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1 Abteilung Mikrobiologie, Universität Osnabrück, 49069 Osnabrück, Germany
2 Institut für Angewandte Mikrobiologie, Universität Giessen, Germany
Correspondence
André Lipski
lipski{at}biologie.uni-osnabrueck.de
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Present address: SGS Institut Fresenius GmbH, Pestalozzistrasse, 78333 Stockach, Germany. 
Present address: Symrise GmbH & Co. KG, Mühlenfeldstrasse 1, 37601 Holzminden, Germany.
Present address: Gymnasium Lohne, An der Kirchenziegelei 12, 49393 Lohne, Germany.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of Chryseobacterium gleum CCUG 14555T, Chryseobacterium indologenes LMG 8337T, strain F-Fue-04IIIaaaaT, strain 5-1St1aT, strain 26-3St2bT and strain DW3T are AM232812, AM232813, AM232806, AM232810, AM232809 and AJ534853, respectively.
API ZYM profiles, polar lipid patterns, pigment absorption spectra and scanning electron micrographs of cells of the four novel isolates are available as supplementary material with the online version of this paper.
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and contained five species, C. balustinum (Harrison, 1929), C. indoltheticum (Campbell & Williams, 1951), C. indologenes (Yabuuchi et al., 1983), C. gleum (Holmes et al., 1984) and C. scophthalmum (Mudarris et al., 1994). The species number remained constant until 2003 when C. defluvii (Kämpfer et al., 2003) and C. joostei (Hugo et al., 2003) were described. In 2005 five more species of the genus were added to the list of approved bacterial names, while six more species were described in 2006. The strains that were isolated and described during the last 4 years were isolated from a broad spectrum of environmental sources, such as activated sludge (Kämpfer et al., 2003), soils and sediments (Kim et al., 2005a; Shen et al., 2005; Tai et al., 2006), rhizosphere (Young et al., 2005; Park et al., 2006) and also from the food processing industry (Hugo et al., 2003; Shimomura et al., 2005; de Beer et al., 2005). This demonstrated that the genus Chryseobacterium encompasses a group of organisms that is ubiquitous in nature.
In this report we describe four novel species of this genus, which were isolated from surfaces of beer-bottling plants located in three different breweries in Germany. Strain DW3T was isolated from a biofilm collected from a bottling plant conveyor (Timke et al., 2004), whereas strains 5-1St1aT, 26-3St2bT and F-Fue-04IIIaaaaT were isolated from cleaned steel coupons that were mounted onto the outer surfaces of the beer-bottling plant and exposed overnight to the airborne microbiota of the filling area. The type strains of C. defluvii and Chryseobacterium formosense were used as reference strains (Kämpfer et al., 2003; Young et al., 2005). Other reference strains were obtained from the DSMZ, the CCUG and the LMG. All isolates and reference strains were cultivated on trypticase soy agar at 25 °C.
Genomic DNA was isolated using a DNeasy Tissue kit according to the instructions of the manufacturer (Qiagen). The 16S rRNA gene of the purified chromosomal DNA was amplified using the universal bacterial primers GM3F and GM4R (Muyzer et al., 1995). An ABI PRISM BigDye Terminator Cycle Sequencing Ready Reaction kit v2.0 (Applied Biosystems) was used for the sequencing reaction. The sequencing primers used were 518F, 787R and 1099F (Buchholz-Cleven et al., 1997). Sequencing products were purified using a DyeEx Spin kit (Qiagen) and electrophoresis was performed on an ABI377 (Applied Biosystems) sequencer. The sequences, each at a length of more than 1400 bases, were compared with the National Center for Biotechnology Information nucleotide sequence database using the BLAST program (Altschul et al., 1997). BLAST analyses revealed that the 16S rRNA gene sequences of all four isolates shared the highest similarity with type strains of species exclusively of the genus Chryseobacterium. The type strain with the most similar sequence to that of strain 5-1St1aT was C. formosense CC-H3-2T (97.5 % sequence similarity). C. joostei LMG 18212T showed the highest sequence similarities to strains DW3T and F-Fue-04IIIaaaaT (96.9 and 98.3 %, respectively). The next most closely related type strain to isolate 26-3St2bT was Chryseobacterium caeni N4T, with a sequence similarity of 96.4 %. A phylogenetic analysis was performed by using MEGA version 3.1 (Kumar et al., 2004). The phylogenetic reconstruction, based on a neighbour-joining analysis, placed all four isolates within the genus Chryseobacterium (Fig. 1). The 16S rRNA genes of the reference strains C. gleum CCUG 14555T and C. indologenes LMG 8337T were also sequenced and included in the analysis because sequences available for these species were of poor quality.
