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. 2012 Jul;62(Pt 7):1587–1591. doi: 10.1099/ijs.0.034751-0

Nonomuraea soli sp. nov., an actinomycete isolated from soil

Yan-Ru Cao 1,2, Rong-Xian Jin 1, Yi Jiang 1,✉, Wen-Xiang He 2, Cheng-Lin Jiang 1
PMCID: PMC3541754  PMID: 21890732

Abstract

A straight-chain, spore-forming actinobacterium, strain YIM 120770T, was isolated from soil. Phylogenetic analysis on the basis of 16S rRNA gene sequence comparisons revealed that the isolate represents a distinct cluster within the clade comprising the genus Nonomuraea and is related most closely to Nonomuraea rhizophila YIM 67092T (96.5 % similarity). Cells of strain YIM 120770T grew in the presence of 0–3 % (w/v) NaCl, at 15–37 °C and at pH 7.0–8.0. The diagnostic amino acid was meso-diaminopimelic acid, cell hydrolysates contained madurose, glucose, mannose, ribose and galactose, the predominant cellular fatty acids were 10-methyl C17 : 0 and iso-C16 : 0, and the DNA G+C content was 66.4 mol%, data consistent with affiliation of strain YIM 120770T to the genus Nonomuraea. Strain YIM 120770T shared low levels of 16S rRNA gene sequence similarity (<97 %) with the type strains of recognized species of the genus Nonomuraea and could be differentiated from its closest phylogenetic relative based on phenotypic characteristics. These results suggested that strain YIM 120770T represents a novel species of the genus Nonomuraea, for which the name Nonomuraea soli sp. nov. is proposed. The type strain is YIM 120770T ( = DSM 45533T = JCM 17347T).

The etymology of the genus Nonomuraea was corrected by Chiba et al. (1999) following description of the genus Nonomuria by Zhang et al. (1998). At the time of writing, the genus comprised 26 recognized species and two subspecies (http://www.bacterio.cict.fr/n/nonomuraea.html).

In an attempt to investigate the diversity of actinomycetes from Weibao Mountain in Dali, Yunnan province, China, numerous strains were obtained and characterized taxonomically. Preliminary comparative 16S rRNA gene sequence analysis showed that one of these strains, designated YIM 120770T, formed a separate lineage within the genus Nonomuraea. As a consequence, it was subjected to further taxonomic study by using a polyphasic approach, which included determination of its phenotypic properties and detailed phylogenetic analysis based on 16S rRNA gene sequences.

A soil sample was collected from an altitude of 2670 m from Weibao Mountain in south-west China in April 2010. The soil suspension was diluted and spread onto mycose-proline agar [5 g mycose, 1 g proline, 1 g (NH4)2SO4, 1 g NaCl, 2 g CaCl2, 1 g K2HPO4, 1 g MgSO4 . 7H2O, 3.7 mg vitamin mixture (Hayakawa & Nonomura, 1987), 20 g agar, pH 7.2] after incubation at 28 °C for 30 days.

General cell morphology was studied by light microscopy (Olympus BH-2) and scanning electron microscopy (QUANTA200; FEI) of a 21-day-old culture of strain YIM 120770T grown on ISP 2 agar medium (Shirling & Gottlieb, 1966). For cultural characterization, strain YIM 120770T was grown for 28 days at 28 °C on ISP media 2, 3, 4 and 5 (Shirling & Gottlieb, 1966), nutrient agar (Difco), Czapek’s agar (Waksman, 1967) and potato-dextrose agar. The colours of substrate and aerial mycelia and any soluble pigments produced were determined by comparison with chips from the colour charts of the Inter-Society Color Council (Kelly, 1964). Temperature and pH ranges for growth and NaCl tolerance were determined on ISP medium 2 as described by Xu et al. (2005). Catalase and oxidase activity was detected by the method of Wang et al. (2008). Hydrolysis of starch, cellulose, gelatin, Tweens 20, 40, 60 and 80, milk coagulation and peptonization, reduction of nitrate, urease activity and H2S production were determined as described by Smibert & Krieg (1994). Utilization of compounds as sole carbon and nitrogen sources was tested according to Gordon et al. (1974).

