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1 Centre for Agricultural Landscape and Land Use Research (ZALF), Institute of Primary Production and Microbial Ecology, Gutshof 7, D-14641 Paulinenaue, Germany
2 Centre for Agricultural Landscape and Land Use Research (ZALF), Institute of Primary Production and Microbial Ecology, Eberswalder Str. 84, D-15374 Müncheberg, Germany
3 DSMZ – German Collection of Microorganisms and Cell Cultures, Mascheroder Weg 1b, D-38124 Braunschweig, Germany
Correspondence
Undine Behrendt
ubehrendt{at}zalf.de
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences analysed in this study are AJ492831 (Pseudomonas trivialis P 513/19T=DSM 14937T=LMG 21464T), AJ492829 (Pseudomonas poae P 527/13T=DSM 14936T=LMG 21465T), AJ492828 (Pseudomonas congelans P 538/23T=DSM 14939T=LMG 21466T), AJ492830 (genotype E1 P 515/12=DSM 14938=LMG 21467), AJ492826 (Pseudomonas tremae CFBP 6111T) and AJ492827 (Pseudomonas cannabina CFBP 2341T).
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). Some species have a strictly commensal relationship with their host plants. Furthermore, potentially phytopathogenic pseudomonads can be found on their specific hosts, as well as on plant species that are not susceptible to these pathogens.
Studies of bacterial communities that live in the phyllosphere of grasses showed that predominantly fluorescent Pseudomonas species comprised most Gram-negative bacteria present (Behrendt, 2001). Most of them were phenotypically highly similar to the saprophytic species Pseudomonas fluorescens or to Pseudomonas syringae, a potentially phytopathogenic bacterium. Moreover, strains that showed physiological similarity to the phytopathogenic species Pseudomonas viridiflava or Pseudomonas cichorii were isolated, but their taxonomic affiliations were ambiguous. Thus, a selection of these strains was characterized by a polyphasic approach to clarify their interspecific position within the genus Pseudomonas.
Isolation of strains from the phyllosphere
Samples of grass plots, characterized by different intensities of management, were taken to investigate the community structures of heterotrophic bacteria, as described by Behrendt (2001). Grass material was homogenized in distilled water by using a Stomacher lab blender and serial dilutions were plated on nutrient agar (SIFIN), supplemented by 0·4 g cycloheximide l-1, to obtain selectivity for bacterial growth. After incubation at 21 °C for 7 days, a representative number of strains was isolated to determine the community structure of culturable heterotrophic bacteria. Isolates were subjected to taxonomic investigations; one set of strains of fluorescent pseudomonads showed a negative arginine dihydrolase reaction and an indefinite taxonomic affiliation after physiological characterization by both conventional tests and application of the commercial Biolog identification system. These strains were used for further studies. Strain numbers of isolates studied and type strains used for comparison are shown in Table 1.
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. 16S rRNA genes were amplified with primers described by Weisburg et al. (1991), resulting in amplification of a single fragment of approximately 1500 bp. Digestion of these PCR products by a set of endonucleases (TaqI, HinfI, AluI, MspI, CfoI, HaeIII and ScrFI) showed identical patterns for almost all isolates; only two, P 516/20 and P 538/23, revealed differences in patterns for two of the enzymes (AluI and ScrFI). These results indicate high 16S rDNA sequence similarity. Thus, genetic classification of strains according to differences in physiological features could not be carried out by using this method. In order to classify the isolates by a method of higher taxonomic resolution, strains were studied by ribotyping with the restriction enzyme EcoRI, which was species-specific within the genus Pseudomonas (Sikorski et al., 2001). These analyses were performed with the automated RiboPrinter Microbial Characterization system (Qualicon DuPont). Band patterns were compared by using the BioNumerics software (Applied Maths). Clustering was carried out by UPGMA based on Pearson's correlation coefficient (optimization coefficient, 1·2 %). This procedure revealed grouping of isolates into six genotypes (Fig. 1). Four of these genotypes (A, B, D and E1), which had similarities between ribopatterns of <60 %, were chosen for further phylogenetic studies. Strains of genotype C were not considered, as no effective physiological characteristics were found to differentiate them clearly from isolates of genotype A (Table 2). Although a few phenotypic features were found that differentiated ribotype E2 from E1, the former was also excluded from further studies due to high similarity between ribopatterns.
