International Journal of Systematic and Evolutionary Microbiology (2002), 52, 1229–1234 DOI: 10.1099/ijs.0.02013-0

Microbacterium aerolatum sp. nov., isolated NOTE from the air in the ‘Virgilkapelle’ in Vienna

1 Institut fu$ r Mikrobiologie Christian Zlamala,1,2 Peter Schumann,3 Peter Ka$ mpfer,4 Maria Valens,5 und Genetik, Universita$ t 5 1 1,2 Wien, A-1030 Wien, Ramon Rossello! -Mora, Werner Lubitz and Hans-Ju$ rgen Busse Austria

2 Institut fu$ r Bakteriologie, Author for correspondence: Hans-Ju$ rgen Busse. Tel: j43 1 25077 2119. Fax: j43 1 25077 2190. Mykologie und Hygiene, e-mail: Hans-Juergen.Busse!vu-wien.ac.at Veterina$ rmedizinische Universita$ t, A-1210 Wien, Austria Three rod-shaped, Gram-positive strains were isolated from the air of the 3 DSMZ – Deutsche chapel ‘Virgilkapelle’ in Vienna. A representative of these three strains, strain Sammlung von T Mikroorganismen und V-73 , shared the highest 16S rDNA sequence similarities with members of the Zellkulturen GmbH,D- genus Microbacterium, in particular Microbacterium foliorum, Microbacterium 38124 Braunschweig, testaceum, Microbacterium esteraromaticum, Microbacterium keratanolyticum Germany and Microbacterium arabinogalactanolyticum. The strains displayed almost 4 Institut fu$ r Angewandte identical biochemical and physiological characteristics and showed no Mikrobiologie, Justus- Liebig-Universita$ t, D-35392 differences in their protein patterns obtained after SDS-PAGE. On the basis of Giessen, Germany Fourier-transform infra-red (FT-IR) spectra and genomic fingerprints, the three 5 Institut Mediterrani strains were grouped together and separated from the other relevant d’Estudis Avancats and members of the genus Microbacterium. The chemotaxonomic characteristics Departament de Biologia analysed, including polar lipids, quinone systems, cell wall composition and Ambiental, Universitat de les Illes Balears (CSIC-UIB), fatty acid profiles, were in good agreement with the characteristics described E-07071 Palma de for the genus Microbacterium. The GMC content of the DNAs was determined to Mallorca, Spain be in the narrow range 693–697 mol%. The results of DNA–DNA hybridization, biochemical/physiological characterization, ERIC-PCR-generated genomic fingerprints and FT-IR spectra demonstrated that the three isolates represent a novel species of the genus Microbacterium. The name Microbacterium aerolatum sp. nov. is proposed for the novel species, of which strain V-73T (l DSM 14217T l CCM 4955T) is the type strain.

Keywords: Microbacterium aerolatum sp. nov., 16S rDNA sequence, chemotaxonomy, biochemical\physiological traits

The genus Microbacterium has been emended recently ‘Virgilkapelle’ underneath the ‘Stephansplatz’ in to combine the genera Microbacterium and Aureo- Vienna, among others, three yellow-pigmented, bacterium (Takeuchi & Hatano, 1998a). In spite of coryneform bacteria were isolated. Here, we describe high 16S rDNA sequence similarities, members of the the classification of these strains, which could be clearly genus are heterogeneous in terms of chemotaxonomic allocated to the genus Microbacterium. The three characteristics such as quinone systems, peptidoglycan strains, designated V-73T, V-62 and V-72, were charac- types and polyamine patterns (Yokota et al., 1993a, b; terized using a set of methods summarized by Zlamala Takeuchi & Hatano, 1998a, b; Altenburger et al., et al. (2002) and Wieser & Busse (2000). 1997; Matsuyama et al., 1999). Species described so far Colonies of the three isolates V-73T, V-62 and V-72 have been isolated from the phyllosphere of grasses, were translucent, yellow-pigmented, opaque, circular, soil, sewage, lake water, steep liquor, milk products or low-convex, moist and 2–7 mm in diameter. Colony cheese and clinical specimens (Breed, 1957; Collins margins were entire on nutrient agar. Cells were small, et al., 1983; Collins & Keddie, 1986; Yokota et al., slender rods and occurred singly or in irregular 1993a, b; Saweljew et al., 1996; Takeuchi & Hatano, clusters. Mycelial growth and a marked rod–coccus 1998a, b; Behrendt et al., 2001). In a study concerning cycle were not observed. The three isolates showed the bacteriological biodiversity in the air of the chapel Gram-positive behaviour in Gram-staining and KOH ...... test. They grew best on the complex organic medium The EMBL accession number of the 16S rDNA sequence of Microbacterium tryptic soy agar (TSA) at temperatures ranging from aerolatum V-73T is AJ309929. 18 to 28 mC and in the presence of 4% NaCl. Good

