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Life Science Research Center, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa 252-8510, Japan
Correspondence
Dalal Asker
dasker{at}brs.nihon-u.ac.jp
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ABSTRACT |
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6c (34.5 %) and C18 : 17c (29.3 %). The presence of Q-10 as the main ubiquinone, the Sphingomonadaceae-specific sphingoglycolipid in the polar lipid profile and 2-hydroxy fatty acids, plus the absence of 3-hydroxy fatty acids, supported identification of this strain as a member of the genus Sphingomonas sensu stricto. Phylogenetic distinctiveness and unique phenotypic characteristics differentiated strain TDMA-16T from closely related Sphingomonas species. The results of polyphasic taxonomic analyses suggest that strain TDMA-16T represents a novel Sphingomonas species, for which the name Sphingomonas jaspsi sp. nov. is proposed. The type strain is strain TDMA-16T (=NBRC 102120T=DSM 18422T=CCUG 53607T).
SEMs of cells of strain TDMA-16T are available as supplementary material with the online version of this paper.
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TOPABSTRACTMAIN TEXTREFERENCES |
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. Subsequently, the genus description was emended (Takeuchi et al., 2001; Yabuuchi et al., 2002) and included in the second edition of Bergey's Manual of Systematic Bacteriology (Yabuuchi & Kosako, 2005). The family comprises the genera Blastomonas, Erythromonas, Sandaracinobacter, Sandarakinorhabdus, Sphingomonas, Sphingosinicella and Zymomonas; it has been proposed recently that the genus Sphingomonas, the type genus of this family that was originally described by Yabuuchi et al. (1990), should be divided into four genera, Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis (Takeuchi et al., 2001). Sphingomonads are strictly aerobic, chemoheterotrophic, Gram-negative bacteria that are of biotechnological interest due to their ability to degrade various xenobiotic substances (Ederer et al., 1997; Zablotowicz et al., 1999; Zipper et al., 1996) and also their potential to produce useful exopolysaccharides (White et al., 1996) and carotenoids (Silva et al., 2004).
Zeaxanthin (3,3'-dihydroxy-
-carotene) is a natural, fat-soluble, yellowish carotenoid that is found in some plants, algae and photosynthetic bacteria (Nelis & De Leenheer, 1989), where it serves as an accessory light-gathering pigment, as well as a protectant against the toxic effects of UV radiation and oxygen radicals. Zeaxanthin is currently utilized as an ingredient in feed for fish and poultry to enhance the pigmentation of animal flesh and egg yolk. Additionally, this pigment has a remarkable potential for use in pharmaceuticals as it prevents age-related macular degeneration and tumour formation. At present, the commercial production of zeaxanthin is carried out mostly by extraction from plant tissues or chemical synthesis. However, there is great potential for the development of a large-scale production system for microbial zeaxanthin.
Recently, some carotenoid-producing bacteria were isolated from freshwater samples that were collected at Misasa (Tottori, Japan), a region known for its high natural radioactivity (Kametani & Matsumura, 1983). A comprehensive taxonomic characterization based on 16S rRNA gene sequences has revealed a unique diversity of carotenoid producers that exist in this radioactive region (D. Asker, T. Beppu & K. Ueda, unpublished results). Among the isolates, a unique heterotrophic, aerobic, yellow-pigmented bacterium (strain TDMA-16T) was found that belongs to the Sphingomonadaceae. This paper deals with the taxonomic characteristics of this organism.
Strain TDMA-16T was isolated from a water sample collected at Misasa on 1 September, 2005 by the conventional dilution-plating method using nutrient agar (NA; Difco). Unless otherwise specified, all the characteristics described hereafter are those of cells of strain TDMA-16T grown on NA for 48 h at 37 °C. The phylogenetic position of the isolate was studied by using standard analysis based on the 16S rRNA gene sequence. The genomic DNA of strain TDMA-16T was extracted using a bacterial genomic DNA purification kit (Edge BioSystems). The DNA fragment that contained the nearly complete 16S rRNA gene of strain TDMA-16T (1431 bp) was amplified using the bacterial universal primers B8F (5'-AGAGTTTGATCCTGGCTCAG; nt 8–27 based on Escherichia coli numbering) and B1492R (5'-GGTTACCTTGTTACGACTT; nt 1510–1492 based on E. coli numbering). The 16S rRNA gene was sequenced directly by using a BigDye Terminator v3.1 cycle sequencing kit on an ABI 3100 automated DNA sequencer (Applied Biosystems).