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. For phylogenetic analysis, 16S rDNA sequences of 77 strains, that represented type strains of all authentic species of the genus Pseudomonas were chosen (except for Pseudomonas gelidicola, for which no 16S rDNA sequence was available). Furthermore, some strains that represented species without validly published names were involved. Sequences were aligned by using the CLUSTALX algorithm (Thompson et al., 1997) and trees were constructed by using the neighbour-joining (Saitou & Nei, 1987) and maximum-likelihood (Felsenstein, 1981) algorithms (PHYLIP version 3.57; Felsenstein, 1993). Both trees showed that the investigated isolates clustered clearly within the genus Pseudomonas (data not shown). Species that formed a closely related cluster with the grass isolates were selected for more detailed phylogenetic analyses. A phylogenetic tree based on 1282 nt (Escherichia coli positions 99–1376) was constructed for this subset of species, as shown in Fig. 2.
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, whereas the strain with genotype D was in the ‘P. syringae group’. As indicated by restriction analysis of 16S rDNA, sequences were highly similar among grass isolates. In particular, a comparison of genotypes A and B revealed 99·93 % similarity. The closest phylogenetic neighbours of both isolates were Pseudomonas veronii and Pseudomonas rhodesiae, with a similarity between 99·3 and 99·4 % (based on a binary comparison of the available length of sequences). The representative strain of genotype E1 displayed highest similarity to Pseudomonas cedrina (99·9 %) and Pseudomonas synxantha (99·0 %), whereas the closest phylogenetic neighbours of genotype D were pathovars of Pseudomonas savastanoi, which displayed similarities of 99·6–99·8 %. Such high conformity in 16S rDNA sequence between species was, to a large extent, found in the studied subset of pseudomonads shown in Fig. 2
. Accordingly, most bootstrap values were relatively low and only certain branches were confirmed by the topology of the maximum-likelihood tree.
To clarify the interspecific position of the investigated genotypes, DNA–DNA hybridization studies were performed according to a method described previously (Martin et al., 1997). Representative strains of genotypes were tested against each other and against species with validly published names that were the closest phylogenetic neighbours, as estimated by binary comparison of 16S rDNA sequences. As shown in Table 3, all tested pairings of genotypes A, B and D resulted in reassociation values <70 %, indicating separate species status. However, hybridization studies between genotype E1 and P. cedrina revealed similarities of 76·4 and 78·3 %, suggesting an affiliation to the species P. cedrina.
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. All grass isolates studied were Gram-negative, non-spore-forming, rod-shaped organisms that occurred as single cells. The cells were motile by means of one or two polar flagella. Colonies were colourless, translucent and formed a green fluorescent pigment on media B and A of King et al. (1954).
Each strain gave positive results for catalase, aesculin hydrolysis and aerobic acid formation from glucose (Hugh & Leifson, 1953). The following characteristics were negative for all strains: hydrolysis of starch, formation of levan from sucrose, reduction of nitrate to nitrite, denitrification, arginine dihydrolase, DNase, indole production, formation of H2S from sodium thiosulphate, utilization of D-tartrate on Dye's medium (Sands, 1990) and 
-haemolysis of sheep blood. Production of oxidase was assayed on an early growth-phase culture with the aid of Bactident Oxidase test strips (Merck). Strains that developed a purple colour after 20–60 s, the time-span given by the manufacturers for a positive reaction, were considered oxidase-weak. Results of oxidase tests are shown in Table 2.
Assimilation of carbon substrates was determined by using Biolog GN MicroPlates as recommended by the manufacturers (MicroLog System, release 4.0). Results were read visually after 48 h incubation at 30 °C. A survey of the assimilation of substances is given in the species descriptions. Physiological tests that were different among the genotypes determined by ribotyping are shown in Table 2.
Taxonomic conclusions
The fluorescent pseudomonads studied, isolated from the phyllosphere of grasses, are composed of six genotypes as determined by ribotyping. The four that showed highest dissimilarity in ribopatterns and physiological features were chosen for further phylogenetic studies. Comparison of 16S rDNA sequences between representative strains and almost all authentic Pseudomonas species revealed a clear affiliation to the genus Pseudomonas sensu stricto. DNA–DNA hybridization studies of these strains and their nearest phylogenetic neighbours (as determined by 16S rDNA sequence comparisons) indicated separate species status for three of the genotypes studied.
