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1 Environmental and Molecular Microbiology Laboratory, Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), 373-1 Guseong-dong, Yuseong-gu, Daejeon 305-701, South Korea
2 Department Biologie I, Fakultät für Biologie, Ludwig-Maximilians-Universität München, Maria-Ward-Strasse 1a, D-80638 München, Germany
Correspondence
Jörg Overmann
j.overmann{at}lrz.uni-muenchen.de
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains PB56T, PB180 and PB229 are respectively AY769083, AY769084 and AY785128.
Details of the analysis of the carotenoids of the novel strains are available in a supplementary figure and table with the online version of this paper.
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TOPABSTRACTMAIN TEXTREFERENCES |
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). Bacteria of the order Sphingomonadales are characterized by glucuronosyl ceramide and 2-OH myristic acid or non-hydroxy myristic acid, which replace the lipopolysaccharides of the Gram-negative cell wall. They contain octadecenoic acid (C18 : 1
7c, C18 : 19t) as the major non-polar fatty acid and ubiquinone Q-10 as the major respiratory quinone.
Members of the Sphingomonadaceae have been repeatedly reclassified and presently comprise the six chemo-organotrophic genera Sphingomonas, Sphingobium, Sphingopyxis, Sphingosinicella, Novosphingobium and Zymomonas and six genera of aerobic anoxygenic phototrophic bacteria, Blastomonas, Erythrobacter, Erythromicrobium, Porphyrobacter, Sandaracinobacter and Sandarakinorhabdus. ‘Lutibacterium’ and ‘Citromicrobium’ represent two additional lineages (Takeuchi et al., 2001; Yabuuchi & Kosako, 2005; Gich & Overmann, 2006).
In an attempt to assess the diversity of aerobic phototrophic bacteria systematically, we isolated a large number of red-, orange- and yellow-pigmented bacteria from surface soil collected on the campus of the Korea Advanced Institute of Science and Technology (KAIST) in Daejeon city, South Korea. After collection, 1 g soil was suspended in distilled water and serially diluted (1 : 10) three times. Aliquots (100 µl) of each dilution were spotted on 10-fold-diluted R2A agar (Difco) plates and the plates were incubated at 25 °C. Isolated strains were also subcultured on undiluted R2A medium. For screening of the isolates, the pufL and pufM genes, which encode the typical type II photosynthetic reaction centre of proteobacteria, were amplified and sequenced as described by Nagashima et al. (1997). Of over 300 isolates, about 100 were found to contain the pufL and pufM genes. The three orange–red-pigmented strains PB56T, PB180 and PB229 were chosen for detailed characterization and were found to represent a novel lineage among the Sphingomonadaceae.
For an initial phylogenetic characterization, chromosomal DNA was extracted and purified using the DNeasy Tissue kit (Qiagen). PCR amplification of 16S rRNA genes and direct sequencing of the purified PCR products were performed as described previously (Yoon et al., 1997, 1998), thereby obtaining the almost-complete (i.e. 1393–1421 nt) 16S rRNA gene sequences of the strains. The 16S rRNA gene sequences of the closest relatives were retrieved by a BLAST search (Altschul et al., 1997) and the sequences were aligned with the CLUSTAL_X program (Thompson et al., 1997). Evolutionary distances were then calculated using the Kimura two-parameter model (Kimura, 1983) and a phylogenetic tree was constructed by neighbour joining (Saitou & Nei, 1987) in MEGA version 2.1 (Kumar et al., 2001) with bootstrap values based on 1000 replications (Felsenstein, 1985).
Based on the phylogenetic analysis (Fig. 1), strains PB56T, PB180 and PB229 are most closely related to species of the genus Sphingomonas, but form a distinct lineage which is supported by a bootstrap value of 100 %. The closest relatives of strain PB56T are Sphingomonas oligophenolica JCM 12082T (95.8 % 16S rRNA gene sequence similarity), Sphingomonas koreensis KCTC 2882T (95.1 %), Sphingomonas mali IFO 15500T (95.1 %), Sphingomonas faeni DSM 14747T (94.8 %), Sphingomonas pruni IFO 15498T (94.7 %), and Sphingomonas aquatilis KCTC 2881T (94.6 %). Although the 16S rRNA gene sequences of Sphingosinicella microcystinivorans Y2T and Sphingosinicella xenopeptidilytica 3-2W4T also showed rather high similarity (95.0–95.2 %), the three new isolates clustered with members of the genus Sphingomonas. This branching pattern was clearly supported by our bootstrap analysis (Fig. 1). Lower sequence similarities were found with the other described Sphingomonas species (<94.6 %) and with Sandaracinobacter sibiricus (92.3 %). The values of 16S rRNA gene sequence similarity suggest that the isolated strains represent a novel bacterial species within the genus Sphingomonas. The closest phylogenetic relatives listed above were selected for subsequent comparisons of physiological and biochemical features (Tables 1 and 2).
