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GBF National Research Center for Biotechnology, Department of Environmental Microbiology, Mascheroder Weg 1, 38124 Braunschweig, Germany
Correspondence
Wolf-Rainer Abraham
wab{at}gbf.de
ABSTRACT |
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Published online ahead of print on 31 October 2003 as DOI 10.1099/ijs.0.02746-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences of Labrys monachus VKM B-1479T, Angulomicrobium tetraedrale VKM B-1335T, Angulomicrobium amanitiforme NCIMB 1785T, Stella humosa DSM 5900T and Stella vacuolata DSM 5901T are AJ535707AJ535711, respectively, and that for [Angulomicrobium] sp. VKM B-1336 is AJ542534.
Present address: MPI, Max Planck Institute for Molecular Genetics, Department of Vertebrate Genomics, Ihnestr. 73, 14195 Berlin, Germany.
INTRODUCTION |
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TOP ABSTRACT INTRODUCTION METHODS RESULTS AND DISCUSSION REFERENCES |
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In 1984, Vasil'eva and Semenov described a strain of budding prosthecate bacteria that was isolated from silt of Lake Mustijärv in the former Estonian SSR (Vasil'eva & Semenov, 1984). Based on radial cell symmetry, multiplication by budding and the presence of prosthecae, the authors placed this strain, VKM B-1479T, in a novel genus with the orthographically incorrect name Labrys monahos (Vasil'eva & Semenov, 1984). The name of this strain has been validly published as Labrys monachus (Vasil'eva & Semenov, 1985). Cells of this strain consisted of flat, triangular cells with prosthecae in two of the three corners, which allows clear morphological distinction from other genera of budding bacteria. So far, the phylogenetic position of L. monachus VKM B-1479T has not been determined.
The first mushroom-shaped, budding bacterium was described by Whittenbury & Nicoll (1971). The authors isolated strain NCIMB 1785T from fresh pond water; this strain differed from previously described budding bacteria in a number of properties, including dividing mode, cell morphology and fine structure (Whittenbury & Nicoll, 1971). This strain has not yet been assigned to a genus or species. A morphologically similar, non-motile, Gram-negative strain (Z-2821T=VKM B-1335T=DSM 5895T) was isolated in 1972 from a cumulative culture of methane-oxidizing bacteria that were sampled from a lowland marsh in Abramtsevo, near Moscow (Namsaraev & Zavarzin, 1973, 1974). Vasil'eva and co-workers (Lafitskaya & Vasil'eva, 1976; Vasil'eva et al., 1980) reported an additional mushroom-shaped bacterial strain, Z-1109 (=VKM B-1336), and proposed a novel genus, Angulomicrobium, with the type species Angulomicrobium tetraedrale VKM B-1335T (Vasil'eva et al., 1986). Despite certain morphological and physiological dissimilarities to strain VKM B-1335T, these authors included strain VKM B-1336 in the genus Angulomicrobium without attributing it to a particular species (Vasil'eva et al., 1980). Two additional strains that resembled mushroom-shaped bacteria were isolated by Stanley et al. (1976). So far, no data on the taxonomic affiliation of mushroom-shaped bacteria have been published.
The aim of the present work was to determine the taxonomy of the type strains of the genera Labrys, Stella and Angulomicrobium by lipid analysis and comparison of 16S rRNA gene sequences. Furthermore, the phylogenetic positions of strains NCIMB 1785T and VKM B-1336 have been determined, resulting in the proposal of Angulomicrobium amanitiforme sp. nov., with the type strain NCIMB 1785T.
METHODS |
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16S rDNA sequencing.
Almost-complete 16S rRNA genes were amplified by PCR from the strains listed in Table 1 and were sequenced as described previously (Abraham et al., 1999). Resulting sequences were aligned with reference 16S rRNA gene sequences (Stoesser et al., 2002; Cole et al., 2003) by the ARB program package (Ludwig et al., 2003), using the evolutionarily conserved primary sequence and secondary structure as references (Gutell et al., 1985). Evolutionary distances (Jukes & Cantor, 1969) were calculated from pairwise similarities of complete sequences by using only homologous, unambiguously determined nucleotide positions. A phylogenetic tree was constructed by using the DNADIST and FITCH programs of the PHYLIP package (Felsenstein, 1989).
Lipid analysis
Polar lipid fatty acid analysis.
Lipids were extracted by using a modified BlighDyer procedure (Bligh & Dyer, 1959) and fatty acid methyl esters were generated and analysed by GC, as described previously (Vancanneyt et al., 1996).
Tandem mass spectrometry (MS).
Fast atom bombardment-MS in the negative mode was performed on the first of two mass spectrometers of a tandem, high-resolution instrument (JMS-HX/HX110A; JEOL) as described previously (Abraham et al., 1997). A mixture of triethanolamine and tetramethylurea was used as the matrix. Negative daughter ion spectra were recorded by using all four sectors of the tandem mass spectrometer. Helium served as the collision gas for generating collision-induced dissociation (CID) for identification of prominent molecular ions.