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. Menaquinones (MK) were analysed using a Hewlett Packard series 1050 HPLC equipped with an ODS Hypersil column and a diode-array detector. Methanol and isopropyl ether (9 : 2, v/v) were used as the mobile phase with a flow rate of 1.0 ml min–1 and a column temperature of 30 °C (Hu et al., 1999). The quinone type of the four strains was identical to those of the reference strains analysed and was therefore identified as MK-6. The polar lipids of the novel isolates were composed of phosphatidylethanolamine, several aminolipids and other polar lipids (see Supplementary Fig. S1, available in IJSEM Online). The two-dimensional patterns of the polar lipids of the isolates and reference strains analysed (not shown) were highly similar and in accordance with published data (Kämpfer et al., 2003; Kim et al., 2005a).
Fatty acid analysis was performed on the novel isolates and the four reference strains using cells grown on trypticase soy agar for 24 h at 30 °C. Saponification with 15 % NaOH in 50 % methanol, acid methylation with 6 M HCl in 50 % methanol and extraction of fatty acid methyl esters were performed as described by Sasser (1990). The fatty acid methyl esters extracts were analysed by GC-FID using a Hewlett Packard model 6890 gas chromatograph equipped with a 5 % phenyl-methyl-silicone capillary column. The identity of the fatty acids was verified by GC-MS with a Hewlett Packard model 5890 series II gas chromatograph equipped with a 5 % phenyl-methyl-silicone capillary column and a model 5972 mass selective detector. The chromatographic conditions used were as described previously (Lipski & Altendorf, 1997). The positions of double bonds were verified by analysing the dimethyl-disulfide adducts of the fatty acid methyl esters (Nichols et al., 1986). The positions of hydroxy-, methyl- and cyclopropene groups and double bonds were given from the carboxyl group of the fatty acid molecule according to the recommendations of the IUPAC-IUB Commission on Biochemical Nomenclature (CBN) (1977). The fatty acid profiles of the isolates showed the branched chain fatty acid 15 : 0 iso as the major compound. Other predominating compounds were 17 : 1 iso cis9 and the hydroxy fatty acids 17 : 0 iso 3-OH and 15 : 0 iso 2-OH.
An in-depth analysis of the fatty acid profiles revealed some discrepancies with the profiles published previously for this genus (Mudarris et al., 1994; Bernardet et al., 2005; Kim et al., 2005b; Quan et al., 2007). We identified a compound as 17 : 1 iso cis9 that was previously named by the MIDI system as 17 : 1 iso 
9c. The different position of the double bond was clearly located by mass spectrometric analysis of the DMDS adducts of the fatty acid methyl esters. All reference strains analysed showed this compound (Table 1). This indicates that 17 : 1 iso cis9 instead of 17 : 1 iso 9c is the usual compound of the fatty acid profiles of members of this genus. The compounds 15 : 0 iso 2-OH and 16 : 1 cis9 (identical to 16 : 17c) were not separated by the chromatographic system used. Discrete amounts for both fatty acids were calculated after DMDS derivatization of unsaturated fatty acids. We found that only 15 : 0 iso 2-OH was present in all isolates and reference strains. The fatty acid 16 : 1 cis9 was detected only in some strains and therefore can be used as a differential feature within the genus.
