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Int J Syst Evol Microbiol 53 (2003), 303-307; DOI  10.1099/ijs.0.02350-0
© 2003 International Union of Microbiological Societies

Note

Agromyces aurantiacus sp. nov., isolated from a Chinese primeval forest

Wen-Jun Li1, Li-Ping Zhang1, Ping Xu1, Xiao-Long Cui1, Li-Hua Xu1, Zhongse Zhang1, Peter Schumann2, Erko Stackebrandt2 and Cheng-Lin Jiang1

1 The Key Laboratory for Microbial Resources of Ministry of Education, PR China, Yunnan Institute of Microbiology, Yunnan University, Kunming, Yunnan 650091, China
2 DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen, Mascheroder Weg 1b, D-38124 Braunschweig, Germany

Correspondence
Cheng-Lin Jiang
lihxu{at}ynu.edu.cn


   ABSTRACT
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A catalase-negative actinomycete, strain YIM 21741T, was isolated from a soil sample collected from a primeval forest at Xishuangbanna, Yunnan Province, China. Analysis of 16S rDNA showed the strain to be related to members of the genus Agromyces, with which it also shares morphological characteristics, e.g. branching hyphae breaking into diphtheroid and rod-like, irregular, non-motile fragments and a peptidoglycan containing the diagnostic amino acid 2,4-diamino-n-butyric acid. Whole-cell hydrolysates of strain YIM 21741T contained rhamnose and small quantities of glucose, galactose and mannose. The major menaquinone was MK-12, while MK-13 and MK-12 were minor components. Diagnostic phospholipids were phosphatidylglycerol and diphosphatidylglycerol. The G+C content of the DNA was 72·8 mol%. Physiological and biochemical characteristics reveal strain YIM 21741T to be different from all validly described species of the genus Agromyces. As DNA–DNA similarity values between this isolate and the phylogenetically neighbouring type strains of Agromyces bracchium and Agromyces luteolus are only moderate, the novel species Agromyces aurantiacus sp. nov. is proposed with strain YIM 21741T (=CCTCC 001012T =AS 4.1717T =DSM 14598T) as the type strain.

Abbreviations: DAB, 2,4-diamino-n-butyric acid; ISP, International Streptomyces Project

The GenBank/EMBL/DDBJ accession number for the 16S rDNA sequence of strain YIM 21741T is AF389342.


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The genus Agromyces was proposed by Gledhill & Casida (1969)Go for the soil organism Agromyces ramosus, a filamentous, branching, catalase-negative actinomycete. The emended genus (Zgurskaya et al., 1992Go) includes seven species and two subspecies, which are characterized chemotaxonomically by menaquinone MK-12 and a peptidoglycan with 2,4-diamino-n-butyric acid (DAB) as the principal amino acid. Here, we report the description of a novel member of the genus, Agromyces aurantiacus sp. nov., based upon the description of strain YIM 21741T.

Strain YIM 21741T, isolated on humic acid-vitamin (HV) agar medium (Hayakawa & Nonomura, 1987Go) after about 2 weeks incubation at 28 °C, originates from a soil sample collected from Xishuangbanna in Yunnan Province, China. The strain was maintained on agar slants of International Streptomyces Project (ISP) media 2 (yeast extract-malt extract) and 5 (glycerol-asparagine) at 4 °C and as glycerol suspensions (20 %, v/v) at -20 °C. Biomass for chemical and molecular-systematic studies was obtained following growth in shake flasks (about 200 r.p.m.) of ISP2 broth, supplemented with the vitamin mixtures of the HV medium (Hayakawa & Nonomura, 1987Go) at 28 °C for 2 weeks.

Morphological features were determined on ISP2 after 3 weeks at 28 °C. Strain YIM 21741T had morphological characteristics typical of the genus Agromyces (Fig. 1Go), in that branching hyphae broke up into diphtheroid and rod-like, irregular, non-motile fragments. Cell dimensions are 0·5–0·9x1·0–1·4 µm. Cultural characteristics were determined after 2 weeks at 28 °C by methods used in the ISP (Shirling & Gottlieb, 1966Go). Strain YIM 21741T showed good growth on all media tested (Table 1Go). Colour determinations (Table 1Go) were made by comparing the pure cultures with colour chips from the ISCC-NBS Color Charts Standard Samples no. 2106 (Kelly, 1964Go). Media and procedures used for examination of physiological and biochemical features and carbon-source utilization were those described by Shirling & Gottlieb (1966)Go and Williams et al. (1989)Go. The results are indicated in Table 2Go in comparison with those of phylogenetically related Agromyces species. On tryptone soy broth agar (Oxoid), 16 h and 4 day old cultures were catalase-negative.



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  		Fig. 1. Morphology of strain YIM 21741T grown on ISP2. Bar, 1 µm.

