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1 Instituto de Recursos Naturales y Agrobiologia de Sevilla, CSIC, Apartado 1052, 41080 Sevilla, Spain
2 All-Russian Collection of Microorganisms (VKM), G. K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, Moscow Region 142292, Russia
3 Hans-Knöll-Institut für Naturstoff-Forschung, Beutenbergstrasse 11a, 07745 Jena, Germany
Correspondence
C. Saiz-Jimenez
saiz{at}irnase.csic.es
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for filamentous, nutritionally fastidious, catalase- and oxidase-negative soil isolates. Zgurskaya et al. (1992) emended the description of the genus and described two species each including two subspecies, Agromyces cerinus subsp. cerinus, A. cerinus subsp. nitratus, Agromyces fucosus subsp. fucosus and A. fucosus subsp. hippuratus, which are characterized by rapid growth on peptone/yeast extract medium and positive catalase and oxidase reactions. Although the proposal of A. cerinus and its subspecies was substantiated by numerical analysis and their respective DNA–DNA relatedness values, the description of A. fucosus subsp. hippuratus was based only on phenotypic traits (Zgurskaya et al., 1992). Subsequently, Suzuki et al. (1996) analysed DNA–DNA relatedness in representatives of the genus Agromyces and found that values between the type strains of A. fucosus subsp. fucosus and A. fucosus subsp. hippuratus were in the range 45–47 %, which is lower than the value of 70 % usually considered to indicate delineation of separate species (Wayne et al., 1987). Recently, five additional Agromyces species have been described, Agromyces bracchium, Agromyces luteolus, Agromyces rhizospherae (Takeuchi & Hatano, 2001), Agromyces aurantiacus (Li et al., 2003) and Agromyces albus (Dorofeeva et al., 2003).
During a study to identify Agromyces strains isolated from caves, Laiz et al. (2000) performed phylogenetic analyses based on the nearly complete 16S rRNA gene sequences of A. fucosus subsp. fucosus VKM Ac-1345T (1473 bp; AY158025) and A. cerinus subsp. nitratus VKM Ac-1351T (1465 bp; AY277619) obtained in this study and the 16S rRNA gene sequences of other Agromyces strains available from public DNA databases. The analysis was performed using the software package ARB (Ludwig et al., 1998) with the neighbour-joining algorithm and the results showed that A. fucosus subsp. fucosus VKM Ac-1345T and A. fucosus subsp. hippuratus VKM Ac-1352T are significantly distant (Fig. 1). They exhibited 96·7 % 16S rRNA gene binary sequence similarity, which is lower than the threshold usually reported for members of a single bacterial species (Stackebrandt & Goebel, 1994; Roselló-Mora & Amann, 2001). The 16S rRNA gene sequence similarities between the type strains of different Agromyces species are in the range 96·5–98·5 % based on sequences of over 1400 bp.
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Tm) as described by De Ley et al. (1970). We found a significant Tm (5·6 °C) between A. fucosus subsp. fucosus and A. fucosus subsp. hippuratus, which is above the value of 5 °C used to indicate separate species (Roselló-Mora & Amann, 2001). This result is in agreement with DNA–DNA relatedness values (45–47 %) reported for these strains by Suzuki et al. (1996). The above data demonstrate that A. fucosus subsp. fucosus and A. fucosus subsp. hippuratus belong to different genomic species (Wayne et al., 1987).
On the basis of previously published data, it was not possible unambiguously to conclude whether A. fucosus subsp. hippuratus represents a separate genomic species within the genus Agromyces, because its relationship with A. cerinus subsp. nitratus is vague. Our phylogenetic analysis based on 16S rRNA gene sequences showed that A. fucosus subsp. hippuratus VKM Ac-1352T is different from both A. cerinus subsp. nitratus VKM Ac-1351T and A. cerinus subsp. cerinus VKM Ac-1340T (Fig. 1
), exhibiting 97·8 and 98·4 % 16S rRNA gene sequence similarities to these strains, respectively. Investigation of DNA–DNA relatedness between A. fucosus subsp. hippuratus VKM Ac-1345T and A. cerinus subsp. nitratus VKM Ac-1352T revealed a Tm of 9·6 °C, suggesting these strains belong to different species (Roselló-Mora & Amann, 2001). Similar analyses performed on the type strains of A. cerinus subsp. cerinus and A. cerinus subsp. nitratus revealed a small Tm (4·1 °C) and confirmed their close DNA–DNA relatedness, as reported by Zgurskaya et al. (1992) and Suzuki et al. (1996).