RESULTS AND DISCUSSION |
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TOP ABSTRACT INTRODUCTION METHODS RESULTS AND DISCUSSION REFERENCES |
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Contrary to DNADNA reassociation data, the genus Stella appears to be quite consistent in terms of morphology, physiology, nutrient requirements and DNA G+C content (approx. 6773 mol%) (Hirsch & Schlesner, 1981; Vasilyeva, 1985). Major distinguishing traits are the occurrence of gas vacuoles in some strains and low DNADNA hybridization values that are reported between a number of strains.
Mass spectra of the phospholipid fractions from Stella spp. showed mainly molecular ions with even mass numbers, pointing to the presence of mainly nitrogen-bearing phospholipids. Although CID-MS for identification of compounds could not be run, due to scarcity of material, the recorded masses, together with the fatty acids found in the polar lipid fraction, strongly favour the presence of phosphatidylethylamine and phosphatidylcholine. Additionally, two unidentified lipids with molecular ions at m/z 893 and 1042 were observed. Sittig & Schlesner (1993) reported the presence of phosphatidyl N-methylethylamine, phosphatidylcholine and cardiolipin for Stella strains; however, the latter could not be detected in the mass spectra. Furthermore, they found relatively high amounts of long-chain hydroxy fatty acids.
Genus Labrys
L. monachus VKM V-1479T exhibited 16S rRNA gene sequence similarities of 9192 % to the most closely related genera, namely species of Mesorhizobium, Rhodopseudomonas and Azorhizobium (Fig. 1). This confirmed the separation of L. monachus VKM B-1479T at the genus level, as has been suggested previously on the basis of morphological and physiological data (Vasil'eva & Semenov, 1984). 16S rRNA gene sequence data did not allow us to affiliate VKM B-1479T with any of the most closely related families that were suggested by Garrity et al. (2001), namely Rhizobiaceae, Brucellaceae, Phyllobacteriaceae, Methylocystaceae, Beijerinckiaceae and Bradyrhizobiaceae. Additionally, L. monachus VKM B-1479T is not affiliated to the family Hyphomicrobiaceae, as has been suggested by Garrity et al. (2001). VKM B-1479T may be assigned to a separate family, Labryaceae, in the future. However, due to the availability of only one strain for characterization, it is too early to resolve the affiliation of L. monachus VKM B-1479T at family level.
Four different types of polar lipid could be detected in this strain: phosphatidylglycerol, phosphatidyl N,N-dimethylethylamine, phosphatidylcholine and a lipid with a mass of 827 Da that belonged to an unknown type of phospholipid. With the aid of CID-MS, most compounds were elucidated. CID of the (M-H) ion yielded abundant carboxylate anions from both the sn-1 and the sn-2 position, thus allowing identification of the fatty acids attached to the different lipids. In addition, there were neutral losses of the sn-2 and sn-1 substituent as free carboxylic acid, as well as loss of each fatty acyl group as a substituted ketene. Furthermore, the positions of the fatty acids at the glycerol backbone could be determined. For the fatty acid positioned at sn-2, neutral loss as free fatty acid, as well as substituted ketene, is more frequent than for that at sn-1 (Murphy & Harrison, 1994). By this method, the structure of the phospholipids was identified (Abraham et al., 1997); Table 2 summarizes the results. Several differences in the structure of the phospholipids can be found between L. monachus VKM B-1479T and A. tetraedrale DSM 5895T (Table 2), which can be used to differentiate between these two genera. Such differentiation was not possible on the basis of phospholipid types alone (Sittig & Schlesner, 1993).
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Strain VKM B-1336, which was originally proposed to be a member of the genus Angulomicrobium, was included in the genus description (Vasil'eva et al., 1980) despite observed differences in morphology, substrate utilization, ultrastructure and mode of division. We determined overall 16S rRNA gene sequence similarity between strains VKM B-1336 and VKM B-1335T (=DSM 5895T) to be as low as 91 %. This points to a remote relationship above genus level between these strains. 16S rDNA sequence data suggest that strain VKM B-1336 is affiliated to the genus Mesohizobium (Fig. 1).
Strain NCIMB 1785T shared 99·4 % 16S rDNA sequence similarity with strain VKM B-1335T (=DSM 5895T). This confirmed the affiliation of strain NCIMB 1785T with the genus Angulomicrobium, which was suggested by earlier morphological and physiological data (Whittenbury & Nicoll, 1971; Stanley et al., 1976; Vasil'eva et al., 1980). DNADNA hybridization between A. tetraedrale DSM 5895T and strain NCIMB 1785T gave 60·6 % DNADNA similarity. An accepted recommendation by Wayne et al. (1987) suggested that strains that share >70 % DNADNA similarity should be included in the same species. Therefore, we propose that strain NCIMB 1785T should be placed in a novel species, Angulomicrobium amanitiforme sp. nov.