Strain YIM 120770T for chemotaxonomic analyses was cultured in ISP 2 broth at 28 °C for 14 days. Diaminopimelic acids and whole-cell sugars were analysed according to the methods described by Hasegawa et al. (1983) and Tang et al. (2009), respiratory quinones were extracted according to Collins et al. (1977) and identified by HPLC (Groth et al., 1996), and analysis of polar lipids was performed by TLC as described by Minnikin et al. (1979) and Collins & Jones (1980). Biomass for fatty acid analysis was harvested from a Bacto trypticase soy broth shaker after 7 days at 28 °C. Nonomuraea rhizophila YIM 67092T was used in parallel for the above experiments. Cellular fatty acid methyl esters were prepared as described by Sasser (1990) and analysed according to the standard protocol of the Microbial Identification System (Sherlock Version 6.1; MIDI database: TSBA6). GC was performed with an Agilent Technologies 7890A system.

Genomic DNA was extracted and purified, and PCR-mediated amplification of the 16S rRNA gene was performed as described by Li et al. (2007). The 16S rRNA gene sequence of strain YIM 120770T was aligned with corresponding sequences obtained from the DDBJ/EMBL/GenBank databases by using the EzTaxon server (http://147.47.212.35:8080/) (Chun et al., 2007). Multiple alignment of the data was performed by using the program clustal x (Thompson et al., 1997). Phylogenetic and molecular evolutionary analyses were conducted with the neighbour-joining (Saitou & Nei, 1987), maximum-parsimony (Fitch, 1971) and maximum-likelihood (Felsenstein, 1981) methods. A phylogenetic tree was constructed by using the neighbour-joining method of Saitou & Nei (1987) with mega version 4 (Tamura et al., 2007). Evolutionary distance matrices (distance options according to the Kimura two-parameter model) were calculated as described by Kimura (1980). The tree topology was assessed by using bootstrap analysis with 1000 replicated datasets (Felsenstein, 1985). The DNA G+C content of strain YIM 120770T was determined by reversed-phase HPLC of nucleosides according to Mesbah et al. (1989).

The 16S rRNA gene sequence of strain YIM 120770T showed 94.3–96.5 % similarity to those of the type strains of all recognized species of the genus Nonomuraea. Strain YIM 120770T was related most closely to the type strain of N. rhizophila YIM 67092T (96.5 % 16S rRNA gene sequence similarity), and phylogenetic analysis based on 16S rRNA gene sequences showed that strain YIM 120770T formed a cluster with the type strains of N. rhizophila YIM 67092T and Nonomuraea rosea GW 12687T (96.1 % 16S rRNA gene sequence similarity) (Fig. 1), which was supported by a high bootstrap value (78 %). This cluster did not form any definite clusters with other closely related Nonomuraea strains. 16S rRNA gene sequence analysis thus suggested that strain YIM 120770T represents a novel species of the genus Nonomuraea. The DNA G+C content of strain YIM 120770T was 66.4 mol%.

Fig. 1.

Fig. 1.

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Neighbour-joining phylogenetic tree based on nearly complete 16S rRNA gene sequences (1524 nt) showing the relationship between strain YIM 120770T and members of the genus Nonomuraea. Numbers at branch nodes are bootstrap values based on 1000 resamplings; only values ≥50 % are shown. The sequence of Planotetraspora phitsanulokensis A-T 1383T was used as an outgroup. Bar, 0.005 substitutions per nucleotide position.

With regard to chemotaxonomic characteristics, strain YIM 120770T had meso-diaminopimelic acid as the diagnostic diamino acid in the cell-wall peptidoglycan, and madurose, mannose and galactose as diagnostic sugars. The major menaquinones were MK-9(H4) (68.8 %), MK-9(H6) (14.9 %) and MK-9(H2) (14.5 %), and the polar lipids comprised diphosphatidylglycerol, phosphatidylmethylethanolamine, phosphatidylethanolamine, OH-phosphatidylethanolamine, OH-phosphatidylmonomethylethanolamine, phosphatidylglycerol, phosphatidylinositol, phosphatidylinositol mannoside, an unknown aminophosphoglycolipid and three unknown phospholipids (see Fig. S1 in IJSEM Online). The predominant fatty acids were 10-methyl C17 : 0 (12.8 %), iso-C16 : 0 (11.9 %), C17 : 1ω6c (9.2 %), anteiso-C15 : 0 (7.4 %) and C16 : 0 (7.4 %). Other components were C17 : 1ω8c (5.8 %), 10-methyl C16 : 0 (5.4 %), iso-C14 : 0 (5.3 %), iso-C15 : 0 (5.0 %), summed feature 3 (C16 : 1ω7c and/or C16 : 1ω6c; 4.6 %), C14 : 0 (3.6 %), C18 : 0 (2.6 %), iso-C16 : 1 G (2.5 %), C16 : 0 2-OH (2.5 %), C17 : 0 (2.3 %), C15 : 0 2-OH (2.2 %), anteiso-C17 : 0 (2.1 %), C13 : 0 (1.9 %), 10-methyl C18 : 0 (1.4 %), C18 : 1ω9c (1.3 %), iso-C17 : 0 (0.8 %), C17 : 0 2-OH (0.6 %), iso-C18 : 0 (0.3 %), anteiso-C15 : 1 A (0.2 %), iso-C15 : 1 G (0.2 %), C14 : 0 2-OH (0.2 %), anteiso-C17 : 1 A (0.2 %), C12 : 0 3-OH (0.2 %) and iso-C13 : 0 (0.1 %).