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). Lambda-DNA was used as a reference. The DNA G+C contents of the isolates were 36.4 mol% for strain F-Fue-04IIIaaaaT, 37.8 mol% for strain 5-1St1aT, 39.2 mol% for strain DW3T and 38.1 mol% for strain 26-3St2bT. For the reference strain C. joostei CCUG 46665T, a G+C content of 36.9 mol% was obtained, which conforms to the data published by Hugo et al. (2003) for this species.
Flexirubin-type pigments were detected after extraction with acetone by their absorption, with a maximum absorbance at 450 nm and a shift to higher wavelengths after addition of 20 % KOH (Yabuuchi et al., 1983). Pigments were detected in strains F-Fue-04IIIaaaaT and 5-1St1aT and the four reference strains (see Supplementary Fig. S2 in IJSEM Online), but not in strains 26-3St2bT or DW3T. All isolates stained Gram-negative using the standard method of Gerhardt et al. (1981). This result was confirmed by using the non-staining KOH and the aminopeptidase tests according to Buck (1982) and Cerny (1978), respectively.
Cell morphology and motility were analysed by phase-contrast microscopy (Zeiss axioscope) of cells incubated for 3 h in trypticase soy broth at 30 °C and at room temperature. Cell dimensions were measured with Zeiss KS300 software from phase-contrast micrographs, based on a minimum of 100 cells. Cells of all isolates were non-motile and rod-shaped. For scanning electron microscopy, cells were grown overnight in trypticase soy broth at 30 °C and spread on polylysine-coated slides. The samples were fixed with glutaraldehyde (2.5 %), dehydrated with a graded ethanol series, dried by critical-point drying with liquid carbon dioxide and coated with gold. Preparations were observed using a Zeiss DSM 962 scanning electron microscope. No flagella were detected (see Supplementary Fig. S3 in IJSEM Online). All chemotaxonomic and morphological data were in accordance with the genus description (Vandamme et al., 1994) and confirmed the assignment of the novel isolates to the genus Chryseobacterium.
The sequence similarities between the novel isolates and the reference type strains were below 98.3 %, indicating that the isolates may represent novel species. Statistical analysis based on Keswani & Whitman (2001) predicted a DNA–DNA hybridization value of less than 70 % from a sequence similarity of 98.6 % with a high level of confidence (99 %). A DNA–DNA hybridization value of 70 % is accepted for species delineation (Wayne et al., 1987). Within the genus Chryseobacterium the sequence similarity between closely related but different species can be as high as 99.3 %, as reported for the C. scophthalmum–Chryseobacterium piscium–C. balustinum complex (de Beer et al., 2006). Hybridization experiments were performed with genomic DNA from the novel isolates and DNA from the next most closely related type strains, C. joostei LMG 18212T and C. formosense CC-H3-2T. The method described by Ziemke et al. (1998) was used except that, for nick translation, 2 µg DNA was labelled during a 3 h incubation at 15 °C. These experiments revealed hybridization values of 21 % (reciprocal 22 %) between strain F-Fue-04IIIaaaaT and C. joostei LMG 18212T, 26 % (reciprocal 35 %) between strain 5-1St1aT and C. formosense CC-H3-2T, 44 % (reciprocal 45 %) between strain 26-3St2bT and C. joostei LMG 18212T and 44 % (reciprocal 40 %) between strain DW3T and C. joostei LMG 18212T. The closely related isolates DW3T and 26-3St2bT showed a hybridization value of 25 % (reciprocal 30 %), which supported the separation of these isolates as representing two different species.
