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Int J Syst Evol Microbiol 53 (2003), 1503-1507; DOI  10.1099/ijs.0.02522-0
© 2003 International Union of Microbiological Societies

Promicromonospora vindobonensis sp. nov. and Promicromonospora aerolata sp. nov., isolated from the air in the medieval ‘Virgilkapelle’ in Vienna

Hans-Jürgen Busse1,2, Christian Zlamala1,2, Sandra Buczolits1,2, Werner Lubitz1, Peter Kämpfer3 and Mariko Takeuchi4,{dagger}

1 Institut für Mikrobiologie und Genetik, Universität Wien, A-1030 Wien, Austria
2 Institut für Bakteriologie, Mykologie und Hygiene, Veterinärmedizinische Universität, Veterinärplatz 1, A-1210 Wien, Austria
3 Institut für Angewandte Mikrobiologie, Justus-Liebig-Universität, Giessen D-35392, Germany
4 Institute for Fermentation, Osaka, 17-85 Juso-honmachi 2-chome, Yodogawa-ku, Osaka 532-8686, Japan

Correspondence
Hans-Jürgen Busse
hans-juergen.busse{at}vu-wien.ac.at


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Two airborne bacterial isolates designated V45T and V54AT were characterized in order to determine their taxonomic position. 16S rDNA sequence analysis showed that the two isolates shared 98·1 % sequence similarity. Highest sequence similarities (98·0–98·5 %) were found to Promicromonospora citrea DSM 43110T and Promicromonospora sukumoe IFO 14650T. Detection of a quinone system with the predominant compound MK-9(H4), a polar lipid pattern containing phosphatidylglycerol, a fatty acid profile with the predominant acids C15 : 0 iso and C15 : 0 anteiso and the diagnostic cell-wall diamino acid L-lysine supported the assignment of the novel isolates to the genus Promicromonospora. The two isolates could be distinguished from P. sukumoe by the presence of glycine in the peptidoglycan, and the detection of the cell-wall sugar galactose differentiates them from the two established species of the genus Promicromonospora. Each of the two isolates displayed a unique biochemical profile. Results from DNA–DNA hybridizations clearly demonstrated that V45T and V54AT represent separate species. Based on these data, it is proposed that V45T (=IFO 16525T=CCM 7044T) and V54AT (=IFO 16526T =CCM 7043T) be classified as the type strains of two novel Promicromonospora species, for which the names Promicromonospora vindobonensis sp. nov. and Promicromonospora aerolata sp. nov. are proposed.

Published online ahead of print on 6 June 2003 as DOI 10.1099/ijs.0.02522-0.

The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences of strains V45T and V54AT are AJ487302 and AJ487303.

DNA–DNA hybridization results and micrographs of cells of the novel strains are available as supplementary material in IJSEM Online.

{dagger}Present address: Takeda Chemical Industries, 17-85, Juso-honmachi 2-chome, Yodogawa-ku, Osaka 532-8686, Japan. Back


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In a study concerning bacterial diversity in the air of the medieval ‘Virgilkapelle’ chapel beneath the ‘Stephansplatz’ square in Vienna, airborne bacteria were collected using a BIOTEST Hycon RCS Plus air-sampler and subcultivated on PYES agar (Zlamala et al., 2002aGo). Strains displaying similar colony types were compared to each other by their protein patterns obtained after SDS-PAGE (Altenburger et al., 1996Go). If protein patterns indicated a relationship at the species level, representatives were selected for further characterization employing partial 16S rDNA sequencing and analysis of chemotaxonomic characteristics including polyamine patterns, polar lipid profiles, cell-wall diamino acids, fatty acids and quinone systems. Based on their classification, the isolates were identified as members of the genera Arthrobacter, Promicromonospora, Moraxella (C. Zlamala and H.-J. Busse, unpublished results), Agrococcus (Zlamala et al., 2002aGo) and Microbacterium (Zlamala et al., 2002bGo). Here, we report the detailed characterization of two Promicromonospora isolates designated V45T and V54AT that did not display any similarities in their protein patterns.

