Mucilaginibacter Soli Sp. Nov., Isolated from Arctic Tundra Soil

International Journal of Systematic and Evolutionary Microbiology (2012), 62, 1630–1635 DOI 10.1099/ijs.0.033902-0

Mucilaginibacter soli sp. nov., isolated from Arctic tundra soil

Fan Jiang, Jun Dai, Yang Wang, Xiuqing Xue, Mengbo Xu, Youhao Guo, Wenxin Li, Chengxiang Fang and Fang Peng

Correspondence China Center for Type Culture Collection (CCTCC), College of Life Sciences, Wuhan University, Fang Peng Wuhan 430072, PR China [email protected]

A novel pale-pink-coloured strain, designated R9-65T, was isolated from a tundra soil near Ny-A˚ lesund, Svalbard Archipelago, Norway (786 N). The cells were facultatively anaerobic, Gram-staining-negative, non-motile and rod-shaped. Growth occurred at 4–32 6C (optimum, 25–28 6C), at pH 5.0–9.0 (optimum, pH 6.0–7.0) and with 0–1.0 % (w/v) NaCl (optimum, no NaCl). Flexirubin-type pigments were absent. Phylogenetic analysis based on 16S rRNA gene sequences indicated that strain R9-65T belonged to the genus Mucilaginibacter in the family Sphingobacteriaceae. The 16S rRNA gene sequence similarity between strain R9-65T and type strains of related species ranged from 93.4 to 96.6 %. Strain R9-65T contained summed

feature 3 (C16 : 1v7c and/or C16 : 1v6c, 34.3 %) and iso-C15 : 0 (20.3 %) as major cellular fatty acids, MK-7 as the major respiratory quinone, and phosphatidylethanolamine as the main polar lipid. The DNA G+C content of strain R9-65T was 47.2 mol%. On the basis of phylogenetic, physiological and chemotaxonomic data, strain R9-65T is considered to represent a novel species of the genus Mucilaginibacter, for which the name Mucilaginibacter soli sp. nov. is proposed. The type strain is R9-65T (5CCTCC AB 2010331T5NRRL B-59458T).

The genus Mucilaginibacter, belonging to the family (Kim et al., 2012). In this study, an Arctic bacterial isolate Sphingobacteriaceae within the phylum Bacteroidetes, was subjected to a polyphasic analysis and identified as a was first described by Pankratov et al. (2007) and its novel member of the genus Mucilaginibacter. description was subsequently emended by Urai et al. (2008) A bacterial strain, designated R9-65T, was isolated from a and Baik et al. (2010). Members of the genus contain soil sample collected from a high Arctic tundra near menaquinone-7 (MK-7) as the major respiratory quinone, the settlement Ny-A˚ lesund (78u 559 N11u 589 E) in the possess straight- and branched-saturated fatty acids as the Svalbard Archipelago, Norway. Isolation was carried out major cellular fatty acids, and have DNA G+C contents in using the standard dilution plating method on 0.36R2A the range 42.4–47.0 mol% (Pankratov et al., 2007; Urai agar (BD) at 25 uC. The isolate produced slime, indicative et al., 2008; Baik et al., 2010). At the time of writing, the of extracellular polysaccharide, around the colonies when genus Mucilaginibacter contained 16 recognized species grown on 0.36R2A agar at 25 uC for 4 days. The novel isolated from various environments such as peat bog, soil, strain was routinely cultured on 0.36R2A agar and stored rice straw, rice paddy, freshwater, the rhizosphere and by lyophilization. decaying lichen, namely M. paludis (the type species) and M. gracilis (Pankratov et al., 2007), M. kameinonensis (Urai Sequencing of the 16S rRNA gene of strain R9-65T was et al., 2008), M. daejeonensis (An et al., 2009), M. ximonen- carried out as described by Lane (1991). An almost- sis (Luo et al., 2009), M. oryzae (Jeon et al., 2009), M. rigui complete 16S rRNA gene sequence (1426 bp) was obtained (Baik et al., 2010), M. gossypii and M. gossypiicola and subjected to comparative analysis. Sequence similarity (Madhaiyan et al., 2010), M. frigoritolerans, M. lappiensis was investigated using NCBI BLAST and pairwise alignment and M. mallensis (Ma¨nnisto¨ et al., 2010), M. dorajii (Kim was calculated using the EzTaxon database (Chun et al., et al., 2010), M. myungsuensis (Joung & Joh, 2011), 2007). Sequences were aligned using CLUSTAL_X software M. boryungensis (Kang et al., 2011) and M. angelicae (Thompson et al., 1997), and phylogenetic trees were constructed by the neighbour-joining (Saitou & Nei, 1987), Abbreviation: PE, phosphatidylethanolamine. maximum-parsimony (Fitch, 1971) and maximum-like- The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene lihood (Felsenstein, 1981) tree-making algorithms using T sequence of strain R9-65 is JF701183. the MEGA version 4.0 (Tamura et al., 2007) and PHYLIP Four supplementary figures are available with the online version of this version 3.6 (Felsenstein, 2005) software packages. Evolu- paper. tionary distances for the neighbour-joining algorithm were