This result is supported by phenotypic features. The yellow-pigmented, halophilic, marine bacterium P. gelidicola, which was not used in 16S rDNA analysis, differed clearly from the grass isolates in its ability to hydrolyse agar and requirement of NaCl for growth (Holt et al., 1994). By 16S rDNA analysis, strains of genotypes A and B (Pseudomonas trivialis sp. nov. and Pseudomonas poae sp. nov., respectively) were grouped with species characterized by a positive arginine dihydrolase reaction (Rudolph et al., 1990; Coroler et al., 1996; Elomari et al., 1996; Dabboussi et al., 1999; Baïda et al., 2002; Gardan et al., 2002; Ivanova et al., 2002; Munsch et al., 2002). They can thus be easily distinguished from their nearest phylogenetic neighbours. Phenotypic features that are effective for differentiation from physiologically similar species, characterized in particular by a negative arginine dihydrolase reaction, are shown in Table 4.
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. Pseudomonas savastanoi, Pseudomonas ficuserectae, Pseudomonas meliae and Pseudomonas amygdali were included as separate species, although extensive DNA–DNA hybridization studies by Gardan et al. (1999) revealed that, together with certain pathovars of P. syringae, they formed a single genomospecies and should therefore be considered as synonymous. Unfortunately, the authors did not formally propose an emended species description, as no phenotypic features were found to distinguish them from six other genomospecies delineated by DNA–DNA hybridization studies of 48 P. syringae pathovars.
Genomic heterogeneity of P. syringae pathovars, as revealed by DNA–DNA hybridization studies (Gardan et al., 1999), is linked with phenotypic differences as shown by Gardan et al. (1991) and makes species demarcation more difficult. Thus, several physiological features in Table 4 would be listed as variable, because of differences between pathovars. Therefore, P. syringae was not included in Table 4. However, phenotypic characterization of 48 P. syringae pathovars and eight related species by Gardan et al. (1999) showed that <10 % of strains studied were able to utilize D-trehalose; they can thus be differentiated from the grass isolates of genotypes A, B and D (P. trivialis, P. poae and P. congelans, respectively), which are positive for this feature. Furthermore, characterization of phenotypic relationships by Billing (1970), Gardan et al. (1991), Hildebrand et al. (1994) and Young & Triggs (1994) showed that pathovars of P. syringae can be differentiated from the grass isolates by a combination of the following features: levan sucrase, aesculin and gelatin hydrolysis, oxidase, ice nucleation activity and utilization of erythritol.
DNA–DNA hybridization studies of the representative strain of genotype E1 revealed an affiliation to the species P. cedrina. However, in contrast to the strains of P. cedrina that were isolated from Lebanese spring water (Dabboussi et al., 1999), grass-associated isolates were characterized by negative arginine dihydrolase and levan sucrase reactions. Furthermore, strains of genotype E1 were not able to assimilate D-trehalose, erythritol, D-sorbitol or adonitol. Thus, the grass isolates showed differences in physiological features that are normally used to distinguish species.
In summary, three of the four characterized grass-associated genotypes can be distinguished from all Pseudomonas species with validly published names on the basis of phenotypic and phylogenetic features. Consequently, the names Pseudomonas trivialis sp. nov., Pseudomonas poae sp. nov. and Pseudomonas congelans sp. nov. are proposed.
General description of novel Pseudomonas species and strains of genotype E1
Cells are Gram-negative, non-spore-forming rods that occur as single cells. Colonies on King A and B media are white-yellowish, smooth with regular margins and produce a pigment with light yellow-green fluorescence on irradiation with UV light. Metabolism is respiratory. Optimal growth temperature is 21 °C. Growth can be observed at 4 °C, but none of the isolates is able to grow at 41 °C.
Each species is positive for catalase, aesculin hydrolysis and aerobic acid formation from glucose. The following characteristics are negative: hydrolysis of starch, formation of levan from sucrose, reduction of nitrate to nitrite, denitrification, arginine dihydrolase, DNase, indole production, formation of H2S from sodium thiosulphate, utilization of D-tartrate and -haemolysis of sheep blood.
Results obtained with Biolog GN MicroPlates show that the species oxidize the following substrates: L-arabinose, D-arabitol, bromosuccinic acid, D-fructose, D-galactose, m-inositol, D-mannitol, D-mannose, methyl pyruvate, acetic acid, cis-aconitic acid, citric acid, D-galactonic acid lactone, D-galacturonic acid, D-gluconic acid, D-glucosaminic acid, D-glucuronic acid, 
-ketoglutaric acid, malonic acid, propionic acid, D-saccharic acid, succinic acid, glucuronamide, L-alaninamide, D-alanine, L-alanine, L-asparagine, L-aspartic acid, L-glutamic acid, itaconic acid, L-leucine, L-pyroglutamic acid, L-serine, L-threonine, Tween 80, 
-aminobutyric acid, urocanic acid, inosine, uridine and glycerol. None of the strains assimilated N-acetyl-D-galactosamine, adonitol, D-arabitol, -cyclodextrin, dextrin, L-fucose, gentiobiose, glucose 1-phosphate, methyl -D-glucoside, -D-lactose, lactulose, maltose, D-melibiose, D-raffinose, turanose, xylitol, sebacic acid, L-phenylalanine, thymidine, phenylethylamine or 2,3-butanediol.
