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Int J Syst Evol Microbiol 54 (2004), 453-456; DOI  10.1099/ijs.0.02814-0
© 2004 International Union of Microbiological Societies

Nocardiopsis aegyptia sp. nov., isolated from marine sediment

Soraya A. Sabry1, Nevine B. Ghanem1, Gehan A. Abu-Ella1, Peter Schumann2, Erko Stackebrandt2 and Reiner M. Kroppenstedt2

1 Alexandria University, Faculty of Science, Division: Microbiology, PO Box, Alexandria, Egypt
2 DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen, Mascheroder Weg 1b, 38124 Braunschweig, Germany

Correspondence
Reiner M. Kroppenstedt
kdt{at}dsmz.de


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An actinomycete, strain SNG49T, was isolated from marine sediment of Abu Qir Bay, on the western seashore of Alexandria, Egypt. The bacterium was aerobic and Gram-positive. It produced beige to light-yellow aerial mycelium, brown substrate mycelium and straight to flexuous hyphae, but no specific spore chains. 16S rDNA sequence analysis and chemotaxonomic markers were consistent with classification of strain SNG49T in the genus Nocardiopsis, i.e. meso-diaminopimelic acid; no diagnostic sugars; phosphatidylcholine, phosphatidylmethylethanolamine, phosphatidylinositol, phosphatidylglycerol and diphosphatidylglycerol as polar lipids; menaquinones of the MK-10 series from MK-10(H0) to MK-10(H8); and iso/anteiso-branched and 10-methyl-branched fatty acids, the principal fatty acids being anteiso-17 : 0 and tuberculostearic acid. Nocardiopsis lucentensis and Nocardiopsis alba are the phylogenetic neighbours of strain SNG49T, respectively showing 98·8 and 98·7 % 16S rRNA gene sequence similarity; however, moderate DNA–DNA reassociation values between these two species and strain SNG49T (44 and 60 %, respectively) showed that strain SNG49T could be clearly separated from them. These data, together with distinct physiological traits, led to the conclusion that this isolate represents a novel species within the genus Nocardiopsis, for which the name Nocardiopsis aegyptia is proposed. The type strain is SNG49T (=DSM 44442T=NRRL B-24244T).

Abbreviations: DPG, diphosphatidylglycerol; PC, phosphatidylcholine; PG, phosphatidylglycerol; PI, phosphatidylinositol; PME, phosphatidylmethylethanolamine

The GenBank accession number for the 16S rRNA gene sequence of strain DSM 44442T is AJ539401.


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Nocardiopsis strains are distributed ubiquitously in the environment (Kroppenstedt & Evtushenko, 2002Go). They are frequently isolated from habitats with moderate to high salt concentrations such as saline soil or marine sediments (Al-Zarban et al., 2002Go; Al-Tai & Ruan, 1994Go; Evtushenko et al., 2000Go) and salterns (Chun et al., 2000Go). The aim of this study was to classify strain SNG49T, a novel strain isolated from marine sediment, by morphological, physiological, chemotaxonomic and molecular biological methods.

Strain SNG49T was isolated from marine sediment taken at a depth of 20 cm on the seashore of Abu Qir Bay, west of Alexandria, Egypt, using dilution plating on ISP agar supplemented with 5 % NaCl (Shirling & Gottlieb, 1966Go). Determination of morphological traits and colours of the aerial and substrate mycelium, as well as of soluble pigments, was done as described by Shirling & Gottlieb (1966)Go. Biochemical tests were performed according to Kroppenstedt & Evtushenko (2002)Go and Al-Zarban et al. (2002)Go. Strain SNG49T showed the typical macroscopic and microscopic appearance of most species of the genus Nocardiopsis (Meyer, 1994Go), with dirty white aerial mycelium, which becomes light- to dark-yellowish grey in ageing cultures grown on GYM medium (4 g glucose, 4 g yeast extract, 10 g malt extract l-1). The substrate mycelium was brownish. No pigments were released into the medium. The hyphae of the aerial mycelium were straight to flexuous. In older cultures, hyphae of aerial mycelium disintegrated into spore-like structures.

Carbon sources utilized by strain SNG49T are listed in Table 1Go. The strain grew at 10 and 40 °C and in 5 % NaCl, but was not able to grow in the presence of 10 % NaCl. Optimal growth was observed at 25–28 °C.


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  		Table 1. Diagnostic characteristics of Nocardiopsis species that are phylogenetically related to strain DSM 44442T and of the type strain of the type species, N. dassonvillei subsp. dassonvillei DSM 43111T

Strains: 1, DSM 44442T; 2, N. prasina DSM 43845T; 3, N. metallicus DSM 44598T; 4, N. exhalans DSM 44407T; 5, N. listeri DSM 40297T; 6, N. alba DSM 43377T; 7, N. tropica DSM 44381T; 8, N. umidischolae DSM 44362T; 9, N. lucentensis DSM 44048T; 10, N. dassonvillei subsp. dassonvillei DSM 43111T. Data were taken from Kroppenstedt & Evtushenko (2002)Go, Peltola et al. (2001)Go (N. exhalans and N. umidischolae) and Schippers et al. (2002)Go (N. metallicus). +, Positive; -, negative; V, variable; ND, no data. None of the strains grew at 45 °C.