02013 # 2002 IUMS Printed in Great Britain 1229 C. Zlamala and others

Table 1. Physiological and biochemical properties of M. aerolatum, M. esteraromaticum and M. arabinogalactanolyticum ...... Properties were analysed as described by Ka$ mpfer et al. (1991) and Zlamala et al. (2002). j, Positive; k, negative; d, some strains positive; , weak reaction. Symbols (†) indicate results that are not in line with those reported previously by Yokota et al. (1993b). All five strains were negative for decomposition of Tween 80† and urea,† acid production from -ribose, -melibiose, -inulin, -raffinose, inositol, dulcitol and sorbitol, utilization of α--melibiose, adonitol, i-inositol, -sorbitol, trans-aconitate, adipate, azelate, citrate,† itaconate, mesaconate, suberate, β-alanine and -tryptophan and hydrolysis of aesculin, p-nitrophenyl (pNP) β--glucuronide, 2-deoxythymidine-5h-pNP phosphate and -glutamate-γ-3-carboxy p-nitroanilide (pNA). All five strains were negative in the Voges–Proskauer, methyl red,† oxidase and indole tests as well as in the production of H#S†. All five strains were positive for decomposition of potato starch and utilization of -arabinose, N-acetyl -glucosamine, -cellobiose, -fructose, -galactose, gluconate, -glucose, -mannose, -maltose, sucrose, -trehalose, acetate, propionate, -3-hydroxybutyrate, pyruvate, -histidine, -ornithine and -proline and hydrolysis of pNP α--glucopyranoside, pNP β--glucopyranoside, bis-pNP phosphate, pNP phenylphosphonate, -alanine pNA and -proline pNA. All five strains grow in the presence of 2%† and 4% NaCl, but not 10% NaCl. All five strains grow well at 28 mC, but not at 42 mC.

Characteristic M. aerolatum M. esteraromaticum M. arabinogalactanolyticum (3 strains) DSM 8609T DSM 8611T

Catalase jk j Nitrate reduction jk j Acid production from: -Glucose jk j -Trehalose kk j -Arabinose jk  -Sucrose jk j -Galactose jk  -Mannose jk j -Maltose jk j -Rhamnose jk j -Lactose kk  -Mannitol jk j -Xylose jk k Glycerol kk j Utilization of: p-Arbutin kj j -Rhamnose jk j -Ribose jk j Salicin kj j Maltitol jj k -Xylose jk j -Mannitol kj j Putrescine kj j cis-Aconitate d (1\3)* kk 4-Aminobutyrate jj k Fumarate kj j Glutarate kj k -Lactate jj k† -Malate kk j Oxoglutarate jk k -Alanine kj j -Aspartate jk k -Leucine jk j -Phenylalanine kk j -Serine kk j 3-Hydroxybenzoate jk k 4-Hydroxybenzoate jk k Phenylacetate kk j Tyrosine decomposition kj k Hydrolysis of:

1230 International Journal of Systematic and Evolutionary Microbiology 52 Microbacterium aerolatum sp. nov.

Table 1 (cont.)