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; Tamaoka & Komagata, 1984). Genomic DNA of strains PB56T, PB180 and PB229 had a G+C content between 69.1 and 69.9 mol% (Table 1
), whereas the G+C content of all Sphingomonas species described to date ranges between 59 and 67 mol% (Yabuuchi et al., 2002).
The 16S rRNA gene sequence similarities between the three strains PB56T, PB180 and PB229 were 98.6–98.8 %. DNA–DNA hybridization was performed in five replicates by the fluorometric method of Ezaki et al. (1989). The DNA–DNA hybridization values between strains PB56T and PB180 were 67.7±11.7 % and those between strains PB56T and PB229 were 73.1±5.0 %. Based on the commonly accepted criteria for the delineation of a bacterial species (
70 % DNA–DNA hybridization and 97 % 16S rRNA gene sequence similarity; Rosselló-Mora & Amann, 2001), and considering the values of the standard deviations, the three isolated strains represent members of a single species.
All three strains formed orange–red, circular, convex and smooth colonies. As observed by phase-contrast microscopy (Zeiss Axiostar Plus), cells grown for 4 days at 25 °C in R2A broth were non-motile rods, 0.7 µm wide and 1.1 µm long. Cells were Gram-negative as determined by the KOH method (Buck, 1982), oxidase-positive (determined by oxidation of 1 % p-aminodimethylaniline oxalate) and catalase-positive (determined by gas production upon addition of 3 % H2O2). Growth was obligately aerobic. Reduction of nitrate and production of indole was not observed. The optimum temperature for growth on R2A agar was 25–30 °C. The strains did not require any vitamins. They did not grow on MacConkey agar (Difco) and only strain PB180 grew readily on nutrient agar at 25 °C (Table 1).
Substrate utilization was assessed with the API 20NE and API 32GN systems and enzyme activities were assessed with the API ZYM microtest system according to the recommendations of the manufacturer (bioMérieux). For reference, we chose the type strains of the five most closely related Sphingomonas species (see above) and Sphingosinicella microcystinivorans Y2T. In addition, the type strains of the four orange-pigmented species Sphingomonas abaci, Sphingomonas aerolata, Sphingomonas aurantiaca and Sphingomonas roseiflava were included in this comparison. The three newly isolated strains utilized D-glucose, L-rhamnose, N-acetylglucosamine, D-mannitol, 4-hydroxybenzoate, L-proline, L-serine and glycogen. In addition, L-arabinose, maltose, mannose, malate, malonate, adipate, caprate and salicin were utilized by individual strains. Of the enzymes tested, alkaline phosphatase, esterase (C4), esterase lipase (C8), leucine arylamidase and trypsin were present (Table 1). The three novel isolates differ from most of their closest phylogenetic relatives by the capacity to use D-mannitol, L-serine and 4-hydroxybenzoate, the poor utilization of gluconate and by the lack of 
-glucosidase (aesculin hydrolysis) and -galactosidase and the lack of growth on tryptic soy agar (Table 1).
For the analysis of fatty acids, the three strains were cultivated for 4 days at 25 °C on R2A agar. The cell mass was saponified and fatty acid methyl esters (FAMEs) were methylated and then extracted according to the protocol of the Sherlock Microbial Identification System (MIDI, Inc.). Fatty acids were analysed by gas chromatography (Hewlett Packard 6890) and identified by the Microbial Identification software package (Sasser, 1990).
Strains PB56T, PB180 and PB229 showed cellular fatty acid profiles with large amounts of the saturated and unsaturated fatty acids C16 : 0 (12.8 %), C16 : 1 (3.2 %), C17 : 1 (7.5 %), summed feature 7 (C18 : 17c/9t/12t) (41.0 %) and summed feature 4 (C16 : 17c/C15 : 0 iso 2-OH) (33.9 %) (Table 2). No significant differences in the fatty acid profiles were found between the three isolates. There were some differences in FAME composition between these strains and their nearest phylogenetic neighbours in the genera Sphingomonas, Erythrobacter, Erythromicrobium and Porphyrobacter. The common dominant fatty acids for all strains are C16 : 0 and summed feature 7. Strains PB56T, PB180 and PB229 differ from the related Sphingomonas species with respect to the absence of 2-OH myristic acid (C14 : 0 2-OH), which dominates the 2-hydroxy fatty acids in all other groups. 2-Hydroxy fatty acids are not completely absent in the novel isolates, however, since C18 : 1 2-OH occurs in strain PB180 (Table 2). Furthermore, C15 : 0 iso 2-OH (contained in summed feature 4) is potentially present in all three strains. Another conspicuous feature of strains PB56T, PB180 and PB229 is the large amount of fatty acids of summed feature 4 (C16 : 17c/C15 : 0 iso 2-OH), which has so far been found only in Sphingomonas faeni (Busse et al., 2003; Yabuuchi & Kosako, 2005) and Sphingosinicella microcystinivorans Y2T (Maruyama et al., 2006).