At the phenotypic level, A. fucosus subsp. hippuratus differs from A. fucosus subsp. fucosus and from both subspecies of A. cerinus with regard to cell wall teichoic acid composition, which are water-soluble carbohydrate-containing polymers covalently linked to peptidoglycan by phosphodiester bridges and which occur in many Gram-positive bacteria (Baddiley, 1972; Naumova et al., 2001). Two strains of A. fucosus subsp. hippuratus (VKM Ac-1352T and VKM Ac-1353) contained 1,5-poly(ribitol phosphate) with tetrasaccharide substituents (Gnilozub et al., 1994; Naumova et al., 2001), whereas four strains of A. fucosus subsp. fucosus (VKM Ac-1345T, VKM Ac-1346, VKM Ac-1347 and VKM Ac-1349) contained 1,3-poly(glycerol phosphate) with 
-N-acetylglucosamine substituents (Malysheva, 1994). Five analysed strains of A. cerinus subsp. cerinus (VKM Ac-1340T, VKM Ac-1342, VKM Ac-1343, VKM Ac-1344 and VKM Ac-1350) contained poly(arabitol phosphate) teichoic acid, and A. cerinus subsp. nitratus VKM Ac-1351T, the only known strain of this subspecies, contained poly(ribofuranosylribitol phosphate) polymer in the cell wall (Shashkov et al., 1993, 1995; Malysheva, 1994; Naumova et al., 2001). The structures and combinations of cell wall teichoic acids are considered of high taxonomic value and were shown to be usually species-specific in all actinomycete genera in which they were analysed (for references, see Naumova et al., 2001). These data are consistent with a clear physiological discrimination between A. fucosus subsp. hippuratus and other recognized species (Zgurskaya et al., 1992; Suzuki et al., 1996; Takeuchi & Hatano, 2001; Li et al., 2003; Dorofeeva et al., 2003). In addition, representatives of the A. fucosus subspecies were reported to differ in polyamine composition (Altenburger et al., 1997); for instance, A. fucosus subsp. fucosus contained putrescine and 1,3-diaminopropane whereas A. fucosus subsp. hippuratus contained putrescine and spermidine.
Fatty acid profiles of the type strains of A. fucosus and A. hippuratus were analysed using the Sherlock Microbial Identification System (MIDI) (Sasser, 1991). They showed only slight differences in their percentages of iso- and anteiso-15 : 0 to 17 : 0 fatty acids, which appeared to be of little value for species differentiation. The cellular fatty acid compositions determined in A. fucosus subsp. hippuratus and A. fucosus subsp. fucosus are, respectively, as follows (%): iso-C14 : 0, 0·9 and 0·6; n-C14 : 0, 0·2 and 0·4; iso-C15 : 0, 10·5 and 6·4; anteiso-C15 : 0, 51·7 and 47·2; n-C15 : 0, 0·1 and 0·1; iso-C16 : 0, 14·3 and 14·6; n-C16 : 0, 1·5 and 1·0; iso-C17 : 0, 1·9 and 2·3; anteiso-C17 : 0, 18·1 and 27·5; n-C18 : 0, 0·1 and 0·2.
Thus, based on the 16S rRNA gene sequence analysis, DNA–DNA relatedness values and differences in phenotypic traits obtained in this and earlier studies (Zgurskaya et al., 1992; Suzuki et al., 1996; Takeuchi & Hatano, 2001; Dorofeeva et al., 2003), we propose to reclassify A. fucosus subsp. hippuratus as a separate species, Agromyces hippuratus sp. nov., comb. nov. (type strain VKM Ac-1352T), and to emend the description of A. fucosus. The latter is restricted to strains assigned previously to A. fucosus subsp. fucosus (Zgurskaya et al., 1992).
Description of Agromyces hippuratus sp. nov., comb. nov.
Agromyces hippuratus (hip.pu.ra'tus. N.L. n. hippuratum hippurate; N.L. masc. adj. hippuratus pertaining to hippurate, relating to the ability to decompose hippurate).
Basonym: Agromyces fucosus subsp. hippuratus Zgurskaya et al. 1992.