Characteristic M. aerolatum M. esteraromaticum M. arabinogalactanolyticum (3 strains) DSM 8609T DSM 8611T

pNP β--galactopyranoside kk j pNP phosphorylcholine kk j Gelatin kk j Casein kk j Tween 20 kj k Growth at\in: 6n5% NaCl j  4 mC j  k 37 mC jj k

* Strain V-62 positive. † Data not in line with Yokota et al. (1993b). growth was observed at 37 mC and in the presence of Y17231; Schumann et al., 1999) and Microbacterium T 6n5% NaCl. There was weak growth at 4 mC and in the barkeri DSM 20145 (accession no. X77446; Rainey et presence of 10% NaCl. No growth occurred at 42 mC al., 1994) (Takeuchi & Hatano, 1998a). This signature or under microaerobic conditions. Physiological and was also found in the 16S rDNA sequence of M. biochemical characteristics of the three isolates are arabinogalactanolyticum DSM 8611T (accession no. summarized in Table 1. Of more than 100 physiological Y17228; Schumann et al., 1999). and biochemical characteristics, the three strains Chemotaxonomic characteristics confirmed the place- differed only in the utilization of cis-aconitate. Almost ment of the three isolates in a single species and also identical protein patterns (results not shown) T their identification as members of the genus Micro- supported the assumption that the three strains V-73 , bacterium. The peptidoglycan of strain V-73T con- V-62 and V-72 are members of a single species. The tained the following amino acids: ornithine, alanine, GjC contents of the genomic DNA of the three glycine, glutamic acid, hydroxyglutamic acid (Hyg) isolates, as determined by the method described by and homoserine (Hsr). From these data and from the Cerda' -Cue! llar et al. (1997), were in the narrow range occurrence of the peptides Gly ! -Glu, Gly ! -Orn, 69n3–69n7mol%. -Ala ! -Orn and -Ala ! -Orn " Gly in the par- Analysis of the 16S rDNA of strain V-73T, the tial hydrolysate of the peptidoglycan (data not shown), representative of this group, resulted in a fragment we concluded that the peptidoglycan type is B2β of 1402 bases (positions 50–1469, Escherichia coli (Schleifer & Kandler, 1972) -Glu(Hyg) ! Gly ! - numbering; Brosius et al., 1978). Sequence com- Orn, with Gly at position 1 and -Hsr at position 3 of T the peptide subunit (type B6; DSMZ, 2001). The parisons showed that strain V-73 shared the highest T similarities with Microbacterium foliorum DSM quinone systems of strains V-73 , V-62 and V-72, T 12966 (98n1%), Microbacterium testaceum DSM which were analysed according to Tindall (1990), T 20166 (98n0%), Microbacterium esteraromaticum consisted of the major menaquinones MK-12 (56– T DSM 8609 (97n7%), Microbacterium arabino- 64%) and MK-13 (30–44%). Minor amounts of T galactanolyticum DSM 8611 (97n6%) and Micro- menaquinone MK-11 (1–6%) were also detected. T bacterium keratanolyticum DSM 8606 (97n6%). Se- Fatty acid composition was analysed as described by Ka$ mpfer et al. (1997). The predominant fatty acids in quence similarities to other species of the genus T Microbacterium were in the range 97n5–95n0% and to V-73 were ai-C"&:! and ai-C"(:!, with significant amounts of i-C"' ! (Table 2). Whereas the fatty acid other species of the family Microbacteriaceae, were in T : T the range 94n0–91n0%. This result demonstrated clearly profiles of V-73 and M. testaceum DSM 20166 were that V-73T is affiliated to the genus Microbacterium similar in their major characteristics, quantitative (Takeuchi & Hatano, 1998a). Signature nucleotides differences in the contents of i-C"&:! and ai-C"(:! T distinguished V-73T from M. esteraromaticum DSM detected in the 16S rDNA sequence of strain V-73 T T were in agreement with those used for the description 8609 , M. arabinogalactanolyticum DSM 8611 and M. keratanolyticum DSM 8606T (Table 2) and from of the genus (Takeuchi & Hatano, 1998a). The close T relationship of V-73T to M. esteraromaticum was the profile reported for M. foliorum DSM 12966 supported by the detection of the signature adenosine (Behrendt et al., 2001). at position 69 of the 16S rDNA sequence (E. coli Polar lipid profiles were analysed by TLC (Ventosa et numbering; Brosius et al., 1978), so far described only al., 1993). Diphosphatidylglycerol and phosphatidyl- for M. esteraromaticum DSM 8609T (accession no. glycerol were found to be predominant in polar lipid http://ijs.sgmjournals.org 1231 C. Zlamala and others