 
Cell material used for chemotaxonomic analyses was obtained from cultures grown in trypticase soy broth (BBL) for 4 days at 28 °C on a rotary shaker. Cells were harvested by centrifugation and washed twice with distilled water. Analyses of amino acid and sugars were carried out using the methods of Staneck & Roberts (1974)Go. Menaquinones and polar lipids were extracted following the procedure of Minnikin et al. (1984)Go. Polar lipids and menaquinones were respectively analysed by TLC (Minnikin et al., 1977Go) and HPLC (Kroppenstedt, 1982Go, 1985Go). Fatty acids were analysed according to the methods of Miller (1982)Go and Sasser (1990)Go. The presence of mycolic acids was determined by the method of Minnikin et al. (1975)Go.

Whole-cell hydrolysates of strain SNG49T contained meso-diaminopimelic acid as the diamino acid in the peptidoglycan. Galactose, glucose and ribose were the only sugars found in the hydrolysates (cell wall type III, according to Lechevalier & Lechevalier, 1980Go). The diagnostic sugars arabinose, xylose and madurose could not be detected. Strain SNG49T synthesized menaquinones from MK-10(H0) to MK-10(H8) (for quantitative distribution, see the species description). The polar lipids comprised the diagnostic phospholipids phosphatidylcholine (PC) and phosphatidylmethylethanolamine (PME) and the non-diagnostic phosphatidylinositol (PI), phosphatidylglycerol (PG) and diphosphatidylglycerol (DPG) (i.e. phospholipid type III, according to Lechevalier et al., 1977Go). This pattern matched quite well with those found in Nocardiopsis species (Kroppenstedt & Evtushenko, 2002Go). The fatty acid composition revealed mainly iso/anteiso-branched and 10-methyl-branched fatty acids. The principal fatty acids were 14-methyl hexadecanoic acid (anteiso-17 : 0) and 10-methyl octadecanoic acid (tuberculostearic acid). This combination of fatty acids is diagnostic for species of the genus Nocardiopsis (fatty acid pattern 3d sensu Kroppenstedt & Evtushenko, 2002Go). Qualitative and quantitative distributions are given in the species description. Mycolic acids were not detected. All chemotaxonomic properties of strain SNG49T were consistent with its classification in the genus Nocardiopsis (Kroppenstedt & Evtushenko, 2002Go).

Genomic DNA extraction, PCR-mediated amplification of the 16S rDNA and purification of PCR products were carried out as described previously (Rainey et al., 1996Go). The ae2 editor (Maidak et al., 1999Go) was used to align the almost complete 16S rDNA sequence of strain SNG49T (1487 nt) against the 16S rDNA gene sequences of representatives of the main actinobacterial lineages and then against sequences of members of the genus Nocardiopsis. Phylogenetic analyses followed described methods (De Soete, 1983Go; Felsenstein, 1993Go). With intrageneric sequence similarities ranging between 95·9 and 98·8 %, strain SNG49T was most closely related to members of the genus Nocardiopsis, especially to Nocardiopsis lucentensis (98·8 % similarity) and Nocardiopsis alba (98·7 %). These similarity values are lower than those found for some other individual pairs of Nocardiopsis species, e.g. Nocardiopsis tropica DSM 44381T and Nocardiopsis umidischolae DSM 44362T (99·2 %); Nocardiopsis metallicus DSM 44598T and Nocardiopsis exhalans DSM 44407T (99·5 %); or N. metallicus DSM 44598T and Nocardiopsis prasina DSM 43845T (99·4 %). Both distance-matrix and maximum-likelihood analyses gave consistent results in that strain SNG49T clustered adjacent to the type strains of N. lucentensis, N. alba and related strains, but bootstrap values for the branching points of most Nocardiopsis type strains were low (<50 %) (Fig. 1Go).



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  		Fig. 1. 16S rDNA dendrogram (De Soete, 1983Go) displaying the phylogenetic position of strain DSM 44442T and phylogenetically related members of the genus Nocardiopsis. Numbers at nodes indicate percentages of bootstrap samplings, derived from 1000 resamplings; values less than 50 % are not shown. Bar, 2 % sequence divergence. More distantly related members of the genus served as a root.

