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Institut für Chemie und Biologie des Meeres, Fakultät für Mathematik und Naturwissenschaften, CvO Universität Oldenburg, PO Box 2503, D-26111 Oldenburg, Germany
Correspondence
Thorsten Brinkhoff
t.brinkhoff{at}icbm.de
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Published online ahead of print on 23 May 2003 as DOI 10.1099/ijs.0.02735-0.
The GenBank accession number of the 16S rRNA gene sequence of Aeromicrobium marinum T2T is AY166703.
A comparison of the cellular fatty acids of A. marinum with those of related taxa is available in IJSEM Online.
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; Rappé et al., 1997; Urakawa et al., 1999) or by hybridization with 16S rRNA genus-specific probes (Moran et al., 1995). The clones recovered from bacterioplankton of the Sargasso Sea and the Pacific Ocean so far form a phylogenetically coherent clade (Rappé et al., 1997) within the newly proposed phylum ‘Actinobacteria’ (Garrity & Holt, 2001) and they are distantly related to their nearest cultivated relatives (Rappé et al., 1999). Recent studies even suggest that marine Gram-positive bacteria represent a large fraction of the culturable heterotrophs from sea water, marine sediments, algae and invertebrates (Jensen & Fenical, 1995; Ortigosa et al., 1997; Mincer et al., 2002) and most of them require sea water for growth. This is an important trait to characterize the origin of Gram-positive bacteria from marine environments. There is an ongoing debate whether Gram-positive bacteria, especially those which were isolated from near-shore habitats, are an indigenous component of the marine bacterial community or whether they were washed in from terrestrial systems (Jensen et al., 1991; Takizawa et al., 1993; Bull et al., 2000). The wash-in hypothesis is based on different studies which demonstrated a high degree of salt tolerance of many terrestrial streptomycetes (Okazaki & Okami, 1976) and showed that the number of actinomycetes in marine habitats decreases with increasing distance from land (Goodfellow & Haynes, 1984). Despite the evidence supporting growth of actinobacterial species in marine environments (Ortigosa et al., 1997; Mincer et al., 2002), only a few marine species, for example, Rhodococcus marinonascens (Helmke & Weyland, 1984), Dietzia maris (Rainey et al., 1995) and Microbacterium maritypicum (Takeuchi & Hatano, 1998), have been characterized in detail. Thus, the ecological role of marine Gram-positive bacteria remains still unexplained. We isolated and characterized an abundant indigenous Gram-positive bacterium from surface waters of the German Wadden Sea. This organism is affiliated with the genus Aeromicrobium and is the first marine representative of the family Nocardioidaceae within the order Actinomycetales.
Aeromicrobium erythreum DSM 8599T and Aeromicrobium fastidiosum DSM 10552T were obtained from the DSMZ (Deutsche Sammlung von Mikroorganismen und Zellkulturen, Braunschweig, Germany) and were cultured as recommended by the supplier. Strain T2T was isolated from the highest positive dilution (10-4) of a most-probable-number (MPN) series (1 ml inoculum added to 9 ml medium). Marine broth (MB; Difco Laboratories) was used as medium and was inoculated with Wadden Sea surface water sampled near the village of Neuharlingersiel 3 h before high tide. Incubation of the MPN series was carried out at 28 °C for 30 days. Total bacterial numbers in the water sample were determined by 4',6-diamidino-2-phenylindole (DAPI) staining according to Crump et al. (1998). Isolation and subcultivation were performed in MB or on marine agar (MA 2216; Difco Laboratories) at 28 °C. For some phenotypic characterizations, the organism was cultured in artificial sea water (ASW) modified after Levring (1946) consisting of (per litre distilled water): 23·6 g NaCl; 0·64 g KCl; 4·53 g MgCl2.6H2O; 5·94 g MgSO4.7H2O; 1·3 g CaCl2.2H2O; 10 mg Na2PO4.2H2O; 2·1 mg NH4NO3. To avoid precipitation, the CaCl2 was sterilized separately. The ASW medium contained as source of carbon 0·3 % (w/v) yeast extract, 0·6 % peptone and 0·3 % glucose (denoted as ASW/YPG). For minimal media containing only defined carbon sources (e.g. mannitol and amino acids), 10 ml of a 10 vitamin solution (Balch et al., 1979) and 1 ml of trace element solution (Widdel & Bak, 1992) were additionally supplied per litre of ASW. All incubations for the characterization experiments were carried out at 20–25 °C for 1–2 weeks. Morphological features were investigated with cells grown on MA or in