Table 2. Fatty acid composition of M. aerolatum sp. nov. 12345678 and related species ...... bp Strains: 1, M. aerolatum V-73T;2,M. testaceum DSM 20166T;3,M. esteraromaticum DSM 8609T;4,M. keratanolyticum DSM 8606T;5,M. arabinogalactanolyticum DSM 8611T. Values are percentages of total fatty acids. tr, Trace. 3675 — Fatty acid 12345 2323 —

ai-C"$:! tr 0n3 i-C"%:! 0n50n93n27n54n8 1371 — C"%:! 0n70n40n8 i-C"&:" 0n2 ai-C"&:" 1n41n20n70n4 i-C"&:! 1n81n911n913n515n2 ai-C"&:! 44n140n168n544n849n6 C"&:! 0n80n5 C"':" iso G 0n6 i-C"':! 13n018n512n327n417n4 C"':! 3n82n50n62n0 ...... ai-C"(:" 1n7 i-C"( ! 0n70n81n61n3 Fig. 1. Negative image of ERIC-PCR-generated genomic : fingerprints of strains V-62 (lane 2), V-72 (3), V-73T (4), M. ai-C"(:! 36n022n88n12n77n9 esteraromaticum DSM 8609T (5) and M. arabinogalactano- lyticum DSM 8611T (6). Lanes 1 and 7, size markers (λ DNA BstEII digest); lane 8, negative control. extracts of strains V-73T, V-62 and V-72. In addition, two unknown glycolipids were detected. These com- bined chemotaxonomic characteristics are in agree- Spectral distance ment with those reported for M. esteraromaticum and 0·2 0·1 0 M. arabinogalactanolyticum (Yokota et al., 1993b), M. arabinogalactanolyticum DSM 8611T two of the most closely related species as indicated V-62 from 16S rDNA sequence comparisons. In contrast, V-73T some of these characteristics distinguished the isolates V-72 from M. keratanolyticum DSM 8606T, which was M. esteraromaticum DSM 8609T reported to have a quinone system with nearly equal ...... amounts of MK-12 and MK-13 but a cell wall of the Fig. 2. Average linkage dendrogram based on the distances peptidoglycan type B2α, as well as from M. testaceum of first derivatives of FT-IR spectra (frequency ranges T −1 −1 −1 DSM 20166 , which contains MK-11 as the major 3000–2800 cm , 1201–900 cm , 901–699 cm ). menaquinone (Yokota et al., 1993b), and from M. foliorum DSM 12966T, with MK-11 and MK-12 as major menaquinones (Behrendt et al., 2001). There- T fore, the 16S rDNA sequence comparison in com- data demonstrate unambiguously that V-73 ,V-62 bination with the quinone system and peptidoglycan and V-72 are members of a single novel species of the Microbacterium type indicated a possible relationship only with M. genus . The three isolates could be also M esteraromaticum T esteraromaticum and M. arabinogalactanolyticum.In distinguished from . DSM 8609 M arabinogalactanolyticum T conclusion, the three strains were compared only to and . DSM 8611 on the M. esteraromaticum DSM 8609T and M. arabino- basis of their characteristic genomic fingerprints galactanolyticum DSM 8611T to determine their taxo- obtained after ERIC-PCR (Wieser & Busse, 2000) and et al nomic status. FT-IR spectra (Wieser ., 2002). A high degree of similarity in genomic fingerprints (Fig. 1) was detected DNA relatedness among V-73T, V-62 and V-72 and for the three strains. However, strains V-62 and V-72 with M. esteraromaticum DSM 8609T and M. arabino- displayed identical fingerprints, indicating a clonal galactanolyticum DSM 8611T was analysed according relationship, whereas strain V-73T could be distin- to Lind & Ursing (1986) and Ziemke et al. (1998). The guished from strains V-62 and V-72 on the basis of three strains shared 100% DNA relatedness among several different bands. Analysis of FT-IR spectra themselves, whereas only low reassociation values showed that the three isolates V-73T, V-62 and V-72 (28n9–48n8%) were obtained between the isolates and were grouped in a cluster and separate from the two the reference strains M. esteraromaticum DSM 8609T closely related species M. esteraromaticum and M. and M. arabinogalactanolyticum DSM 8611T. These arabinogalactanolyticum (Fig. 2).