A sequence similarity search in the GenBank/EMBL/DDBJ nucleotide sequence database performed using the program BLASTN (http://www.ncbi.nlm.nih.gov/blast/) revealed that strain TDMA-16T belongs to the family Sphingomonadaceae. Highest similarity was found with sequences of established species of the genus Sphingomonas sensu stricto including Sphingomonas mali IFO 15500T (95.1 %), Sphingomonas aquatilis JSS7T (95.0 %), Sphingomonas pruni IFO 15498T (94.9 %), Sphingomonas melonis DSM 14444T (94.9 %), Sphingomonas asaccharolytica IFO 15499T (94.5 %), Sphingomonas faeni MA-olkiT (94.3 %), Sphingomonas aerolata NW12T (94.2 %), Sphingomonas abaci C42T (94.2 %), Sphingomonas echinoides ATCC 14820T (94.2 %), Sphingomonas panni C52T (94.0 %) and Sphingomonas aurantiaca MA101bT (93.9 %). These results clearly demonstrated that strain TDMA-16T represents a novel species within the genus Sphingomonas sensu stricto.
A neighbour-joining phylogenetic tree was constructed using the programs CLUSTAL W (Thompson et al., 1994) and NJ plot (Perrière & Gouy, 1996). The tree topology was estimated by bootstrap analysis (Felsenstein, 1993) with 1000 resamplings of the dataset. Phylogenetic analysis of a nearly full-length 16S rRNA gene sequence of strain TDMA-16T indicated that it is a member of the genus Sphingomonas sensu stricto (Takeuchi et al., 2001), forming a distinct phylogenetic lineage (Fig. 1). The 16S rRNA gene sequence of strain TDMA-16T retained all the signature nucleotides, namely C : G at position 52 : 359, G at position 134, G at position 593, G : C at position 987 : 1218 and U : G at position 990 : 1215 (based on E. coli numbering) (Brosius et al., 1978), that are conserved in the genus Sphingomonas sensu stricto (Takeuchi et al., 2001).
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and bacterial cells were observed under a Zeiss Axioskop 2 microscope (Carl Zeiss Microimaging). SEM observation was performed using a model VE-8800 (Keyence). Anaerobic growth was assessed on NA incubated in a GasPak anaerobic system (BBL). The following tests were performed as described in each reference: casein hydrolysis (Norris et al., 1985); catalase activity, spore formation and hydrolysis of Tween 80, DNA and starch (Smibert & Krieg, 1994); and hydrolysis of chitin, carboxymethylcellulose (high viscosity; Sigma) and agar (Barrow & Feltham, 1993). Oxidase activity was tested by using commercial cytochrome oxidase test strips (BioChemika). Other enzyme activities, growth on carbohydrates, acid production from carbohydrates, nitrate reduction, and the production of H2S, indole and acetoin were examined using the commercial systems API 20E, API 20NE and API 50 CH (bioMérieux) according to the manufacturer's instructions. To determine optimal growth temperature, the strain was cultivated on NA at 4, 10, 20, 30, 37, 40 and 45 °C. NaCl tolerance was studied using nutrient broth (NB) supplemented with different concentrations of NaCl. Growth at pH 3.0–10.0 was evaluated in NB adjusted with HCl or NaOH. To determine the survival rate after exposure to gamma radiation, cells of strain TDMA-16T were grown on NA plates and suspended in NB (5 ml). Aliquots of the cell suspension (1 ml) were irradiated at 2.35 kGy (13 Gy min–1, 137Cs source), serially diluted and plated onto NA. The plates were incubated aerobically at 37 °C. E. coli C600 was treated similarly. Percentage survival was determined by comparison with unirradiated cultures. Cells of strain TDMA-16T were Gram-negative, pleomorphic, motile, short rods (0.4–0.5x0.7–1.0 µm). Spores were not observed. Buds formed on the mature cells (see SEMs available as Supplementary Fig. S1 in IJSEM Online). Strain TDMA-16T formed yellow-pigmented, convex, circular colonies (1–2 mm in diameter) after 48 h incubation at 37 °C. The temperature range for growth of strain TDMA-16T was 20–40 °C (optimum, 35–37 °C). No growth occurred at 45 °C. The pH range for growth was pH 6.0–9.0 (optimum, pH 6.0–7.0). Strain TDMA-16T was strictly aerobic and chemo-organotrophic. The strain was positive for oxidase and catalase, but negative in the oxidation/fermentation test and gas/acid production test with glucose. Strain TDMA-16T was slightly tolerant to gamma-ray irradiation, showing 0.45 % survival rate after exposure to a 2.3 kGy dose (13 Gy min–1, 137Cs source). At this dose, the survival rate of E. coli C600 was 0 %.