 

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  		Table 1. Cultural characteristics of strain YIM 21741T

 

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  		Table 2. Characteristics that differentiate YIM 21741T from the type strains of its phylogenetic neighbours

All strains are negative for nitrate reduction and urease; all strains are positive for starch hydrolysis and produce acid from aesculin, fructose, glucose, maltose, mannitol, mannose, melibiose, rhamnose and sucrose. Acid production from fructose, glucose and mannitol was negative using the non-commercial test described in the text. Data for reference strains were taken from Takeuchi & Hatano (2001)Go, based on API 50CH tests.

 
Metabolic properties were determined using the API Coryne, API 50CHE and API 50CHL test kits (bioMérieux), the latter processed under aerobic conditions. Acid production from fructose, glucose, arabinose, mannitol and xylose was also analysed aerobically by colour change of bromocresol purple (0·04 %) in medium containing (l-1) 1·0 g (NH4)2HPO4, 0·2 g KCl, 0·2 g MgSO4.7H2O, 0·2 g yeast extract, 15·0 g agar and sterile-filtered substrate (final concentration 1 %). Under these conditions, growth was positive on fructose, glucose, arabinose, mannitol and xylose but acid was not produced. Similarly, acid was not produced using the API Coryne substrate panel. Acid production was tested by the API 50CHE substrate panel. Reactions are listed in either Table 3Go or the species description.


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  		Table 3. Cellular fatty acid compositions of strain YIM 21741T and related strains of the genus Agromyces

Strains: 1, YIM 21741T; 2, A. luteolus IFO 16235T; 3, A. bracchium IFO 16238T; 4, A. rhizospherae IFO 16236T; 5, A. mediolanus JCM 3346T; 6, A. ramosus JCM 3108T. Values are percentages of the total fatty acids. Data for reference strains were taken from Suzuki et al. (1996)Go and Takeuchi & Hatano (2001)Go.

 
Cell walls were purified and analysed using the TLC method of Lechevalier & Lechevalier (1980)Go. The procedures of Becker et al. (1964)Go and Lechevalier & Lechevalier (1980)Go were used for analysis of principal amino acids: the principal component was DAB. The main component of whole-cell hydrolysates, determined according to Takahashi & Egusa (1992)Go, was rhamnose. Phospholipid analysis was carried out using the method of Minnikin et al. (1979)Go and Collins & Jones (1980)Go. Phosphatidylglycerol and diphosphatidylglycerol were detected as the diagnostic phospholipids. Menaquinones were extracted using the procedures of Collins et al. (1977)Go and identified as described by Groth et al. (1996)Go; the principal menaquinone was MK-12. Fatty acids (Table 3Go) were determined following the procedure of Takeuchi & Hatano (1998)Go. On a variety of different media, Agromyces type strains synthesize anteiso-C15 : 0, anteiso-C17 : 0 and iso-C16 : 0 as predominant fatty acids.

Genomic DNA, used in the determination of G+C content and 16S rDNA amplification, was extracted using a procedure (Hopwood et al., 1985Go) slightly modified by Cui et al. (2001)Go. The base composition of strain YIM 21741T was determined by the thermal denaturation method (Mandel & Marmur, 1968Go). 16S rDNA was amplified by PCR using TaKaRa ExTaq as described previously (Cui et al., 2001Go). Following a BLAST search (Altschul et al., 1997Go), the sequences with the highest scores were retrieved from various databases. Calculations of levels of sequence similarity were carried out using CLUSTAL W 1.74 (Higgins et al., 1992Go). The phylogenetic tree was reconstructed using the neighbour-joining method of Saitou & Nei (1987)Go from Knuc values (Kimura, 1980Go) and the algorithm of De Soete (1983)Go. The topology of the phylogenetic tree was evaluated by bootstrap resampling (Felsenstein, 1985Go) with 1000 replicates. The almost complete 16S rDNA sequence of strain YIM 21741T (1464 bp) revealed the highest similarity to members of Agromyces (95·1–97·6 %). Dendrograms of relatedness obtained with different algorithms were identical with respect to the position of strain YIM 21741T, which formed a distinct branch with its closest relatives Agromyces luteolus IFO 16235T (97·9 % similarity) and Agromyces bracchium IFO 16238T (97·2 %). Agromyces mediolanus DSM 20152T branched slightly deeper. A phylogenetic dendrogram, based on the algorithms of De Soete (1983)Go, is depicted in Fig. 2Go.



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  		Fig. 2. 16S rDNA dendrogram (De Soete, 1983Go) displaying the phylogenetic position of strain YIM 21741T and some related members of the genus Agromyces. Numbers indicate percentages of bootstrap support, derived from 1000 resamplings. Bar, 1 % sequence divergence.