MB. Colony morphology was studied using a Zeiss Axiolab microscope. Transmission electron microscopy was carried out with negatively stained cells (Cole & Popkin, 1981) using a transmission electron microscope 109 (Zeiss). Motility was checked microscopically. The ability to grow with different carbon sources was analysed in ASW supplemented with 2–5 mM of the tested carbon source. The temperature range for growth was determined in ASW/YPG between 4 and 55 °C. The pH range (4·5–10·5) was tested in a minimal medium (ASW) containing 5 mM mannitol. Growth was determined by an increase in turbidity. Gram staining, catalase and oxidase tests were performed as described by Smibert & Krieg (1994). Salinity range was determined using ASW/YPG as basis medium. Exoenzyme activities (amylase by starch hydrolysis, caseinase by casein hydrolysis, chitinase by chitin hydrolysis and cellulase by hydrolysis of cellulose) were analysed on solidified ASW medium with 1·5 % (w/v) agarose and supplemented with 0·5 % (w/v) starch, 10 % (w/v) skim milk powder, 0·5 % (w/v) chitin and 1·0 % (w/v) cellulose, respectively, as described previously (Smibert & Krieg, 1994). Lipase activity was also studied on solidified ASW medium supplemented with 2 % (v/v) vegetable oil. After incubation at 20 °C, the colonies in Petri dishes were covered with a 0·5 % CuSO4 solution and incubated for 15 min. The solution was discarded and a positive result was indicated by a bluish or green colour around the colonies. The ability to denitrify was determined in ASW/YPG as described previously (Smibert & Krieg, 1994). The peptidoglycan was analysed by TLC on cellulose plates according to the method described by Rhuland et al. (1955) which was modified by Hasegawa et al. (1983). Menaquinones were determined by HPLC as described previously (Groth et al., 1996) and results were verified by electron ionization MS. Fatty acid analysis was carried out as described by Sass et al. (2002). Isolation of genomic DNA (Cashion et al., 1977) and determination of the G+C content by HPLC (Tamaoka & Komagata, 1984; Mesbah et al., 1989) followed described procedures. DNA–DNA hybridization analysis was performed by using the renaturation method of De Ley et al. (1970) with the modifications of Escara & Hutton (1980) and Huss et al. (1983). Renaturation rates were computed with the TRANSFER.BAS program by Jahnke (1992). The dot-blot hybridization procedure was performed as described recently (Bruns et al., 2002). In brief, a digoxigenin (DIG)-labelled probe (length 569 bp) for the detection of strain T2T was generated from a PCR-amplified 16S rRNA gene fragment (position 341–907 according to Escherichia coli numbering; Brosius et al., 1981) of its genomic DNA. This probe was used to hybridize 16S rRNA gene fragments amplified from the complete natural bacterial community. For calibration, different amounts of genomic DNA of strain T2T were used for amplification, subsequently blotted and hybridized with this probe. Intensities of the hybridization signals of the natural community and of the calibration were used to estimate the proportion of DNA from strain T2T in the community DNA. Preferential amplification of the 16S rRNA gene of strain T2T was tested by adding different concentrations of genomic DNA of strain T2T to 10 ng of the community DNA prior to PCR amplification and hybridization. Cross-hybridization was tested by using A. erythreum DSM 8599T and A. fastidiosum DSM 10552T. Hybridization signals were detected with the DIG luminescence detection kit (Roche) and Lumi-Film (Roche) according to the manufacturer's instructions. For quantification of individual spots, the image was digitized and analysed by using ZERO-DSCAN software (Scanalytics). PCR amplification of almost-complete 16S rRNA genes, purification of PCR products and subsequent sequencing analysis were performed according to Brinkhoff & Muyzer (1997). The sequence of strain T2T was compared with similar sequences of reference organisms by BLAST search (Altschul et al., 1997). Phylogenetic analysis was performed with the ARB software package (Ludwig et al., 2002). For tree calculation, only sequences with more than 1300 bp were considered. A phylogenetic tree was constructed using neighbour-joining and maximum-likelihood analyses. Alignment positions at which less than 50 % of the sequences of the entire set of data had the same residues were excluded from the calculations to prevent uncertain alignments within highly variable positions of the 16S rRNA genes, which cause mistakes in tree topology.