1232 International Journal of Systematic and Evolutionary Microbiology 52 Microbacterium aerolatum sp. nov.

From the results presented here, it becomes evident Breed, R. S. (1957). Genus III. Flavobacterium Bergey et al. 1923. In that the three strains V-73T, V-62 and V-72 represent a Bergey’s Manual of Determinative Bacteriology, 7th edn, pp. 309–322. Edited by R. S. Breeds, E. G. D. Murray & M. R. Smith. Baltimore: single novel species of the genus Microbacterium that Williams & Wilkins. can be distinguished from chemotaxonomically similar Brosius, J., Palmer, M. L., Kennedy, P. J. & Noller, H. F. (1978). species of the genus such as M. esteraromaticum and Complete nucleotide sequence of a 16S ribosomal RNA gene from M. arabinogalactanolyticum on the basis of genomic Escherichia coli. Proc Natl Acad Sci U S A 75, 4801–4805. ' ! ! fingerprints (Fig. 1), FT-IR spectra (Fig. 2) and more Cerda-Cuellar, M., Rossello-Mora, R. A., Lalucat, J., Jofre, J. & than 25 biochemical\physiological characteristics Blanch, A. (1997). Vibrio scophthalmi sp. nov., a new species from (Table 1). Thus, we propose the name Microbacterium turbot (Scophthalmus maximus). Int J Syst Bacteriol 47, 58–61. aerolatum sp. nov. for the novel species. Collins, M. D. & Keddie, R. M. (1986). Genus Microbacterium Orla- Jensen 1919, 179AL.InBergey’s Manual of Systematic Bacteriology, vol. 2, pp. 1320–1322. Edited by P. H. A. Sneath, N. S. Mair, M. E. Sharpe Description of Microbacterium aerolatum sp. nov. & J. G. Holt. Baltimore: Williams &Wilkins. Collins, M. D., Jones, D., Keddie, R. M., Kroppenstedt, R. M. & Microbacterium aerolatum (ae.ro.lahtum. Gr. n. aer air, Schleifer, K. H. (1983). Classification of some coryneform bacteria in L. part. adj. latum carried, N.L. part. adj. aerolatum a new genus Aureobacterium. Syst Appl Microbiol 4, 236–252. airborne). DSMZ (2001). Catalogue of Strains, 7th edn, p. 617. Braunschweig: DSMZ. Cells are small rods. The cells vary in size from 0n5to $ Kampfer, P., Steiof, M. & Dott, W. (1991). Microbiological charac- 0n7 µm wide by 1n5to1n9 µm long. Cells occur singly or terization of a fuel-oil contaminated site including numerical identi- in irregular clusters. They are Gram-positive and non- fication of heterotrophic water and soil bacteria. Microb Ecol 21, motile. Endospores are not observed. Colonies are 227–251. $ circular, slightly convex, opaque and moist. Colony Kampfer, P., Denner, E. B. M., Meyer, S., Moore, E. R. B. & Busse, diameters on TSA are 2–7 mm. The colour of the H.-J. (1997). Classification of ‘‘Pseudomonas azotocolligans’’ Anderson colonies on nutrient agar is yellow. Aerobic. Catalase 1955, 132, in the genus Sphingomonas as Sphingomonas trueperi sp. nov. is produced. Oxidase-negative. Nitrate is reduced to Int J Syst Bacteriol 47, 577–583. nitrite. Physiological and biochemical traits are shown Lind, E. & Ursing, J. (1986). Clinical strains of Enterobacter agglomerans (synonyms: Erwinia herbicola, Erwinia milletiae) identified in Table 1. The cell wall diamino acid is -ornithine by DNA-DNA-hybridization. Acta Pathol Microbiol Immunol Scand and the peptidoglycan type is B2β containing the Sect B 94, 205–213. amino acids ornithine, alanine, glycine, glutamic acid, Matsuyama, H., Kawasaki, K., Yumoto, I. & Shida, O. (1999). hydroxyglutamic acid and homoserine. The polar Microbacterium kitamiense sp. nov., a new polysaccharide-producing