 
DNA–DNA reassociation was performed to determine the relatedness between strain YIM 21741T, A. bracchium IFO 16238T and A. luteolus IFO 16235T, which appeared as the closest relatives as judged from 16S rDNA analysis. DNA was isolated as described by Cashion et al. (1977)Go and Escara & Hutton (1980)Go and DNA–DNA reassociation (Huß et al., 1983Go; Jahnke, 1992Go), performed under optimal conditions (2x times; SSC with 10 % dimethyl sulphoxide at 70 °C), was recorded with a Gilford 2600 spectrophotometer. Relatedness values determined for strain YIM 21741T were respectively 52 and 50 % with the type strains of A. bracchium and A. luteolus. The interspecies similarity value of the latter two species was 67 %. This value was significantly higher than that reported by Takeuchi & Hatano (2001)Go (13 %) using the fluorometric hybridization method of Ezaki et al. (1989)Go. These authors also determined the degree of binding of A. luteolus and A. bracchium to A. mediolanus. As the binary values were low (respectively 21 and 24 %), A. mediolanus was also not considered to be related to strain YIM 21741T at the strain level.

Taxonomic conclusions
Based on the morphology, chemotaxonomy, base composition of DNA and 16S rDNA sequence, strain YIM 21741T is a member of the genus Agromyces, where it forms a distinct branch together with A. luteolus, A. bracchium and A. mediolanus. Based on differences in phenotypic properties, we suggest that strain YIM 21741T represents a novel species of the genus. This is substantiated by DNA–DNA reassociation values of significantly less than 70 %, determined for strain YIM 21741T and A. luteolus (50 %) and A. bracchium (52 %). These three taxa differ from each other in acid production from various carbohydrates, as determined by the API 50C system (Table 2Go). While A. luteolus IFO 16235T shows mainly negative reactions (7 of 25), A. bracchium IFO 16238T forms acid from almost all carbohydrates (21 of 25). Strain YIM 21741T shows an intermediate reaction, in that acid is produced from 16 of 25 sources. The acid production pattern of strain YIM 21741T is also different from those of other type strains of Agromyces species listed by Takeuchi & Hatano (2001)Go. The close phylogenetic neighbour A. mediolanus IFO 15704T differs from strain YIM 21741T in nitrate reduction, urease production, starch hydrolysis and acid production from amygdalin, ribose, rhamnose and salicin. The name Agromyces aurantiacus sp. nov. is proposed for the novel species.

Description of Agromyces aurantiacus sp. nov.
Agromyces aurantiacus (au.ran.ti.a'cus. N.L. fem. adj. aurantiacus orange-coloured).

Gram-positive, non-acid-fast and aerobic. Catalase-negative. Branching hyphae break up into diphtheroid and rod-like, irregular, non-motile fragments. Colony pigmentation and formation of aerial mycelium are indicated in Table 1Go. The cell wall contains DAB. Whole-cell hydrolysates contain rhamnose and small quantities of galactose, glucose and mannose. Optimal growth temperature is 28 °C. Milk coagulation is positive, gelatin liquefaction, milk peptonization, H2S production and melanin production are negative. The following substrates are utilized: glucose, galactose, fructose, sucrose, xylose, raffinose, D-arabinose, inulose, sorbitol, mannitol and inositol. Lactose and rhamnose are not utilized. According to the API Coryne system, positive for {alpha}-glucosidase and aesculin, weakly positive for {beta}-galactosidase and negative for alkaline phosphatase, {beta}-glucuronidase, N-acetyl-{beta}-glucosaminidase and gelatin hydrolysis. According to the API 50CHE test system, positive for inulin, weakly positive for L-arabinose and negative for erythritol, D-arabinose, adonitol, L-sorbose, dulcitol, sorbitol, lactose, xylitol, L-lyxose, D-tagatose, D- and L-fucose and D- and L-arabitol. Other physiological and biochemical properties are indicated in Table 2Go. The predominant cellular fatty acids are iso-C16 : 0, anteiso-C 15 : 0 and anteiso-C17 : 0. Phosphatidylglycerol and diphosphatidylglycerol are the predominant phospholipids. The major menaquinone is MK-12; minor components are MK-13 and MK-11. Fatty acids are indicated in Table 3Go. The G+C content of the DNA of the type strain is 72·8 mol%.

The type strain, YIM 21741T, was isolated from a soil sample collected from Xishuangbanna in Yunnan Province, China, and has been deposited in the Chinese Center of Type Culture Collection as strain CCTCC 001012T (=AS 4.1717T =DSM 14598T).


   ACKNOWLEDGEMENTS
 
This research was supported by Key Laboratory for Microbial Resources of Ministry of Education, PR China and Yunnan Provincial Natural Science Foundation. We thank Bettina Sträubler for performing the DNA–DNA reassociation experiments, Anja Frühling for the determination of metabolic properties and Anika Vester for some chemotaxonomic analysis.


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