Strain YIM 120770T formed extensively branched substrate mycelia and aerial mycelia on ISP 2 agar, spore chains borne on aerial mycelia were straight and the spore surfaces were smooth (Fig. 2). Good growth was observed on ISP 2 and nutrient media, and moderate growth was seen on other media tested. Orange–yellow to orange substrate mycelia and white aerial mycelia appeared on all media tested. No diffusible pigment was produced on any medium. Other physiological properties are given in the species description below and in Table 1.

Fig. 2.

Fig. 2.

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Scanning electron micrograph of spiral spore chains on aerial mycelium of strain YIM 120770T grown on ISP 2 at 28 °C for 21 days. Bar, 5 µm.

Table 1. Characteristics that differentiate strain YIM 120770T from the type strains of Nonomuraea rhizophila and Nonomuraea rosea.

Strains: 1, YIM 120770T; 2, N. rhizophila YIM 67092T; 3, N. rosea GW 12687T. Data are from the present study except where indicated. nd, Not determined.

Characteristic 1 2 3*
Spore chain Straight Spiral* Spiral
Spore ornamentation Smooth Rough* nd
Max. NaCl tolerance (%) 3 7 5
Oxidase + − +
Milk coagulation − + nd
Milk peptonization − + nd
Urea hydrolysis − + −
Nitrate + − nd
Tween 20 − + −
Carbon source utilization:
 Cellobiose − + +
 d-Fructose − + +
 myo-Inositol − + +
 Lactose − + +
 Glycerol + − nd
 d-Xylose + − +
Nitrogen source utilization:
 Hypoxanthine − + +
 Xanthine − + +
Polar lipids† DPG, PG, PME, PE, OH-PME, OH-PE, APGL, PI, PIM, 3PLs DPG, PG, PME, PE, PI, GluNu, PLs* DPG, PG, PME, PE, OH-PME, OH-PE, APGL, PI, PIMs, PL1
Major fatty acids (≥5 %) 10-methyl C17 : 0 (12.8 %), iso-C16 : 0 (11.9 %), C17 : 1ω6c (9.2 %), anteiso-C15 : 0 (7.4 %), C16 : 0 (7.4 %), C17 : 1ω8c (5.8 %), 10-methyl C16 : 0 (5.4 %), iso-C14 : 0 (5.3 %), iso-C15 : 0 (5.0 %) 10-methyl C17 : 0 (26.7 %), iso-C16 : 0 (24.0 %), iso-C16 : 1 G (14.1 %), C17 : 1ω6c (5.6 %) iso-C16 : 0 (43.4 %), 10-methyl C17 : 0 (19.8 %), C17 : 1ω6c (10.2 %), iso-C16 : 1 G (6.9 %)
Menaquinones MK-9(H4) (68.8 %), MK-9(H6) (14.9 %), MK-9(H2) (14.5 %) MK-9(H4) (82.4 %), MK-9(H6) (12.6 %), MK-9(H2) (5.0 %) MK-9(H4) (76 %), MK-9(H2) (11 %), MK-9(H6) (6 %), MK-9 (6 %)
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†

DPG, Diphosphatidylglycerol; PG, phosphatidylglycerol; PL, phospholipid; PME, phosphatidylmethylethanolamine; PE, phosphatidylethanolamine; OH-PME, OH-phosphatidylmonomethylethanolamine; OH-PE, OH-phosphatidylethanolamine; APGL, unknown aminophosphoglycolipid; PI, phosphatidylinositol; PIM, phosphatidylinositol mannoside; GluNu, unknown glucosamine-containing phospholipid.