lipid profile is composed of diphosphatidylglycerol, bacterium isolated from the wastewater of a sugar-beet factory. Int J phosphatidylglycerol and two unknown glycolipids. Syst Bacteriol 49, 1353–1357. The fatty acid profile consists of the predominant Rainey, F. A., Weiss, N., Prauser, H. & Stackebrandt, E. (1994). Further evidence for the phylogenetic coherence of actinomycetes with compounds ai-C"&:!, ai-C"(:! and i-C"':!, and i-C"&:! is group B-peptidoglycan and evidence for the phylogenetic intermixing present in minor amounts. The quinone system consists of the genera Microbacterium and Aureobacterium as determined by 16S of the major menaquinones MK-12 and MK-13. The rDNA analysis. FEMS Microbiol Lett 118, 135–140. GjC content is 69n3–69n7mol%. Saweljew, P., Kunkel, J., Feddersen, A., Baumert, M., Baehr, J., T T Ludwig, W., Bhakdi, S. & Husmann, M. (1996). Case of fatal systemic The type strain, V-73 (l DSM 14217 l CCM T infection with an Aureobacterium sp.: identification of isolate by 16S 4955 ), was isolated from the air in the chapel rRNA gene analysis. J Clin Microbiol 34, 1540–1541. ‘Virgilkapelle’ in Vienna, Austria. Schleifer, K. H. & Kandler, O. (1972). Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36, 407–477. Schumann, P., Rainey, F. A., Burghardt, J., Stackebrandt, E. & Acknowledgements Weiss, N. (1999). Reclassification of Brevibacterium oxydans This work was supported by a grant from the Austrian (Chatelain and Second 1966) as Microbacterium oxydans comb. nov. Int Fonds zur Fo$ rderung der Wissenschaftlichen Forschung J Syst Bacteriol 49, 175–177. (P12820 MOB). We are grateful to Hans Tru$ per for advice in Takeuchi, M. & Hatano, K. (1998a). Union of the genera nomenclatural problems and to Christian Radatz for sup- Microbacterium Orla-Jensen and Aureobacterium Collins et al.ina port in FT-IR. The research of R.R.-M. was supported by redefined genus Microbacterium. Int J Syst Bacteriol 48, 739–747. the Spanish Ministry of Science and Technology with the Takeuchi, M. & Hatano, K. (1998b). Proposal of six new species in the grant BOS2000-1123-C02-01. genus Microbacterium and transfer of Flavobacterium marinotypicum ZoBell and Upham to the genus Microbacterium as Microbacterium maritypicum comb. nov. Int J Syst Bacteriol 48, 973–982. References Tindall, B. J. (1990). 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Int J Syst Evol Microbiol 50, 1087–1093. after mulching the sward, and reclassification of Aureobacterium $ resistens (Funke et al. 1998) as Microbacterium resistens comb. nov. Int Wieser, M., Denner, E. B. M., Kampfer, P. & 10 other authors J Syst Evol Microbiol 51, 1267–1276. (2002). Emended descriptions of the genus Micrococcus, Micrococcus http://ijs.sgmjournals.org 1233 C. Zlamala and others luteus (Cohn 1872) and Micrococcus lylae (Kloos et al. 1974). Int J Syst bacterium as Aureobacterium esteraromaticum comb. nov. Int J Syst Evol Microbiol 52, 629–637. Bacteriol 43, 555–564. $ ! Yokota, A., Takeuchi, M. & Weiss, N. (1993a). Proposal of two new Ziemke, F., Hofle, M. G., Lalucat, J. & Rossello-Mora, R. (1998). species in the genus Microbacterium: Microbacterium dextranolyticum Reclassification of Shewanella putrefaciens Owen’s genomic group II as sp. nov. and Microbacterium aurum sp. nov. Int J Syst Bacteriol 43, Shewanella baltica sp. nov. 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