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Int J Syst Evol Microbiol 57 (2007), 2472-2475; DOI  10.1099/ijs.0.65079-0
© 2007 International Union of Microbiological Societies

Nocardioides terrigena sp. nov., isolated from soil

Jung-Hoon Yoon, So-Jung Kang, Soo-Young Lee and Tae-Kwang Oh

Korea Research Institute of Bioscience and Biotechnology (KRIBB), PO Box 115, Yusong, Taejon, Korea

Correspondence
Jung-Hoon Yoon
jhyoon{at}kribb.re.kr


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A Gram-positive, rod- or coccoid-shaped bacterial strain, DS-17T, was isolated from a soil in Dokdo, Korea, and its taxonomic position was investigated by using a polyphasic approach. Strain DS-17T grew optimally at around pH 8.0 and 30 °C in the presence of 0.5–1.0 % (w/v) NaCl. Phylogenetic analyses based on 16S rRNA gene sequences showed that strain DS-17T belonged to the genus Nocardioides. The chemotaxonomic properties of strain DS-17T were consistent with those of the genus Nocardioides: the cell-wall peptidoglycan type was based on LL-2,6-diaminopimelic acid, MK-8(H4) was the predominant menaquinone and iso-C16 : 0, C17 : 1{omega}8c and C17 : 0 were the major fatty acids. The DNA G+C content was 71.5 mol%. Strain DS-17T exhibited 16S rRNA gene sequence similarity values of 94.5–96.9 % to the type strains of recognized Nocardioides species. Strain DS-17T could be distinguished from recognized Nocardioides species by differences in phenotypic characteristics. On the basis of phenotypic, chemotaxonomic and phylogenetic data, strain DS-17T is considered to represent a novel species of the genus Nocardioides, for which the name Nocardioides terrigena sp. nov. is proposed. The type strain is DS-17T (=KCTC 19217T=JCM 14582T).

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain DS-17T is EF363712.

A table detailing the differential phenotypic characteristics of strain DS-17T and related Nocardioides species is available as supplementary material with the online version of this paper.


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The genus Nocardioides was proposed by Prauser (1976)Go. At the time of writing, it comprised 23 recognized species, including the recently described species Nocardioides lentus (Yoon et al., 2006aGo), N. kongjuensis (Yoon et al., 2006bGo), N. furvisabuli (Lee, 2007Go), N. insulae (Yoon et al., 2007Go), N. marinus (Choi et al., 2007Go) and N. panacihumi (An et al., 2007Go). Here we report the taxonomic characterization of a Nocardioides-like strain, DS-17T, which was isolated from soil in Dokdo, Korea.

A soil sample collected from Dokdo (3 ° 14' 12'' N 13 ° 52' 07'' E) was used as a source for the isolation of bacterial strains. Strain DS-17T was isolated by using the standard dilution plating technique at 25 °C on 10x diluted nutrient agar (Difco). The morphological, physiological and biochemical characteristics of strain DS-17T were investigated via routine cultivation on R2A agar (Difco) at 25 °C. Morphological, physiological, cultural and biochemical properties were examined as described by Yoon et al. (2005a)Go. Growth at various NaCl concentrations (0, 0.5, 1.0, 2.0, 3.0, 4.0 and 5.0 %, w/v) was investigated in liquid R2A medium (R2A broth) prepared according to the formula of the Difco medium except that agar was not added. The pH range for growth was determined in R2A broth that was adjusted to various pH values (pH 4.0–10.5 at intervals of 0.5 pH units) by the addition of HCl and Na2CO3. The susceptibility to various antibiotics was tested on R2A agar plates by using antibiotic discs as follows: polymyxin B (100 U), streptomycin (50 µg), penicillin G (20 U), chloramphenicol (100 µg), ampicillin (10 µg), cephalothin (30 µg), gentamicin (30 µg), novobiocin (5 µg), tetracycline (30 µg), kanamycin (30 µg), lincomycin (15 µg), oleandomycin (15 µg), neomycin (30 µg), carbenicillin (100 µg). Utilization of various substrates, enzyme activities and other physiological and biochemical properties were tested by using the API 20E, API 20NE, API 50 CH and API ZYM systems (bioMérieux); utilization of various substrates was determined by inoculating the API 50 CH strip with cells suspended in AUX medium (bioMérieux). Morphological, cultural, physiological and biochemical characteristics of strain DS-17T are given in the species description (see below) or are detailed in Table 1Go and Supplementary Table S1 (available in IJSEM Online).