The description is based on phenotypical data of Zgurskaya et al. (1992), Gnilozub et al. (1994), Malysheva (1994), Groth et al. (1996), Suzuki et al. (1996), Altenburger et al. (1997) and Dorofeeva et al. (2003). Colonies on nutrient media are opaque, entire, convex and usually penetrate into the agar media. Produces a yellow carotenoid pigment. Branching hyphae (width, 0·2–0·6 mm) break into diphtheroid and rod-like, irregular, non-motile fragments. Aerobic, catalase- and oxidase-positive. Mesophilic; optimum growth is at 26–30 °C. Strains are able to grow at 7 °C; weak or no growth occurs at 37 °C. D-Arabinose, cellobiose, D-fructose, D-galactose, D-glucose, maltose, D-mannose, melezitose, melibiose, L-rhamnose, salicin, sucrose, trehalose and D-xylose are used for growth as sole carbon sources in a salt medium supplemented with 0·1 % (w/v) yeast extract (Zgurskaya et al., 1992). Adonitol, dulcitol, meso-inositol, lyxose, D-mannitol, methyl -D-arabinopyranoside and L-sorbose are not used as sole carbon sources in the same medium. Acids are produced from D-arabinose, glycerol and L-rhamnose; no acid production from cellobiose, inulin, lactose, maltose, raffinose, D-ribose, salicin or trehalose. Acid production from L-arabinose and sucrose is variable. Fumarate, hippurate, malate and pyruvate are utilized. No alkaline reactions with ascorbate, citrate, gluconate, oxalate, propionate, salicylate, succinate and tartrate are observed; some strains show positive reaction with trans-aconitate. Nitrate is reduced to nitrite and tyrosinase is produced. Aesculin, hypoxanthine and starch are hydrolysed. Adenine, elastin, guanine, pectin, testosterone, urea and xanthine are not decomposed or hydrolysed. Casein is usually not hydrolysed. Indole test is negative. No growth occurs on media supplemented with 5 % NaCl, 0·01 % sodium azide or 0·0175 % potassium tellurite. The major menaquinone is MK-12 with a minor amount of MK-13. Polyamine content is low; putrescine and spermidine are predominant compounds (data for the type strain only). Cell wall sugars are rhamnose, galactose and trace mannose. Cell wall contains 1,5-poly(ribitol phosphate) teichoic acid. The G+C content of the DNA is about 71 mol%. Isolated from soil.
The type strain is VKM Ac-1352T (=JCM 9087T). The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of this strain is D45061.
Emended description of Agromyces fucosus
The description is based on phenotypical data of Zgurskaya et al. (1992), Malysheva (1994), Groth et al. (1996), Suzuki et al. (1996), Altenburger et al. (1997) and Dorofeeva et al. (2003).
Colonies on nutrient media are opaque, entire and convex, and occasionally penetrate into the agar media. Produces a yellow carotenoid pigment. Branching hyphae (width, 0·2–0·6 mm) break into diphtheroid and rod-like, irregular, non-motile fragments. Catalase- and oxidase-positive. Mesophilic; optimum growth is at 26–30 °C. Strains are able to grow at 7 °C; no or weak growth occurs at 37 °C. D-Arabinose, cellobiose, D-fructose, D-galactose, D-glucose, maltose, D-mannose, melezitose, methyl D-glucoside, L-rhamnose, salicin, sucrose, trehalose and D-xylose are used for growth as sole carbon sources in a salt medium supplemented with 0·1 % (w/v) yeast extract (Zgurskaya et al., 1992). Dulcitol, erythritol, lyxose, D-mannitol, methyl--D-arabinopyranoside and L-sorbose are not used as sole carbon sources in the same medium. Some strains, including the type strain, use melibiose for growth, whereas adonitol and meso-inositol are not used by most of the strains, including the type strain. Acids are usually produced from L-arabinose, cellobiose, glycerol, inulin, lactose, maltose, L-rhamnose, salicin, sucrose and D-xylose by most strains (reactions of the type strain are positive or variable). Acetate, malate and pyruvate are utilized. Alkaline reactions with fumarate and propionate are variable (type strain is positive). Some strains utilize citrate and succinate (type strain is negative). Ascorbate, trans-aconitate, gluconate, oxalate, salicylate and tartrate are not utilized. Production of H2S is variable; the type strain shows a positive reaction. Arbutin, aesculin and starch are hydrolysed; adenine, elastin, guanine, pectin, testosterone, urea and xanthine are not decomposed or hydrolysed. Hippurate, hypoxanthine, Tween 40 and tyrosine are decomposed by some strains, including the type strain. Casein is usually not hydrolysed. Indole test is negative. Nitrate reduction test is negative or weak reaction is observed. No growth occurs on media supplemented with 5 % NaCl, 0·01 % sodium azide or 0·0175 % potassium tellurite. The major menaquinone is MK-12; the second most common component is MK-13. Polyamine content is low; putrescine and 1,3-diaminopropane are the predominant compounds (data for the type strain only). Cell wall sugars are galactose, rhamnose, fucose and minor mannose (type strain); glucose may occur but fucose is lacking in other strains. Cell wall contains 1,3-poly(glycerol phosphate) teichoic acid. The G+C content of the DNA is 70–72 mol%. Isolated from soil.
The type strain is VKM Ac-1345T (=DSM 8597T). The GenBank accession number for the 16S rRNA gene sequence of this strain is AY158025.
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ACKNOWLEDGEMENTS |
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