The genus Promicromonospora currently consists of two species, Promicromonospora citrea (Krasilnikov et al., 1961Go) and Promicromonospora sukumoe (Takahashi et al., 1987Go). A third species, Promicromonospora enterophila, has been transferred to the re-established genus Oerskovia as Oerskovia enterophila (Stackebrandt et al., 2002Go). Although reported to form monospores (Krasilnikov et al., 1961Go), this observation was not confirmed by other studies (Lechevalier & Lechevalier, 1981Go). Species of the genus are characterized by the production of mycelia that fragment into bacillary or coccoid elements. Phylogenetically, the genus Promicromonospora is most closely related to the genera Rarobacter, Cellulosimicrobium, Oerskovia and Cellulomonas (Schumann et al., 2001Go).

16S rDNA studies
16S rRNA-encoding genes were analysed as described by Zlamala et al. (2002a)Go. The resulting 16S rDNA sequences of V45T and V54AT respectively consisted of 1342 (positions 81–1444; Escherichia coli numbering) and 1393 (29–1442; E. coli numbering) nucleotides. In a FASTA search (Pearson & Lipman, 1988Go), the two isolates shared 98·1 % sequence similarity. Isolates V45T and V54AT exhibited highest sequence similarities (98.3–98·4 % and 98·1–98·3 %, respectively) to the type strains of the two established species P. citrea (DSM 43110T) and P. sukumoe (IFO 14650T). The 16S rDNA sequences were aligned with published sequences available from DDBJ, EMBL and GenBank. Phylogenetically, the two isolates were located on the Promicromonospora lineage and the degree of branching was supported by high bootstrap values (Fig. 1Go).



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  		Fig. 1. Dendrogram based on 16S rDNA sequences showing the phylogenetic relationships of Promicromonospora species and related genera. The dendrogram was constructed after multiple alignment of data by CLUSTAL_X (Thompson et al., 1997Go). Distances (distance options according to the Kimura-2 model) and clustering with maximum-parsimony method were performed by using the software package MEGA version 2.1 (Kumar et al., 2001Go). Bootstrap values based on 1000 replications are given at branching points.

 
DNA studies
The G+C content of strains V45T and V54AT was analysed according to the methods of Mesbah et al. (1989)Go and Tamaoka & Komagata (1984)Go and determined to be 70 mol%. DNA–DNA hybridization experiments were carried out as described previously (Ezaki et al., 1989Go). The results (Supplementary Table A, available in IJSEM Online) demonstrated that strains V45T and V54AT represent two separate, previously unrecognized species.

Chemotaxonomic characteristics
The quinone systems of both isolates, analysed according to the procedure of Ventosa et al. (1993)Go, contained the predominant menaquinone MK-9(H4). In addition, the quinone system of strain V45T contained 4 % MK-9(H2) and 4 % MK-9(H6) and the quinone system of V54AT contained 7 % MK-9(H2). Polar lipids were analysed as described by Tindall (1990)Go. The polar lipid profile of V45T consisted of diphosphatidylglycerol, phosphatidylglycerol, two unknown glycolipids, three unknown phosphoglycolipids, one unknown phospholipid and one unknown polar lipid. The polar lipid profile of V54AT consisted of diphosphatidylglycerol, phosphatidylglycerol, two unknown glycolipids, two unknown phosphoglycolipids and one unknown phospholipid. Both the quinone systems and the polar lipid compositions are in excellent agreement with the characteristics reported for representatives of the genus Promicromonospora (Kalakoutskii et al., 1989Go; Takahashi et al., 1987Go). Fatty acids were analysed as described by Kämpfer & Kroppenstedt (1996)Go. Both isolates had a fatty acid profile similar to that of P. citrea IFO 12397T and P. sukumoe IFO 14650T, which contained the predominant acids C15 : 0 anteiso and C15 : 0 iso and moderate amounts of C16 : 0 and C17 : 0 anteiso (Table 1Go). The two isolates were only distinguishable from each other and from reference strains of the genus by quantitative differences and the presence/absence of some minor acids. Cell walls were prepared and analysed according to Schleifer & Kandler (1972)Go and amino acid and sugar compositions were identified by HPLC as described by Takeuchi et al. (1999)Go. The cell wall of V45T consisted of Glu : Gly : Ala : Lys (0·98 : 0·69 : 2·88 : 1·0) and that of V54AT consisted of Glu : Gly : Ala : Lys (1·05 : 0·43 : 3·4 : 1·0). Asp and Ser could not be detected in their cell walls. Based on these results, the structure of the linkage may be Gly–Ala, suggesting peptidoglycan type A3{alpha} (Schleifer & Kandler, 1972Go). The cell-wall sugars of strains V45T and V54AT were rhamnose (respectively 14 and 4 %), galactose (both 37 %) and glucose (49 and 59 %). The presence of glycine in the peptidoglycan distinguishes the two isolates from P. sukumoe IFO 14650T, and the presence of the cell-wall sugar galactose has not been reported for either species of Promicromonospora (Takahashi et al., 1987Go).