Other phenotypic properties of strain TDMA-16T are given in the species description and those characteristics that differentiate strain TDMA-16T from related members of the genus Sphingomonas sensu stricto are listed in Table 1.
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The yellow pigments were extracted by agitating bacterial cells in methanol on a rotary shaker (100 r.p.m.) at 50 °C in the dark until the cells were bleached followed by centrifugation at 5000 g for 5 min. The resultant supernatant was scanned for absorbance between 260 and 700 nm at room temperature on a Hitachi U2000 spectrophotometer. Carotenoid composition was characterized by HPLC-MS (LCMS-2010EV; Shimadzu) using a Shim-Pack FC-ODS (150x4.6 mm, 5 µm particle size; column temperature 35 °C) and acetonitrile : methanol : tetrahydrofuran (5.8 : 3.5 : 0.7, by vol.) as the mobile phase at a flow rate of 0.8 ml min–1. Zeaxanthin was identified by its retention time, absorption spectrum and molecular mass. Commercial zeaxanthin (DHI; Water & Environment) was used as a standard. The menaquinone content was determined by an HPLC method (Collins, 1994) using an extract of Sphingopyxis alaskensis DSM 13593T and Sphingomonas asaccharolytica NBRC 15499T as a reference for Q-10. The fatty acid methyl esters of strain TDMA-16T were extracted and analysed according to the standard protocol of the Sherlock Microbial Identification System (version 5.0; MIDI). Glycosphingolipids were analysed by TLC as described by Kawahara et al. (1991) and Takeuchi et al. (2001). Polar lipids were determined according to Tindall (1990). The DNA G+C content was determined by using an HPLC method (Mesbah & Whitman, 1989).
The yellow pigments of strain TDMA-16T were identified as carotenoids, including zeaxanthin [UV-vis 
max 451 and 476 nm; molecular mass (M++1), 569], nostoxanthin [UV-vis max 449 and 475 nm; molecular mass (M++1), 601] and an unidentified polar carotenoid. Nostoxanthin is also found in Sphingomonas paucimobilis and Sphingomonas echinoides (Jenkins et al., 1979; Rowe et al., 2000). The quinone system of strain TDMA-16T consisted mainly of ubiquinone Q-10. This quinone profile is a characteristic of the majority of species within the class Alphaproteobacteria (Collins & Jones, 1981), including the genus Sphingomonas sensu stricto (Busse et al., 1999; Takeuchi et al., 2001). The polar lipid profile of strain TDMA-16T was characterized by the presence of phosphatidylethanolamine, phosphatidylglycerol, diphosphatidylglycerol, sphingoglycolipid and an unidentified glycolipid as the predominant lipids and moderate amounts of two unidentified glycolipids. Additionally, strain TDMA-16T contained minor amounts of various unidentified lipids, including an aminophospholipid and two glycolipids. Phosphatidylmonomethylethanolamine and phosphatidyldimethylethanolamine were not detected in strain TDMA-16T. The polar lipid profile of strain TDMA-16T was distinguishable from that of Sphingomonas mali, Sphingomonas pruni and Sphingomonas asaccharolytica in that phosphatidylmonomethylethanolamine and phosphatidyldimethylethanolamine were absent (Busse et al., 1999; Kämpfer et al., 1997). The major fatty acids were C17 : 16c (34.5 %) and C18 : 17c (29.3 %). Table 2 shows the detailed fatty acid composition of strain TDMA-16T. This profile is in excellent agreement with those of representatives of