Biochemical tests were performed at 25 °C on the isolates and the four reference strains according to MacFaddin (1980) unless indicated otherwise. Growth at 5, 25, 37 and 42 °C and in the presence of 1, 2, 3, 4 and 5 % NaCl was tested on nutrient agar, containing 5 g peptone l–1, 3 g meat extract l–1 and 15 g agar l–1. The susceptibility to 11 antimicrobials was determined by using the disc-diffusion method with susceptibility test discs (Oxoid). API ZYM, API 20E and API 20NE profiles (bioMérieux) were recorded according to the recommendations of the manufacturer. In addition to the carbohydrates included in the API 20E galleries, acid production from mannitol, adonitol, rhamnose, myo-inositol, sorbitol and dulcitol was also examined using Hugh and Leifson's O–F medium (MacFaddin, 1980). Haemolytic activity was tested on Columbia agar with 5 % sheep blood (bioMérieux). Phenotypically, strain F-Fue-04IIIaaaaT could be differentiated from all other strains tested including the next most closely related type strain, C. joostei CCUG 46665T, by a set of biochemical characteristics such as urease activity and resistance to erythromycin and tetracycline (Table 2). Phylogenetically, strain 5-1St1aT was only distantly related to C. formosense CC-H3-2T, although the two strains showed high 16S rRNA gene sequence similarity. Accordingly, several phenotypic markers differed between both taxa: amounts of the fatty acids 16 : 1 cis9 and 17 : 1 iso cis9, growth at 37 and 4 °C, formation of indole, assimilation of glucose, arabinose and maltose, susceptibility to kanamycin and trypsin, and 
- and β-glucosidase activities (Tables 1
and 2 and Supplementary Table S1 in IJSEM Online). In contrast to all isolates and reference strains analysed, strain 5-1St1aT showed two absorption maxima (455 and 479 nm) when acetone-extracted pigments were treated with 20 % KOH (see Supplementary Fig. S2 in IJSEM Online). Strains DW3T and 26-3St2bT differed from all other Chryseobacterium strains by the absence of flexirubin-type pigments. This property was also reported for the closely related genus Sejongia (Yi et al., 2005), but the strains of this genus were phylogenetically well separated from strains DW3T and 26-3St2bT and also showed different chemotaxonomic properties such as the presence of 16 : 0 iso and different amounts of 15 : 0 iso and 16 : 1 cis9 (Table 1 and Yi et al., 2005). Morphologically, strains DW3T and 26-3St2bT showed the smallest cell length (about 1.3 µm) of all strains analysed (see Supplementary Fig. S3 in IJSEM Online). Phenotypically, strains DW3T and 26-3St2bT could be separated based on growth in the presence of 2 % NaCl, reduction of nitrate, growth on adipate and susceptibility to ampicillin. Isolate DW3T was the only strain in our study that showed this susceptibility. This is also in contrast to all other representatives of the genus Chryseobacterium (Vandamme et al., 1994; Michel et al., 2005).
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). Three of the novel strains were isolated from short-term exposed steel coupons. This indicates the involvement of Chryseobacterium strains in the rapid recolonization of cleaned plant surfaces and their participation in biofilm formation.
Description of Chryseobacterium ureilyticum sp. nov.
Chryseobacterium ureilyticum (u.re.i.ly'ti.cum. N.L. fem. n. urea urea; Gr. adj. lyticus dissolving; N.L. neut. adj. ureilyticum urea-dissolving).
Cells are aerobic, non-spore-forming, non-motile rods, approximately 2.0 µm (SD 0.4 µm) in length and 0.7 µm (SD 0.1 µm) in width. After growth for 2 days at 30 °C on trypticase soy agar, colonies are circular and yellow-pigmented with a diameter of 2–3 mm. Gram-negative and oxidase- and catalase-positive. Yellow flexirubin-type pigments are produced. Grows at 25 °C but not at 4 or 37 °C. Grows on plain nutrient agar and on nutrient agar containing up to 2 % NaCl, but not on nutrient agar containing 3 % NaCl. Growth occurs on Cetrimide agar but not on MacConkey or Simmons' citrate agars. Positive for urease, gelatinase and haemolytic activities; production of indole; and hydrolysis of aesculin and Tweens 20 and 80. Negative for starch hydrolysis; oxidation of gluconate; fluorescence on King B agar; production of acetoin; lecithinase, arginine dihydrolase, lysine and ornithine decarboxylases and tryptophan deaminase activities; reduction of nitrate and nitrite to N2; production of H2S; and acid formation from glucose, lactose, sucrose, arabinose, rhamnose, mannitol, adonitol, myo-inositol, sorbitol, dulcitol, melibiose and amygdalin. Glucose and maltose are utilized as sole carbon sources, but arabinose, mannose, N-acetylglucosamine, gluconate, adipate, malate, citrate, phenylacetate and caprate are not. Susceptible to novobiocin, nalidixic acid, neomycin, furazolidone and fusidic acid and resistant to kanamycin, streptomycin, erythromycin, tetracycline, ampicillin and gentamicin. Major fatty acids are 15 : 0 iso, 17 : 1 iso cis9, 17 : 0 iso 3-OH and 15 : 0 iso 2-OH. Predominant respiratory quinone type is MK-6. Polar lipids are composed of phosphatidylethanolamine, several aminolipids and other polar lipids. The G+C content of the genomic DNA of the type strain is 36.4 mol%.
