salt (Sigma) solution. To confirm anaerobic growth, cells were inoculated into marine broth 2216 in a serum vial capped with an aluminium seal and cultivated at 15 °C for 2 days. The physiological, biochemical and morphological characteristics of strain HJ039T are given in the species description and in Table 1Go.


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  		Table 1. Physiological characteristics differentiating strain HJ039T and the type strains of related Shewanella species

Strains: 1, HJ039T; 2, S. gaetbuli TF-27T; 3, S. decolorationis S12T; 4, S. algae ATCC 51192T; 5, S. hafniensis P010T; 6, S. putrefaciens LMG 26268T; 7, S. amazonensis SB2BT. Data for strain HJ039T are from this study; data for the other taxa are from Bowman (2005)Go, Satomi etal. (2006)Go, Venkateswaran et al. (1999)Go, Yoon et al. (2004)Go and Xu et al. (2005)Go. +, Positive reaction; –, negative reaction; V, variable reaction; ND, not determined. All are straight, rod-shaped organisms, oxidase- and catalase-positive, and do not utilize citrate.

 
The cellular fatty acid profile of strain HJ039T was determined from 2-day-old culture at 15 °C according to the procedure described by Sohn et al. (2004)Go. Dominant fatty acids were i-13 : 0 (8.5 %), 15 : 0 (4.2 %), i-15 : 0 (23.2 %), i-15 : 1 (7.9 %), 16 : 0 (8.7 %), 16 : 1{omega}7 (21.0 %) and 17 : 1{omega}8 (6.4 %) (see Supplementary Table S1 in IJSEM Online). The major respiratory quinone was Q-8, as determined by HPLC analysis (according to the method of Collins, 1985Go). The DNA G+C content was 52.8 mol%, as determined by HPLC using a symmetry reversed-phase C18 column (Waters) (Stackebrandt & Liesack, 1993Go).

Extraction of genomic DNA and amplification of the 16S rRNA gene were conducted according to Sohn et al. (2004)Go and a phylogenetic analysis using the 16S rRNA gene sequence was conducted according to the procedure described by Kwon et al. (2005)Go. The 16S rRNA gene sequence of strain HJ039T comprised a continuous stretch of 1474 nt, and approximately 1350 bp corresponding to positions 94–1440 of the Escherichia coli numbering system (Weisburg et al., 1991Go) was compared in considerations of sequence quality. Exceptions to this were for Shewanella halifaxensis (1279 bp) and Shewanella sediminis (1271 bp) because only short sequences were available from the GenBank database. Aeromonas salmonicida CIP 103209T (GenBank accession no. X74681) and Ferrimonas balearica DSM 9799T (GenBank accession no. X93021) served as outgroups for phylogenetic analysis. Sequence similarity after alignment indicated that the closest relatives of strain HJ039T were Shewanella gaetbuli TF-27T (95.2 %), Shewanella decolorationis S12T (94.9 %), Shewanella putrefaciens LMG 26268T (94.6 %), Shewanella hafniensis P010T (94.6 %), Shewanella algae ATCC 51192T (94.5 %) and Shewanella kaireitica c931T (94.5 %).

The phylogenetic tree based on 16S rRNA gene sequences of members of the genus Shewanella has been divided into two major groups, with S. algae and Shewanella amazonensis forming relatively distinct branches (Bowman, 2005Go). The first group (group I) includes psychrotolerant, non-halophilic strains and the second group (group II) includes psychrotolerant, Na+-requiring strains. According to this definition, the six closest relatives of strain HJ039T could be affiliated into group II with the exception of S. kaireitica. However, strain HJ039T shared a phyletic line with S. algae and S. amazonensis rather than with S. gaetbuli, S. decolorationis, etc., within group II (Fig. 1Go). This result matched well with the DNA G+C values (>50 mol% for strain HJ039T, S. algae and S. amazonensis), although these data cannot be used to specify the phylogenetic position of any particular strain.


Figure 1
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  		Fig. 1. Rooted neighbour-joining tree based on nearly complete 16S rRNA gene sequences showing the relationship between strain HJ039T and members of the genus Shewanella. Approximately 1350 bp corresponding to positions 94–1440 of the E. coli numbering system was compared. Bootstrap values of 1000 resampled datasets at all nodes are shown. Bar, 0.01 substitutions per nucleotide position.

 
Strain HJ039T did not have an obligate Na+ requirement for growth, although the presence of Na+ ions enhanced growth, a trait observed for other members of Shewanella group II. Some characteristics, such as utilization of D-fructose and sucrose, lack of nitrate-reducing ability and high levels of the fatty acid i-15 : 1, can be used to differentiate strain HJ039T from closely related members of the genus Shewanella. On the basis of this polyphasic taxonomic evidence, strain HJ039T is considered to represent a novel species of the genus Shewanella, for which the name Shewanella spongiae sp. nov. is proposed.

Description of Shewanella spongiae sp. nov.
Shewanella spongiae (spon.gi'ae. L. gen. n. spongiae of a sponge, the source of the type strain).

Cells are Gram-negative, rod-shaped (1.8–3.54 µmx0.27–0.73 µm) and motile. Cells appear singly or in chains. Colonies formed after 2 days on MA at 15 °C are white, circular, opaque and convex with entire margins. Growth does not occur under anaerobic conditions on MA. Growth is observed at 5–26 °C (optimum 15 °C), pH 5.0–8.5 (optimum 6.0–6.5) and in the presence of 0–6 % (w/v) NaCl (optimum 2.0 %). Produces oxidase and catalase. When assayed with the API ZYM system, esterase (C4), esterase lipase (C8), alkaline phosphatase, leucine arylamidase, acid phosphatase and naphthol-AS-BI-phosphohydrolase are present and valine arylamidase activity is weakly positive. Negative for lipase (C14), cystine arylamidase, trypsin, {alpha}-chymotrypsin, {alpha}-galactosidase, beta-galactosidase, beta-glucuronidase, {alpha}-glucosidase, beta-glucosidase, N-acetyl-beta-glucosaminidase, {alpha}-mannosidase and {alpha}-fucosidase. Degrades sucrose, D-trehalose, dextrin, D-arabitol, D-fructose, {alpha}-D-glucose, D-mannose and L-serine and can utilize turanose (weakly) on Microlog GN2 plates. Major fatty acids are i-13 : 0, 15 : 0, i-15 : 0, i-15 : 1, 16 : 0, 16 : 1{omega}7 and 17 : 1{omega}8. The major respiratory quinone is Q-8. The DNA G+C content is 52.8 mol%.

The type strain, HJ039T (=KCCM 42304T=JCM 13830T), was isolated from a marine sponge in the East Sea, Korea, at 20 m water depth.


   ACKNOWLEDGEMENTS
 
This work was supported by the Marine and Extreme Genome Research Center Program of the Ministry of Marine Affairs and Fisheries, Korea. Special thanks are due to Dr J. P. Euzéby for nomenclature and Y. Y. Yoon (Kwandong University) for provision of SCUBA-diving and laboratory facilities.


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