 
DNA was isolated by chromatography on hydroxyapatite by the procedure of Cashion et al. (1977)Go. DNA–DNA hybridization was carried out as described by Huß et al. (1983)Go using a Gilford 2600 spectrophotometer equipped with a Gilford 2527-R thermoprogrammer and plotter. Reassociation was performed under optimal conditions [2xSSC+10 % (v/v) DMSO at 68 °C] and was recorded using a Gilford 2600 spectrophotometer (Huß et al., 1983Go; Jahnke, 1992Go). The DNA–DNA relatedness of strain SNG49T to N. lucentensis DSM 44048T was 44 %, whereas the value for N. alba DSM 43377T was 60 %. These values are below the threshold value of about 70 %, recommended by Wayne et al. (1987)Go for assigning strains to the same species.

Automated ribotyping was carried out with the RiboPrinter microbial characterization system (Qualicon; DuPont). Sample preparation and analysis were performed according to the manufacturer's instructions using PvuII to generate restriction fragments. The RiboPrint pattern of strain SNG49T confirmed that this strain differed from the type strains of both phylogenetic neighbours and representatives of other Nocardiopsis species (Fig. 2Go).



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  		Fig. 2. RiboPrint patterns of Nocardiopsis strains. Fragments were generated from DNA by PvuII.

 
Based on the phenotypic, chemotaxonomic and genotypic data, it is concluded that SNG49T represents a novel species in the genus Nocardiopsis; the name Nocardiopsis aegyptia sp. nov. is proposed. Isolate SNG49T is currently the only strain of this species.

The phylogenetic position of this organism is within the cluster defined by N. lucentensis and N. alba (Fig. 1Go). Strain SNG49T can be differentiated from described Nocardiopsis species by a combination of morphological, physiological and chemotaxonomic data: by morphology from Nocardiopsis synnemataformans, which produces synnemata, and Nocardiopsis listeri, which does not produce a well-developed aerial mycelium; by physiology from Nocardiopsis halophila and Nocardiopsis halotolerans, which can grow at 15 % NaCl or higher; and by the ability of strain SNG49T to use nearly all of the carbon sources investigated, except L-arabinose (see Table 1Go). Chemotaxonomically, Nocardiopsis species fall into two groups: those that synthesize mainly menaquinones with highly saturated isoprenoid side-chains, i.e. SNG49T, Nocardiopsis dassonvillei subsp. dassonvillei, N. alba, Nocardiopsis kunsanensis, N. prasina, N. lucentensis, Nocardiopsis trehalosi, N. tropica and N. halophila; and others, including N. halotolerans, N. dassonvillei subsp. albirubida, N. listeri and N. synnemataformans, that contain non-saturated isoprene units (Kroppenstedt & Evtushenko, 2002Go).

Description of Nocardiopsis aegyptia sp. nov.
Nocardiopsis aegyptia (ae.gyp.ti'a. L. fem. adj. aegyptia from Egypt, referring to the country of isolation).

Aerobic, Gram-positive, non-motile actinomycete that forms dirty white aerial mycelium, becoming light-yellowish grey in ageing cultures. No endo- or exopigments produced. Hyphae of the aerial mycelium are straight to flexuous. In older cultures, hyphae of aerial mycelium disintegrate into spore-like structures. Optimal growth obtained on GYM at 28 °C. Grows at 10 °C and in 5 % NaCl, but not at 45 °C or in 10 % NaCl. Physiological reactions are indicated in Table 1Go. Whole cell hydrolysates contain meso-diaminopimelic acid, but no diagnostic sugars. Menaquinones are: MK-10(H0), 6 %; MK-10(H2), 7 %; MK-10(H4), 19 %; MK-10(H6), 38 %; and MK-10(H8), 30 %. Traces of MK-9(H4) and MK-9(H6) are also found. Polar lipids are PC, PME, PI, PG and DPG. The fatty acid composition (>1 % of total) is as follows: iso-C14 : 0 (12·12 %), iso-C15 : 0 (1·70 %), iso-C16 : 0 (19·14 %), iso-C17 : 0 (5·10 %), iso-C18 : 0 (3·16 %), anteiso-C15 : 0 (6·49 %), anteiso-C17 : 0 (17·85 %), anteiso-C17 : 1 (1·35 %), 10-methyl C16 : 0 (1·50 %), 10-methyl C17 : 0 (2·58 %), 10-methyl C18 : 0 (12·19 %), C16 : 0 (4·21 %), C16 : 1 (1·10 %), C17 : 0 (1·72 %), C17 : 1 (1·72 %), C18 : 0 (7·32 %) and C18 : 1 (7·76 %). Mycolic acids are absent.

The type strain is SNG49T (=DSM 44442T=NRRL B-24244T), isolated from marine sediments at a depth of 20 cm on the seashore of Abu Qir Bay, west of Alexandria, Egypt.


   ACKNOWLEDGEMENTS
 
We thank Ina Kramer, Gabriele Pötter, Bettina Sträubler and Jolantha Swiderski for technical assistance.


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