Major phenotypic properties that differentiate strain T2T from related taxa are summarized in Table 1. Strain T2T is a Gram-positive, non-motile, rod-shaped bacterium. No flagella, pili or other appendages were observed (Fig. 1a, b). This morphology remained constant irrespective of cell age. No spores were produced. Colonies were ivory and 0·5–1·0 mm in diameter, circular and convex. Diffuse haloes of different sizes were observed around the colonies with a microscope (Fig. 1c). The haloes could not be stained with DAPI, indicating that they did not consist of bacterial cells (compare Fig. 1d, e). Treatment with Coomassie blue and Alcian Blue for detection of proteins or acidic polysaccharides, respectively, led to a weak staining of the haloes by Alcian Blue, indicating that one component of the haloes may be acidic polysaccharides. We assume that exopolysaccharides are excreted to attach to surfaces, as was proposed for other bacteria (Becker, 1996; Gehrke et al., 2001). Surfaces for attachment might be decaying organic material in the water column, for example, algae, since strain T2T is able to utilize mannitol (Table 1). Mannitol is a major component of seaweed (Budavari, 1989) and it is also known to be a compound of algal exudates (Spencer, 1990). Strain T2T is a strictly aerobic and salt-requiring bacterium showing optimal growth in ASW/YPG medium with salt concentrations in the range 6·3–107 
and a maximum at 53·5 . The growth rate at 0·8 was significantly lower and no growth was observed when no salts were added. Besides the results shown in Table 1, strain T2T showed growth with cellobiose, succinate, fumarate, pyruvate, crotonic acid, 2-oxoglutarate, arginine and glutamic acid as sole sources of carbon and energy. No growth was observed with fructose, xylose, sucrose, maltose, citrate, ethanol, propanol, butanol, pimelic acid, inositol, benzoic acid, nicotinic acid, salicylic acid, asparagine, aspartic acid, cysteine, glutamine, glycine and histidine. In contrast to related organisms, strain T2T did not hydrolyse starch and casein (Table 1).
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9c, oleic acid), 10-methyl octadecanoic acid (10-Me C18 : 0, tuberculostearic acid) and 2-hydroxy hexadecanoic acid (2-OH C16 : 0, hydroxypalmitic acid). The fatty acid profiles of the Aeromicrobium species can be clearly distinguished from those of their close relatives Nocardioides albus ATCC 27980T and Kribbella sandramycini ATCC 39419T, which were characterized by other major fatty acids (compare data in supplementary table in IJSEM Online; http://ijs.sgmjournals.org). The cellular fatty acid profiles clearly distinguish the three Aeromicrobium species from their relatives. It is noteworthy that the major fatty acid tuberculostearic acid (10-methyl octadecanoic acid) was not found to the same extent in any other closely related species within the suborder Propionibacterineae (Schumann et al., 1997; Park et al., 1999). However, it was found in other genera within the order Actinomycetales, i.e. Mycobacterium, Microbispora, Micromonospora, Arthrobacter, Nocardia, certain Streptomyces spp. (Lechevalier, 1977) and Dietzia (Rainey et al., 1995).