the genus (Table 2) (Busse et al., 1999, 2005, 2003; Yang et al., 2006) and consistent with the assignment of strain TDMA-16T to the genus Sphingomonas sensu stricto. The presence of 2-hydroxy fatty acids and the lack of 3-hydroxy fatty acids are important characteristics of members of the family Sphingomonadaceae (Busse et al., 1999; Takeuchi & Hiraishi, 2001; Takeuchi et al., 2001). However, strain TDMA-16T differed from members of the genus Sphingomonas sensu stricto both qualitatively and quantitatively with regard to certain fatty acids and by the presence of 2-OH C18 : 1 as the major hydroxy fatty acid (Table 2).
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), which is in agreement with the values of 62–68 mol% given for the genus (Takeuchi et al., 2001). The results of the analysis of the 16S rRNA gene sequence, quinone system, fatty acids, polar lipids and DNA G+C content thus proved that strain TDMA-16T is a member of the genus Sphingomonas sensu stricto. The strain can be distinguished from its close relatives by its 16S rRNA gene sequence, fatty acid composition and numerous physiological characteristics. On the basis of these results, it is concluded that strain TDMA-16T represents a novel carotenoid-producing species of the genus Sphingomonas sensu stricto, for which the name Sphingomonas jaspsi sp. nov. is proposed.
Description of Sphingomonas jaspsi sp. nov.
Sphingomonas jaspsi [ja.sp'.si. N.L. n. jaspsum arbitrary name derived from the acronym JSPS (Japan Society for the Promotion of Science); N.L. gen. n. jaspsi of JSPS, the organization that supported this study].
Cells are Gram-negative-staining pleomorphic short rods that are strictly aerobic, motile and non-spore-forming. Cells are 0.4–0.5 µm in width and 0.7–1.0 µm in length. Budding morphology may be observed. On NA, forms yellow, circular, dry colonies (1–2 mm in diameter) within 48 h. Carotenoids such as zeaxanthin and nostoxanthin are produced. Grows at 20.0–40.0 °C (optimum, 35.0–37.0 °C) and pH 6.0–9.0 (optimum, pH 6.0–7.0). Optimal growth occurs in the absence of NaCl; growth is inhibited by the presence of >0.25 % (w/v) NaCl. Anaerobic growth does not occur. Tween 80, gelatin and starch are hydrolysed, whereas aesculin, agar, DNA, casein, cellulose and chitin are not. Negative reactions are observed for glucose fermentation and acid production from all tested sugars. Indole and H2S are not produced. Nitrate is not reduced. Catalase- and oxidase-positive. -Galactosidase-positive. Negative for tryptophan deaminase, lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase and urease activities. Glucose and maltose are assimilated, but arabinose, mannose, mannitol, N-acetylglucosamine, gluconate, capric acid, adipic acid, malate, trisodium citrate and phenylacetic acid are not. The major fatty acids are C17 : 16c (34.5 %), C18 : 17c (29.3 %) and summed feature 4 (containing C16 : 17c and/or 2-OH iso-C15 : 0) (8.1 %). The major hydroxy fatty acid is 2-OH C18 : 1 (6.1 %). The predominant ubiquinone is Q-10. Glycosphingolipids are present.
The type strain is TDMA-16T (=NBRC 102120T=DSM 18422T=CCUG 53607T), which was isolated from a freshwater sample collected at Misasa (Tottori, Japan). The DNA G+C content of the type strain is 63.3 mol%.
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ACKNOWLEDGEMENTS |
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