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  		Table 1. Differential phenotypic characteristics of strain DS-17T and two phylogenetically related Nocardioides species

Taxa: 1, strain DS-17T; 2, N. pyridinolyticus; 3, N. aquiterrae. Data taken from Yoon et al. (1997Go, 2004Go) and this study. +, Positive reaction; –, negative reaction; W, weakly positive reaction. All are positive for Gram-stain, catalase, nitrate reduction, hydrolysis of casein and gelatin, utilization of D-xylose, glucose, fructose, cellobiose, maltose, sucrose, trehalose, starch and D-turanose, esterase lipase (C8), leucine arylamidase, naphthol-AS-BI-phosphohydrolase and {alpha}-glucosidase. All are negative for hydrolysis of hypoxanthine and urea, utilization of glycerol, erythritol, D-arabinose, L-xylose, adonitol, methyl beta-D-xyloside, mannose, sorbose, dulcitol, sorbitol, methyl {alpha}-D-mannoside, methyl {alpha}-D-glucoside, N-acetylglucosamine, amygdalin, salicin, inulin, raffinose, glycogen, xylitol, D-tagatose, D-fucose, L-fucose, L-arabitol, 2-ketogluconate, 5-ketogluconate, caprate, citrate and phenylacetate, lipase (C14), {alpha}-chymotrypsin, {alpha}-galactosidase, beta-glucuronidase, N-acetyl-beta-glucosaminidase, {alpha}-mannosidase and {alpha}-fucosidase.

 
Cell biomass for DNA extraction and for the analyses of cell-wall and isoprenoid quinones was obtained by cultivation for 3 days at 30 °C in R2A broth. For fatty acid methyl ester analysis, cell mass of strain DS-17T was harvested from R2A agar plates after incubation for 7 days at 30 °C. Molecular systematic and chemotaxonomic studies were performed as described by Yoon et al. (2005a)Go. The isomer type of the diamino acid in the cell-wall peptidoglycan was analysed by using TLC according to the method described by Komagata & Suzuki (1987)Go.

The almost complete 16S rRNA gene sequence of strain DS-17T determined in this study comprised 1470 nt (approximately 96 % of the Escherichia coli 16S rRNA gene sequence). Comparative 16S rRNA gene sequence analyses showed that strain DS-17T was affiliated most closely to the genus Nocardioides (Fig. 1Go). In the neighbour-joining phylogenetic tree based on 16S rRNA gene sequences, strain DS-17T fell within the radiation of the cluster comprising Nocardioides species (Fig. 1Go). Strain DS-17T exhibited highest 16S rRNA gene sequence similarity values (96.9 %) to the type strains of Nocardioides aquiterrae, Nocardioides pyridinolyticus and Nocardioides kribbensis. Strain DS-17T exhibited 16S rRNA gene sequence similarity values of 94.5–96.7 % to the type strains of other Nocardioides species and of less than 94.7 % to other species used in the phylogenetic analysis.


Figure 1
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  		Fig. 1. Neighbour-joining phylogenetic tree based on 16S rRNA gene sequences showing the positions of strain DS-17T and related taxa. Bootstrap values (expressed as percentages of 1000 replications) of >50 % are shown at branch points. Filled circles indicate that the corresponding nodes were also recovered in the trees generated with the maximum-likelihood and maximum-parsimony algorithms. Open circles indicate that the corresponding nodes were also recovered in the tree generated with the maximum-likelihood or maximum-parsimony algorithms. Bar, 0.01 substitutions per nucleotide position.