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  		Table 1. Major fatty acid components of Promicromonospora strains

Strains: 1, P. vindobonensis sp. nov. V45T; 2, P. aerolata sp. nov. V54AT; 3, P. sukumoe IFO 14650T; 4, P. citrea IFO 12397T. Values are percentages of total fatty acids. Isolates V45T and V54AT were grown at 28 °C on GYM agar (l-1 distilled water: 4 g glucose, 4 g yeast extract, 10 g malt extract, 2 g CaCO3, 12 g agar); the remaining strains were grown on trypticase soy agar at 28 °C prior to analysis. Fatty acid nomenclature: the position of the double bond in an unsaturated fatty acid can be located by counting from the methyl ({omega}) end of the carbon chain; cis isomers are indicated by the suffix c. Summed feature 5 contains 18 : 2{omega}6,9c and/or 18 : 0 anteiso, which could not be separated by GLC with the MIDI system.

 
Analysis of the polyamine patterns of strains V45T, V54AT, P. citrea IFO 12397T and P. sukumoe IFO 14650T was done as described by Altenburger et al. (1997)Go. Three strains (V45T, V54AT and P. citrea IFO 12397T) contained similar polyamine patterns, consisting of the major compound spermidine [5·6, 3·5 and 2·7 µmol (g dry weight)-1, respectively] and moderate to minor amounts of spermine [1·7, 1·3 and 0·5 µmol (g dry weight)-1] and putrescine [0·3, 0·1 and 0·5 µmol (g dry weight)-1]. Traces of 1,3-diaminopropane and cadaverine were also detected. In contrast, P. sukumoe IFO 14650T exhibited a polyamine pattern in which the concentrations of the major polyamines were two orders of magnitude lower, clearly distinguishing it from the other three strains. These results indicate that at least two different polyamine patterns can be found in the genus Promicromonospora. Similar polyamine patterns have already been reported for representatives of related genera such as Cellulomonas, Cellulosimicrobium and Oerskovia (Hamana, 1995Go).

Biochemical characteristics
Investigation of P. citrea IFO 12397T, P. sukumoe IFO 14650T, V45T and V54AT revealed metabolic profiles that were distinct for each strain (Table 2Go). They could be distinguished from each other easily by their biochemical profiles, supporting the idea that each of strains V45T and V54AT represents a distinct species. Gram-staining (Moaledji, 1986Go) of cells of the two isolates revealed Gram-positive behaviour.


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  		Table 2. Biochemical characteristics of Promicromonospora strains

Strains: 1, P. vindobonensis sp. nov. V45T; 2, P. aerolata sp. nov. V54AT; 3, P. sukumoe IFO 14650T; 4, P. citrea IFO 12397T. +, Positive; (+), weakly positive; -, negative; pNA, p-nitroanilide; pNP, p-nitrophenyl. All strains are positive for aesculin ({beta}-glucosidase), gelatinase, catalase and pyrazinamidase (API Coryne). All strains are negative for alkaline phosphatase, {beta}-glucuronidase, {alpha}-glucosidase, {beta}-galactosidase and N-acetyl-{beta}-glucosaminidase (API Coryne), fermentation of ribose, xylose, mannitol and lactose and production of acid from erythritol, D-arabinose, L-arabinose, ribose, xylose, adonitol, methyl {beta}-xyloside, sorbose, rhamnose, dulcitol, inositol, sorbitol, methyl {alpha}-mannoside, lactose, melibiose, inulin, raffinose, starch, xylitol, gentiobiose, lyxose, tagatose, fucose, arabitol, gluconate, 2-ketogluconate and 5-ketogluconate (API 50CH).