Description of Pseudomonas trivialis sp. nov.
Pseudomonas trivialis (tri.vi.a'lis. L. fem. adj. trivialis trivial).
Cells are motile by one polar flagellum and are 1·6–3·3 µm long and about 0·8 µm wide. Oxidase reaction is weak and ice nucleation activity is negative. In addition to the general description, the following substances are assimilated: formic acid, -D-glucose, -ketovaleric acid, glycyl L-glutamic acid, L-histidine, -hydroxybutyric acid, -ketobutyric acid, D-alanine, L-proline, quinic acid, monomethyl succinate, succinamic acid, D-trehalose and Tween 40. None of the strains assimilates i-erythritol, glucose 6-phosphate, glycogen, glycolyl L-aspartic acid or D-psicose. Gelatinase, casein hydrolysis and utilization of N-acetyl-D-glucosamine, D-cellobiose, L-rhamnose, -hydroxybutyric acid, -hydroxybutyric acid, DL-lactic acid, hydroxy-L-proline, L-ornithine, D-serine, DL-carnitine, putrescine, 2-aminoethanol, DL--glycerolphosphate, p-hydroxyphenylacetic acid and D-sorbitol are strain-dependent.
The type strain, P 513/19T (=DSM 14937T=LMG 21464T), was isolated from the phyllosphere of grasses in Paulinenaue (Germany).
Description of Pseudomonas poae sp. nov.
Pseudomonas poae (po'ae. Gr. n. poa grass; N.L. gen. n. poae of/from grass).
Cells are motile by one polar flagellum and are 2·5–3·3 µm long and about 0·8 µm wide. Strains show a weak oxidase reaction. Ice nucleation activity is negative. In addition to the general description, the following substances are assimilated: 2-aminoethanol, -hydroxybutyric acid, L-proline, L-histidine, DL-lactic acid, putrescine, quinic acid, succinaminic acid, sucrose, D-trehalose and Tween 40. None of the strains assimilates -hydroxybutyric acid, D-cellobiose, i-erythritol, glucose 6-phosphate, DL--glycerol phosphate, glycyl L-aspartic acid, p-hydroxyphenylacetic acid, -ketovaleric acid, D-sorbitol or L-rhamnose. Gelatinase, casein hydrolysis and utilization of glycogen, N-acetyl-D-glucosamine, -D-glucose, D-psicose, monomethyl succinate, formic acid, -hydroxybutyric acid, -ketobutyric acid, glycyl L-glutamic acid, hydroxy-L-proline, L-ornithine, D-serine and DL-carnitine are strain-dependent.
The type strain, P 527/13T (=DSM 14936T=LMG 21465T), was isolated from the phyllosphere of grasses in Paulinenaue (Germany).
Description of Pseudomonas congelans sp. nov.
Pseudomonas congelans (con.ge'lans. L. part. adj. congelans freezing/forming ice).
Cells are motile by one polar flagellum and are 2·5–2·9 µm wide and about 0·8 µm long. Strains are positive for gelatinase, casein hydrolysis and ice nucleation activity. Oxidase reaction is negative. In addition to the general description, the following substances are assimilated: DL-lactic acid, 2-aminoethanol, i-erythritol, -D-glucose, glycyl L-glutamic acid, DL--glycerol phosphate, -hydroxybutyric acid, -hydroxybutyric acid, formic acid, L-histidine, monomethyl succinate, L-proline, D-psicose, quinic acid, D-sorbitol, D-serine, succinamic acid, sucrose, D-trehalose and Tween 40. None of the strains assimilates N-acetyl-D-glucosamine, DL-carnitine, D-cellobiose, glucose 6-phosphate, glycyl L-aspartic acid, -hydroxybutyric acid, hydroxy-L-proline, glycogen, p-hydroxyphenylacetic acid, -ketovaleric acid, L-ornithine, putrescine or L-rhamnose.
The type strain, P 538/23T (=DSM 14939T=LMG 21466T), was isolated from the phyllosphere of grasses in Paulinenaue (Germany).
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ACKNOWLEDGEMENTS |
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