The type strain, F-Fue-04IIIaaaaT (=DSM 18017T=CCUG 52546T), was isolated from a steel surface of a beer-bottling plant in Germany.
Description of Chryseobacterium gambrini sp. nov.
Chryseobacterium gambrini [gam.bri'ni. N.L. gen masc. n. gambrini of Gambrinus, the alleged ‘god of beer’ of the German students (17th century)].
Cells are aerobic, non-spore-forming, non-motile rods, approximately 3.6 µm (SD 1.1 µm) in length and 1.1 µm (SD 0.3 µm) in width. After growth for 2 days at 30 °C on trypticase soy agar, colonies are circular and yellow-pigmented with a diameter of approximately 2 mm. Gram-negative and oxidase- and catalase-positive. Yellow flexirubin-type pigments are produced. Growth occurs at 25, 37 and 42 °C, but not at 4 °C. Grows on plain nutrient agar and on nutrient agar containing up to 1 % NaCl, but not on nutrient agar containing 2 % NaCl. Growth occurs on Cetrimide agar but not on MacConkey or Simmons' citrate agars. Positive for gelatinase and haemolytic activities and hydrolysis of aesculin and Tweens 20 and 80. Negative for starch hydrolysis; oxidation of gluconate; fluorescence on King B agar; production of acetoin and indole; lecithinase, urease, arginine dihydrolase, lysine and ornithine decarboxylases and tryptophan deaminase activities; reduction of nitrate and nitrite to N2; production of H2S; and acid formation from glucose, lactose, sucrose, arabinose, rhamnose, mannitol, adonitol, myo-inositol, sorbitol, dulcitol, melibiose and amygdalin. Glucose, arabinose, mannose, maltose, adipate and phenylacetate are utilized as sole carbon sources, but N-acetylglucosamine, malate, citrate and caprate are not. Susceptible to kanamycin, streptomycin, erythromycin, tetracycline, gentamicin, novobiocin, nalidixic acid, neomycin, furazolidone and fusidic acid and resistant to ampicillin. Major fatty acids are 15 : 0 iso, 17 : 0 iso 3-OH, 15 : 0 iso 2-OH and17 : 1 iso cis9. Predominant respiratory quinone type is MK-6. Polar lipids are composed of phosphatidylethanolamine, several aminolipids and other polar lipids. The G+C content of the genomic DNA of the type strain is 37.8 mol%.
The type strain, 5-1St1aT (=DSM 18014T=CCUG 52549T), was isolated from a steel surface of a beer-bottling plant in Germany.
Description of Chryseobacterium pallidum sp. nov.
Chryseobacterium pallidum (pal'li.dum. L. neut. adj. pallidum pale).