Comparison of the almost-complete 16S rRNA gene sequence of strain T2T with sequences from GenBank demonstrated that this strain is the first described marine bacterium affiliated to the family Nocardioidaceae within the order Actinomycetales. The phylogenetic tree shown in Fig. 2 demonstrates that strain T2T forms a cluster with the two previously described Aeromicrobium species. Similarities between the 16S rRNA gene sequence of strain T2T and those of A. fastidiosum DSM 10552T and A. erythreum DSM 8599T were 97·7 and 97·0 %, respectively. Other members of the Actinomycetales can be readily distinguished from this branch (Fig. 2). The percentage of DNA–DNA relatedness was 44·4 % for strain T2T and A. erythreum DSM 8599T, and 29·1 % for strain T2T and A. fastidiosum DSM 10552T. The reference strains A. erythreum DSM 8599T and A. fastidiosum DSM 10552T exhibited a DNA–DNA relatedness of 30·7 %. According to Wayne et al. (1987), the phylogenetic definition of a species generally includes strains with more than 70 % DNA–DNA relatedness. Thus, strain T2T is clearly distinguishable from the existing Aeromicrobium species.
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). Tests with the addition of 
100- to 500-fold excess of genomic DNA of the natural community prior to PCR and hybridization analysis showed no interference with the detection of strain T2T DNA from a pure culture. The intensities of the hybridization signals for strain T2T alone or in combination with the natural community remained similar (compare first and second lane in Fig. 3). Some cross-hybridization was observed with DNA from A. erythreum DSM 8599T; however, the intensity of the hybridization signal was only 10 % of that obtained with the same concentration of DNA of strain T2T (Fig. 3). DNA of A. fastidiosum DSM 10552T gave only very faint hybridization signals (data not shown). This is probably due to nine non-homologous bases within the 16S rRNA gene sequence of A. fastidiosum DSM 10552T versus only six non-homologous bases within the sequence of A. erythreum DSM 8599T when aligned with the probe sequence. The weak signals obtained with A. erythreum DSM 8599T and A. fastidiosum DSM 10552T also indicate the specificity of the probe and the hybridization conditions developed for the detection of strain T2T. Based on the results of our dot-blot procedure, genomic DNA of strain T2T and possibly of very closely related strains represents 
1 % of the total genomic DNA of the natural community (Fig. 3). These results are consistent with those of the MPN counts and indicate a high abundance (1 %) of these bacteria in the natural pelagic community. High amounts of Gram-positive bacteria may result from wash-in events of terrestrial bacteria, as has been discussed previously (Goodfellow & Haynes, 1984). However, the fact that strain T2T is an obligately salt-requiring bacterium and shows its optimal growth at sea water salinities gives striking evidence for its indigenous abundance in a marine habitat, as demonstrated for other marine Gram-positive bacteria (Jensen et al., 1991; Jensen & Fenical, 1995).
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Aerobic. Cells are Gram-positive, non-motile rods that are 0·7–1·3 µm long and 0·3–0·5 µm wide. Ivory-coloured colonies are 0·5–1·0 mm in diameter and are characterized by a diffuse halo. Grows between 4 and 35 °C, with optimum growth at 25 °C. Growth occurs between pH 5·5 and 9·5, with optimum growth at pH 7·0–8·5. The optimal salinity for growth is 53·5 ; growth is possible between 0·8 and 107 . Catalase-positive and oxidase-negative. Does not reduce nitrate. Grows with the carbon sources trehalose, cellobiose, crotonic acid, 2-oxoglutarate, succinate, fumarate, mannitol, pyruvate, arginine and glutamic acid. Unable to hydrolyse starch, cellulose, lipids, chitin and casein. Contains LL-diaminopimelic acid as the diamino acid in the cell-wall peptidoglycan. The major menaquinone is MK-9(H4). The cellular fatty acids are predominantly hexadecanoic acid (palmitic acid), cis-9-octadecenoic acid (oleic acid), 10-methyl octadecanoic acid (tuberculostearic acid) and 2-hydroxy hexadecanoic acid (hydroxypalmitic acid).
The type strain is T2T (=DSM 15272T=LMG 21768T). The G+C content of its DNA is 70·6 mol%. Isolated from surface waters of the German Wadden Sea.
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ACKNOWLEDGEMENTS |
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