Isoprenoid quinones were extracted with chloroform/methanol (2 : 1, v/v) and purified by TLC on Merck silica gel 60F254 plates (20x20 cm, 0.5 cm thick) using a mixture of petroleum benzene and diethyl ether (85 : 15, v/v) as the solvent. Spots were scraped off and then analysed by HPLC as described earlier (Collins & Jones, 1981; Shin et al., 1996). The major isoprenoid quinone of isolates PB56T, PB180 and PB229 was ubiquinone Q-10, as in all known members of the Sphingomonadaceae (Rainey et al., 2003).
Within the genus Sphingomonas sensu stricto, only Sphingomonas (Blastomonas, Erythromonas) ursincola DSM 9006T and Sphingomonas (Blastomonas) natatoria DSM 3183T are currently known to be capable of synthesizing bacteriochlorophyll (BChl) a (Yabuuchi & Kosako, 2005). The other BChl a-containing members of the family Sphingomonadaceae are found within the genera Erythrobacter (Erythrobacter longus DSM 6997T, Erythrobacter litoralis DSM 8509T), Erythromicrobium [Erythromicrobium ramosum DSM 8510T, ‘Erythromicrobium ezovicum’ E-1, ‘Erythromicrobium hydrolyticum’ E4(1)] and Porphyrobacter (Porphyrobacter cryptus DSM 12079T, P. dokdonensis DSM 17193T, P. donghaensis DSM 16220T, P. neustonensis DSM 9434T, P. sanguineus ATCC 25659T, P. tepidarius DSM 10594T) and also include ‘Citromicrobium bathyomarinum’ JF-1, Sandaracinobacter sibiricus RB16-17T and Sandarakinorhabdus limnophila so42T (Hiraishi et al., 2002; Rainey et al., 2003; Yabuuchi & Kosako, 2005; Gich & Overmann, 2006; Yoon et al., 2004, 2006).
Using the 1.5 kb amplification product obtained for the pufLM genes (see above), the respective nucleotide sequences were determined and a phylogenetic tree was constructed as described for the 16S rRNA gene sequences. The pufLM gene sequences of strains PB56T, PB180 and PB229 were found to be most closely related to those of Sphingomonas (Blastomonas, Erythromonas) ursincola DSM 9006T and Sphingomonas (Blastomonas) natatoria DSM 3183T and to form a distinct lineage separate from all other species of the family Sphingomonadaceae, which is supported by high bootstrap resampling values (Fig. 2). The closer affiliation with the only BChl a-containing members of genus Sphingomonas sensu stricto rather than the other aerobic anoxygenic phototrophic genera is commensurate with the 16S rRNA gene phylogeny.
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. Spectra were recorded by an absorption UV/Vis diode array detector and recorded at 450 and 770 nm. At these wavelengths, absorbance coefficients used for quantification were 128.0 mol l–1 cm–1 (Yurkov et al., 1994) for carotenoids and 54.8 mol l–1 cm–1 for BChl a (Permentier et al., 2000), respectively. Excreted sulfated carotenoids were extracted directly from lyophilized culture supernatants. To remove the sulfate group, they were hydrolysed with 0.6 M HCl in tetrahydrofuran for 10 min at room temperature (http://lipidbank.jp/) and then subjected to HPLC analysis.
All strains produced numerous carotenoids. With the exception of spirilloxanthin and -carotene, which constituted only minor amounts (peaks 12 and 14; see Supplementary Fig. S1 available in IJSEM Online), all other compounds differed from known carotenoids with respect to retention time and absorption spectrum (Supplementary Table S1). However, most carotenoids were ketocarotenoids, as indicated by their absorption spectra, which exhibited only one broad maximum (data not shown). The main carotenoid was a very polar xanthophyll sulfate (compound 2 in Supplementary Fig. S1), but differed from erythroxanthin sulfate or caloxanthin sulfate produced by Erythrobacter longus and Erythromicrobium ramosum (Supplementary Table S1). The spectra of PB180 and PB229 were almost identical (Supplementary Fig. S1b), but differed from the spectrum of PB56T (Supplementary Fig. S1a and Supplementary Table S1). Strains PB180 and PB229 released part of the sulfated carotenoid into the medium during growth. The excreted sulfated carotenoid corresponded to peak 2 of the cellular extract.