16S rRNA gene sequence analysis (Fig. 1) showed that strain YIM 120770T belongs to the genus Nonomuraea. It formed extensively branched substrate and aerial mycelia and straight chains of spores with a smooth ornamentation. The diagnostic diamino acid, cell hydrolysates, predominant menaquinones, polar lipids (Fig. S1), major fatty acids and DNA G+C content were all consistent with its classification in the genus Nonomuraea.

However, strain YIM 120770T could be differentiated phenotypically from its closest phylogenetic neighbours, N. rhizophila YIM 67092T and N. rosea GW 12687T, based on morphology (Fig. 2). In addition, strain YIM 120770T differed from N. rhizophila YIM 67092T and N. rosea GW 12687T in utilization of cellobiose, d-fructose, myo-inositol, lactose, hypoxanthine and xanthine. In the polar lipid profile, strain YIM 120770T contained OH-phosphatidylmonomethylethanolamine, OH-phosphatidylethanolamine and an unknown aminophosphoglycolipid, which were lacking in N. rhizophila YIM 67092T and N. rosea GW 12687T. Strain YIM 120770T also differed from N. rhizophila YIM 67092T and N. rosea GW 12687T in lacking iso-C16 : 1 G as a major fatty acid (≥5.0 %). Strain YIM 120770T lacked MK-9, which accounts for 6 % in strain N. rosea GW 12687T. Differential characteristics among strain YIM 120770T, N. rhizophila YIM 67092T and N. rosea GW 12687T are given in Table 1.

On the basis of data from the present taxonomic study, we conclude that strain YIM 120770T represents a novel species of the genus Nonomuraea, for which the name Nonomuraea soli sp. nov. is proposed.

Description of Nonomuraea soli sp. nov.

Nonomuraea soli (so′li. L. neut. gen. n. soli of soil, the source of the type strain).

Substrate mycelia are orange–yellow to orange and aerial mycelia are white. Spore chains are straight, and show a smooth ornamentation. No diffusible pigment is produced. Growth occurs at 15–37 °C (optimum 28 °C), at pH 7.0–8.0 (optimum pH 7.0) and in the presence of 0–3 % NaCl (optimum 0 %). Positive for catalase, oxidase and nitrate reductase; negative for hydrolysis of starch, cellulose, gelatin, and Tweens 20, 40, 60 and 80, milk coagulation and peptonization, urease activity and H2S production. Utilizes glucose, maltose, d-mannose, d-mannitol, raffinose, l-rhamnose, glycerol, d-sorbitol, d-xylose, xylitol, succinic acid and sodium dl-malate, but not cellobiose, d-fructose, myo-inositol, lactose, l-arabinose, d-galactose, dextrin, dulcitol, fucose or l-sorbose. Utilizes l-serine and adenine as sole nitrogen sources, but not hypoxanthine or xanthine. The diagnostic diamino acid is meso-diaminopimelic acid. Cell hydrolysates contain madurose, ribose, mannose, glucose and galactose. The predominant menaquinones are MK-9(H4), MK-9(H6) and MK-9(H2). Polar lipids include diphosphatidylglycerol, phosphatidylmethylethanolamine, phosphatidylethanolamine, OH-phosphatidylethanolamine, OH-phosphatidylmonomethylethanolamine, phosphatidylglycerol, phosphatidylinositol, phosphatidylinositol mannoside, an unknown aminophosphoglycolipid and three unknown phospholipids. Major fatty acids are 10-methyl C17 : 0, iso-C16 : 0, C17 : 1ω6c, anteiso-C15 : 0 and C16 : 0.

The type strain, YIM 120770T ( = DSM 45533T = JCM 17347T), was isolated from Weibao Mountain, south-west China. The DNA G+C content of the type strain is 66.4 mol%.

Acknowledgements

This research was supported by the National Natural Science Foundation of China (no. 30900002 and no. 21062028), National Major Scientific and Technology Special Projects (2009ZX09302-003) and National Institutes of Health (1P41GM086184-01A1).

Footnotes

One supplementary figure is available with the online version of this paper.

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