 
Chemotaxonomic properties confirmed the phylogenetic affiliation of strain DS-17T as a member of the genus Nocardioides (Tamura & Yokota, 1994Go; Yoon et al., 1997Go; Lawson et al., 2000Go; Urzì et al., 2000Go; Wang et al., 2001Go). The diagnostic diamino acid found in strain DS-17T was LL-2,6-diaminopimelic acid, which is characteristic of wall chemotype I sensu Lechevalier & Lechevalier (1970)Go. Strain DS-17T contained menaquinone-8(H4) as the predominant isoprenoid quinone. The fatty acid profile of strain DS-17T included the following (each constituting >0.5 % of the total fatty acids): branched fatty acids iso-C16 : 0 (35.5 %), iso-C17 : 0 (2.3 %), iso-C15 : 0 (1.6 %), iso-C16 : 1 (1.5 %), iso-C14 : 0 (1.3 %), iso-C18 : 0 (1.3 %) and anteiso-C17 : 0 (1.2 %); unsaturated fatty acids C17 : 1{omega}8c (30.2 %), C18 : 1{omega}9c (2.7 %), C17 : 1{omega}6c (1.1 %) and C15 : 1{omega}6c (0.8 %); straight-chain fatty acids C17 : 0 (11.5 %), C15 : 0 (2.6 %) and C16 : 0 (1.7 %); 10-methyl fatty acid C17 : 0 (1.8 %); summed feature 3 (C16 : 1{omega}7c and/or iso-C15 : 0 2-OH, 1.6 %); and hydroxy fatty acid C17 : 0 3-OH (1.1 %). Tuberculostearic acid was not detected. This fatty acid profile was similar to those of recognized Nocardioides species, although there were differences in the proportions of some components, particularly iso-C16 : 0, C17 : 1{omega}8c and C17 : 0, perhaps because of differences in cultivation and extraction conditions (Yoon et al., 1997Go, 1999Go, 2004Go, 2005aGo, bGo, 2006aGo, bGo, 2007Go; Yi & Chun, 2004Go; Kubota et al., 2005Go). The DNA G+C content of strain DS-17T was 71.5 mol%. Strain DS-17T differed from recognized Nocardioides species in several phenotypic characteristics (Table 1Go and Supplementary Table S1 in IJSEM Online). The phylogenetic distinctiveness, together with differential phenotypic properties, were sufficient to allocate strain DS-17T to a species that is separate from all recognized Nocardioides species (Stackebrandt & Goebel, 1994Go). Therefore, on the basis of the data presented, strain DS-17T is considered to represent a novel species of the genus Nocardioides, for which the name Nocardioides terrigena sp. nov. is proposed.

Description of Nocardioides terrigena sp. nov.
Nocardioides terrigena (ter.ri.ge'na. L. masc. or fem. n. terrigena child of the earth, referring to the isolation of the type strain from soil).

Cells are aerobic, non-spore-forming, rods or cocci (0.4–0.7 µmx0.7–2.0 µm) in the exponential phase of growth. Cells show rod-to-coccus morphogenesis from the early exponential phase to the stationary phase. Gram-positive but Gram-variable in old cultures. Colonies are circular, slightly convex, smooth, glistening, ivory in colour and 1.0–1.2 mm in diameter after 7 days incubation on R2A agar at 30 °C. Neither substrate nor aerial mycelia are formed. Growth occurs at 4 and 35 °C, but not at 36 °C. Optimal pH for growth is around 8.0. Growth occurs in the presence of 0–3 % (w/v) NaCl with optimum growth in the presence of 0.5–1.0 % (w/v) NaCl. Arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase and tryptophan deaminase are absent. H2S and indole are not produced. Tweens 20, 40 and 60 are hydrolysed. Adipate, L-malate, starch, gentiobiose, D-turanose and gluconate are utilized as sole carbon and energy sources and D-lyxose is weakly utilized, but caprate, citrate, phenylacetate, glycerol, erythritol, D-arabinose, L-xylose, methyl beta-D-xyloside, sorbose, dulcitol, methyl {alpha}-D-mannoside, methyl {alpha}-D-glucoside, N-acetylglucosamine, amygdalin, arbutin, aesculin, salicin, inulin, glycogen, xylitol, D-tagatose, D-fucose, L-fucose, D-arabitol, L-arabitol, 2-ketogluconate and 5-ketogluconate are not. Susceptible to ampicillin, carbenicillin, cephalothin, chloramphenicol, kanamycin, lincomycin, neomycin, novobiocin, oleandomycin, penicillin G and streptomycin and weakly susceptible to tetracycline, but not to gentamicin or polymyxin B. The cell-wall peptidoglycan contains LL-2,6-diaminopimelic acid as the diagnostic diamino acid. The predominant menaquinone is MK-8(H4). The major fatty acids (>10 % of the total fatty acids) are iso-C16 : 0, C17 : 1{omega}8c and C17 : 0. The DNA G+C content is 71.5 mol% (determined by HPLC). Other phenotypic characteristics are given in Table 1Go and Supplementary Table S1 (available in IJSEM Online).

The type strain, DS-17T (=KCTC 19217T=JCM 14582T), was isolated from soil.


   ACKNOWLEDGEMENTS
 
This work was supported by the 21C Frontier Program of Microbial Genomics and Applications (grant MG05-0401-2-0) from the Ministry of Science and Technology (MOST) of the Republic of Korea.


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