Four different types of polar lipids were detected in strains DSM 5895T and NCIMB 1785T: phosphatidylglycerol, phosphatidyl N,N-dimethylethylamine, phosphatidylcholine and lipids that belonged to an unknown type of phospholipid (Table 2). Phosphatidylglycerol was only found in A. tetraedrale DSM 5895T; strain NCIMB 1785T lacked this class of phospholipids. From the structure of the different phospholipids, it is apparent that strain NCIMB 1785T prefers C19 : 08,9 cyclopropyl fatty acids more than strain DSM 5895T, and that all main lipids of strain NCIMB 1785T had this fatty acid. Angulomicrobium strains were the only strains in this study to possess unidentified lipids with masses of 932 and 946 Da. Their CID spectra all showed the formation of glycerophosphatic acid (GPA) ions, identifying this group of polar lipids as phospholipids. Analysis of GPAs revealed the fatty acids and their relative position at the glycerol backbone of these unknown phospholipids. Further studies are needed to identify these lipids, which may be glycophospholipids.
In this study, it was demonstrated for the two type strains of Stella species that high 16S rDNA sequence similarity (99 %) does not necessarily correspond to high DNA similarity [DNADNA hybridization value <15 %; data from Reimer & Schlesner (1989)]. This well-known phenomenon (Regenhardt et al., 2002; Stackebrandt et al., 2002 and references therein) also applies to the genus Angulomicrobium. Although strains NCIMB 1785T and VKM B-1335T share 99·4 % 16S rRNA gene sequence similarity, they are not related at species level, as shown by DNADNA hybridization. Aside from this, strain NCIMB 1785T differs from A. tetraedrale VKM B-1335T by the use of citrate, D-()-ribose and L-serine as substrates and the inability to utilize D-(+)-malate, D-(+)-mannose, D-(+)-melibiose, methylamine hydrochloride and L-(+) and D-()-tartrate as substrates.
Description of Angulomicrobium amanitiforme sp. nov.
Angulomicrobium amanitiforme (a.ma.ni'ti.for.me. N.L. n. Amanita name of fungal genus; L. adj. suffix -formis -is -e -like, of the shape of; N.L. neut. adj. amanitiforme formed like a toadstool).
The description of the species is as that for the genus, with the following additions. Cells are non-motile, non-spore-forming, capsulated and irregularly shaped. They are 1·0x1·5 µm in size with radial symmetry and show tetrahedral cell morphology during the early stages of cell replication. A complex membranous system is not developed, but in addition to the cytoplasmic membrane, some peripherally aligned membranes and a membranous cell body at the site of cell division are present. The budding process is initiated by doubling the tube part of the cell, followed by enlargement of the tube part end-section. Finally, symmetric fission of the tube forms two mushroom-shaped cells. Colonies are white, round and mucous with a pearly shine. However, there is a second colony morphology with smaller, non-slimy colonies. Nutritional type is chemoorganotrophic. CO2 in the presence of H2 is not utilized as a sole carbon and energy source. Organic growth factors are not required, but do stimulate growth. Glucose, arabinose, galactose, fructose, mannitol, glycerol, formate, acetate, propionate, lactate, fumarate, succinate, citrate and glutarate are used as sole carbon and energy sources, whereas mannose, lactose, maltose, sucrose, dulcitol, butyrate, tartrate, urea, glycine and methanol are not. Contrary to VKM B-1335T, strain NCIMB 1785T utilizes citrate, D-()-ribose and L-serine and does not utilize D-(+)-malate, D-(+)-mannose, D-(+)-melibiose, methylamine hydrochloride or (L+)- or (D)-tartrate. Metabolism is strictly aerobic. Catalase and oxidase activities are present. Nitrate, carbonate and sulfate are not utilized as electron acceptors. Cytochromes a, b and c are present. Acids are produced from sugar and sugar alcohols. Growth temperature ranges from 15 to 40 °C, with an optimum growth temperature between 28 and 30 °C. At 30 °C, growth occurs at pH values between 5·2 and 8·0, with an optimum at pH 6·87·0. Main phospholipids are phosphatidyl N,N-dimethylethylamine and phophatidylcholine, containing at least one C19 : 08,9 cyclopropyl fatty acid. DNA G+C content is 67·7 mol% for the type strain. 16S rRNA gene sequencing places this species in the Alphaproteobacteria. DNADNA hybridization between the type strain and A. tetraedrale DSM 5895T was 60·6 %.
The type strain of the species is NCIMB 1785T (=DSM 15561T).
ACKNOWLEDGEMENTS |
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