Cells are aerobic, non-spore-forming, non-motile rods, approximately 1.3 µm (SD 0.3 µm) in length and 0.8 µm (SD 0.1 µm) in width. After growth for 2 days at 30 °C on trypticase soy agar, colonies are circular and pale-cream-coloured with a diameter of approximately 1 mm. Gram-negative and oxidase- and catalase-positive. Does not produce flexirubin-type pigments. Growth occurs at 25 and 37 °C but not at 4 or 42 °C. Grows on plain nutrient agar and on nutrient agar containing up to 1 % NaCl, but not on nutrient agar containing 2 % NaCl. No growth occurs on Cetrimide, MacConkey or Simmons' citrate agars. Positive for gelatinase, lecithinase and haemolytic activities; production of indole; nitrate reduction; and hydrolysis of aesculin and Tweens 20 and 80. Negative for starch hydrolysis; oxidation of gluconate; fluorescence on King B agar; production of acetoin; urease, arginine dihydrolase, lysine and ornithine decarboxylases and tryptophan deaminase activities; production of H2S; and acid formation from glucose, lactose, sucrose, arabinose, rhamnose, mannitol, adonitol, myo-inositol, sorbitol, dulcitol, melibiose and amygdalin. Glucose, arabinose, mannose, maltose, adipate and malate are utilized as sole carbon sources, but N-acetylglucosamine, gluconate, phenylacetate, citrate and caprate are not. Susceptible to kanamycin, streptomycin, erythromycin, tetracycline, gentamicin, novobiocin, nalidixic acid, neomycin, furazolidone and fusidic acid and resistant to ampicillin. Major fatty acids are 15 : 0 iso, 16 : 1 cis9 and 17 : 0 iso 3-OH. Predominant respiratory quinone type is MK-6. Polar lipids are composed of phosphatidylethanolamine, several aminolipids and other polar lipids. The G+C content of the genomic DNA of the type strain is 38.1 mol%.
The type strain, 26-3St2bT (=DSM 18015T=CCUG 52548T), was isolated from a steel surface of a beer-bottling plant in Germany.
Description of Chryseobacterium molle sp. nov.
Chryseobacterium molle (mol'le. L. neut. adj. molle pliant, sensitive, referring to the sensitivity to antibiotics).
Cells are aerobic, non-spore-forming, non-motile rods, approximately 1.3 µm (SD 0.8 µm) in length and 0.9 µm (SD 0.1 µm) in width. After growth for 2 days at 30 °C on trypticase soy agar, colonies are circular and pale-cream-coloured with a diameter of approximately 1 mm. Gram-negative and oxidase- and catalase-positive. Does not produce flexirubin-type pigments. Growth occurs at 25 and 37 °C but not at 4 or 42 °C. Grows on plain nutrient agar and on nutrient agar containing up to 2 % NaCl, but not on nutrient agar containing 3 % NaCl. No growth occurs on Cetrimide, MacConkey or Simmons' citrate agars. Positive for gelatinase, lecithinase and haemolytic activities; production of indole; and hydrolysis of aesculin and Tweens 20 and 80. Negative for starch hydrolysis; oxidation of gluconate; fluorescence on King B agar; production of acetoin; urease, arginine dihydrolase, lysine and ornithine decarboxylases and tryptophan deaminase activities; reduction of nitrate and nitrite to N2; production of H2S; and acid formation from glucose, lactose, sucrose, arabinose, rhamnose, mannitol, adonitol, myo-inositol, sorbitol, dulcitol, melibiose and amygdalin. Glucose, arabinose, mannose, maltose and malate are utilized as sole carbon sources, but N-acetylglucosamine, gluconate, adipate, phenylacetate, citrate and caprate are not. Susceptible to kanamycin, streptomycin, erythromycin, tetracycline, ampicillin, gentamicin, novobiocin, nalidixic acid, neomycin, furazolidone and fusidic acid. Major fatty acids are 15 : 0 iso, 15 : 0 anteiso, 16 : 1 cis9 and 17 : 0 iso 3-OH. Predominant respiratory quinone type is MK-6. Polar lipids are composed of phosphatidylethanolamine, several aminolipids and other polar lipids. The G+C content of the genomic DNA of the type strain is 39.2 mol%.
The type strain, DW3T (=DSM 18016T=CCUG 52547T), was isolated from a biofilm of a beer-bottling plant conveyor of a brewery in Germany.
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ACKNOWLEDGEMENTS |
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