No BChl a was detected in cells of strain PB56T, whereas cells of strains PB180 and PB229 contained small amounts of BChl a. Aerobic anoxygenic photosynthetic bacteria analysed so far contain BChl a esterified with phytol (BChl aP; Takaichi, 1999). Strain PB229 also had BChl aP (Supplementary Fig. S1b, peak c). In addition, PB180 contained two more types of BChl a, tentatively identified as BChl a esterified with farnesol (BChl aF; Supplementary Fig. S1b, peak a) and BChl a esterified with geranylgeraniol (BChl aGG; Supplementary Fig. S1b, peak b) based on a comparison with pigment extracts from Rhodobacter capsulatus DSM 155 and from Rhodospirillum rubrum DSM 107. The ratio of BChl a to cell dry weight ranged from 0.5 (strain PB229) to 12.2 (PB180) µg g–1, depending on the medium composition and the illumination. The maximum cellular BChl a content in strain PB180 thus reached 6.4x10–22 mol per cell, which is about 200 times lower than the average BChl a content of aerobic anoxygenic photosynthetic bacteria (1.2x10–19 mol per cell; Jiao et al., 2003; Kolber et al., 2001). The ratio of BChl a to carotenoids in the cells of strains PB180 and PB229 ranged from 1 : 60 to 1 : 600.
Strains PB56T, PB180 and PB229 thus differ clearly from Sphingomonas (Blastomonas) ursincola DSM 9006T and Sphingomonas natatoria DSM 3183T and from the type species of the aerobic anoxygenic phototrophic genera Sandaracinobacter, Erythrobacter, Erythromicrobium and Porphyrobacter in that they were non-motile, differed in colour, did not contain nostoxanthin and zeaxanthin and had no (PB56T) or only trace amounts (PB180, PB229) of BChl a. These morphological and physiological differences are in accordance with the sequence divergence of the respective 16S rRNA and pufLM genes.
Based on the results of the present characterization, strains PB56T, PB180 and PB229 are classified as members of the genus Sphingomonas sensu stricto (Takeuchi et al., 2001). However, the three strains represent a separate phylogenetic lineage and exhibit considerable physiological differences from the recognized Sphingomonas species such as non-motile cells, orange–red colour, lack of -glucosidase and -galactosidase, utilization of D-mannitol, L-serine and 4-hydroxybenzoate and lack of 2-OH myristic acid. Therefore, strains PB56T, PB180 and PB229 are assigned to a novel species, for which the name Sphingomonas kaistensis sp. nov. is proposed.
Description of Sphingomonas kaistensis sp. nov.
Sphingomonas kaistensis [ka.is.ten'sis. N.L. fem. adj. kaistensis of or pertaining to the Korea Advanced Institute of Science and Technology (KAIST)].
Cells are 0.7 µm wide and 1.1 µm long. Gram-negative, non-motile, non-spore-forming rods that grow aerobically. Colonies are circular, entire, low-convex, smooth, opaque and orange–red-coloured and grow chemo-organotrophically on R2A agar (Difco) without requirement for vitamins. All known strains contain two structural genes of the type II photosynthetic reaction centre (pufL and pufM), but BChl a synthesis is detected in strains PB180 and PB229 only in very small amounts. Oxidase- and catalase-positive. Optimum temperature is 25–30 °C. Nitrate is not reduced to nitrite or N2. Indole is not produced. Strains are positive for enzyme activities of alkaline phosphatase, esterase (C4), esterase lipase (C8), leucine arylamidase and trypsin and negative for enzyme activities of arginine dihydrolase, lipase (C14), N-acetyl--glucosaminidase, protease (gelatin hydrolysis), urease, -glucosidase (aesculin hydrolysis), 
-galactosidase, -galactosidase (PNPG hydrolysis), -glucuronidase, -fucosidase and -mannosidase. Strains do not grow on MacConkey agar. All strains utilize D-glucose, L-rhamnose, D-mannitol, N-acetylglucosamine, 4-hydroxybenzoate, L-proline, L-serine and glycogen. 2-Ketogluconate, 5-ketogluconate, acetate, propionate, valerate, citrate, lactate, phenylacetate, L-alanine and L-histidine are not utilized. The DNA base composition is 69.1–69.9 mol% G+C. The major isoprenoid quinone is ubiquinone Q-10 and major cellular fatty acids are C18 : 1, summed feature 4 (C16 : 17c/C15 : 0 iso 2-OH) and C16 : 0, but cells lack any 2-hydroxy fatty acid.
The type strain is PB56T (=KCTC 12334T=DSM 16846T), which was isolated from soil on the campus of KAIST in Daejeon city in South Korea.
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ACKNOWLEDGEMENTS |
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