 
Taxonomic considerations
16S rDNA sequence comparisons and chemotaxonomic characteristics of the isolates suggest assignment of strains V45T and V54AT to the genus Promicromonospora. Results from DNA–DNA hybridizations, as well as unique physiological profiles, demonstrate that each of strains V45T and V54AT represents a separate species within the genus.

Since the four species of the genus Promicromonospora exhibit not more than 98·5 % 16S rDNA sequence similarity to each other, in future studies, highest values below 98·6 % can be considered to suggest the detection of a novel species of the genus Promicromonospora.

Description of Promicromonospora vindobonensis sp. nov.
Promicromonospora vindobonensis (vin.do.bo.nen'sis. L. fem. adj. vindobonensis of Vindobona, the Roman name for Vienna, where the type strain was isolated.)

Cells show branching hyphae (Supplementary Fig. A, available in IJSEM Online) that are 0·3–0·5 µm in diameter after 18 h of growth on PY agar. Cells stain Gram-positive. After 3 days of growth, the mycelium fragments into non-motile, Y- or V-shaped, rod-like, coccoid elements, 0·3–0·5x0·6–1·5 µm. No sessile, oval spores, chlamydospore-like or other spore-like elements are observed. On PY agar, colonies are whitish, translucent, convex, glistening and approx. 1 mm in diameter with an entire edge. Physiological and biochemical characteristics are summarized in Table 2Go. In the peptidoglycan, glutamic acid, glycine, alanine and lysine are present. Cell-wall sugars are glucose, galactose and rhamnose. Diphosphatidylglycerol, phosphatidylglycerol, two unknown glycolipids, three unknown phosphoglycolipids, one unknown phospholipid and one unknown polar lipid are present in the polar lipid profile. Predominant acids in the fatty acid profile are C15 : 0 anteiso and C15 : 0 iso. C16 : 0 and C17 : 0 anteiso are present in moderate amounts. The quinone system consists of the major compound MK-9(H4). Spermidine is the predominant cellular polyamine and spermine is present in moderate amounts. The G+C content is 70 mol%.

The type strain, V45T (=IFO 16525T=CCM 7044T), was isolated from the air in the ‘Virgilkapelle’ chapel in Vienna.

Description of Promicromonospora aerolata sp. nov.
Promicromonospora aerolata (a.e.ro.la'ta. Gr. n. aer air; L. part. adj. latum, -a carried; N.L. part. fem. adj. aerolata airborne).

Cells show branching hyphae (Supplementary Fig. B, available in IJSEM Online) that are 0·3–0·5 µm in diameter after 18 h of growth on PY agar. Cells stain Gram-positive. After 3 days of growth, the mycelium fragments into <@?show=[to]>non-motile, Y- or V-shaped, rod-like, coccoid elements, 0·3–0·5x0·6–1·5 µm. No sessile, oval spores, chlamydospore-like or other spore-like elements are observed. Colonies are light yellow, translucent and reach approx. 1 mm in diameter. Physiological and biochemical characteristics are summarized in Table 2Go. The peptidoglycan contains glutamic acid, glycine, alanine and lysine. Cell-wall sugars are glucose, galactose and rhamnose. Diphosphatidylglycerol, phosphatidylglycerol, two unknown glycolipids, two unknown phosphoglycolipids and one unknown phospholipid are present in the polar lipid profile. Predominant acids in the fatty acid profile are C15 : 0 anteiso and C15 : 0 iso. C16 : 0 and C17 : 0 anteiso are present in moderate amounts. The quinone system consists of the major compound MK-9(H4). Spermidine is the predominant cellular polyamine and spermine is present in moderate amounts. The G+C content is 70 mol%.

The type strain, V54AT (=IFO 16526T=CCM 7043T), was isolated from the air in the ‘Virgilkapelle’ chapel in Vienna.


   ACKNOWLEDGEMENTS
 
This work was supported by grant P12820-MOB provided by the Austrian Science Foundation (FWF).


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