1630 033902 G 2012 IUMS Printed in Great Britain Mucilaginibacter soli sp. nov. calculated with the Kimura two-parameter model (Kimura, 2 weeks at 25 uC. Cell morphology was examined by 1980) and close-neighbour-interchange (search level52, phase-contrast (BX51; Olympus) and transmission electron random additions5100) was applied in the maximum- (8100; Hitachi) microscopy using cells grown for 2 days at parsimony analysis. In each case, bootstrap values were 25 uC on R2A agar. Gliding motility was investigated calculated based on 1000 replications (Felsenstein, 1985). as described by Bowman (2000). Cell life-cycle was examined using cultures grown on R2A agar for up to Phylogenetic analysis based on 16S rRNA gene sequence 2 weeks. Growth under anaerobic conditions was tested on revealed that strain R9-65T was affiliated to the genus 0.36R2A agar in a GasPak (BBL) jar at 25 uC for 7 days. Mucilaginibacter in the family Sphingobacteriaceae, and Oxidase activity was evaluated via the oxidation of 1 % (w/ formed a robust clade with M. rigui WPCB133T in the v) tetramethyl-p-phenylenediamine. Catalase activity was neighbour-joining tree (Fig. 1). The same relationship was determined by measurement of bubble production after the also found in trees constructed using the maximum- application of 3 % (v/v) hydrogen peroxide solution. The likelihood (Fig. S1, available in IJSEM Online) and presence of flexirubin-type pigments was tested using the maximum-parsimony algorithms (Fig. S2). Levels of 16S KOH test as described by Bernardet et al. (2002). For rRNA gene sequence similarity between strain R9-65T pectin hydrolysis activity, the isolate was cultured on a and the type strains of recognized species of the genus 0.36R2A agar plate containing 0.3 % (w/v) citric pectin, Mucilaginibacter (93.4–96.6 %) were below the 97.0 % followed by staining with a solution of 1 % n-hexadecyl- threshold recommended for the discrimination of separate trimethylammonium bromide. Hydrolysis of chitin, CM- bacterial species (Stackebrandt & Goebel, 1994). Based on cellulose, alginate, casein, starch, tyrosine and xylan was data from phylogenetic analysis, strain R9-65T could not be investigated on 0.36R2A agar after 1 week of incubation assigned to any recognized species and thus represents a according to Smibert & Krieg (1994). The hydrolysis of novel species within the genus Mucilaginibacter. Tween 20, 40, 60 and 80 was measured using the formation Growth was evaluated at 25 uC on several standard of an opaque halo of precipitation around the colony bacteriological media (all from BD): R2A agar, 0.36R2A (Barrow & Feltham, 1993). Acid production from sugars agar , 0.36marine broth 2216 (MB) agar, tryptic soy broth was examined by using phenol red broth base containing (TSB) agar, nutrient agar (NA) and MacConkey agar. 1 % of each sugar. Antibiotic sensitivity was tested by using Gram-staining of cells was carried out according to the filter-paper discs (diameter, 6.35 mm) impregnated with the classical Gram-stain procedure described by Doetsch following antibiotics (concentration per disc): ampicillin (1981). Growth at different temperatures (0, 4, 8, 18, 20, (10 mg), aztreonam (30 mg), ceftriaxone (30 mg), cefepime 25, 28, 30, 32, 37 and 42 uC) was investigated on R2A (30 mg), ceftazidime (30 mg), streptomycin (10 mg), kana- agar for up to 2 weeks. The pH range for growth was mycin (30 mg), piperacillin (100 mg), gentamicin (10 mg), determined in 0.36MB at pH 4.0–11.0 (in increments of oxacillin (1 mg), penicillin G (10 mg), erythromycin (15 mg), 1.0 pH unit). Salt tolerance was tested on 0.36R2A agar vancomycin (30 mg), clindamycin (2 mg), chloramphenicol supplemented with 0, 0.5, 1, 2, 3, 4 and 5 % NaCl (w/v) for (30 mg), amikacin (30 mg), tetracycline (30 mg), ciprofloxacin

Fig. 1. Neighbour-joining tree based on 16S rRNA gene sequences, showing the relationship of strain R9-65T and related taxa. Percentage bootstrap values (1000 replications) .70 % are shown at nodes. The sequence of Flexibacter flexilis NBRC 15060T was used as an outgroup. Bar, 0.02 substitutions per nucleotide position. http://ijs.sgmjournals.org 1631 F. Jiang and others

Table 1. Differential characteristics of strain R9-65T and related species of the genus Mucilaginibacter

Strains: 1, R9-65T;2,M. rigui NBRC 101115T;3,M. paludis DSM 18603T;4,M. lappiensis LMG 25358T;5,M. dorajii KACC 14556T. Data were obtained in this study unless otherwise indicated. +, Positive; (+), weakly positive; 2, negative. In API ZYM tests, all strains were positive for alkaline phosphatase, esterase (C4), esterase lipase (C8), leucine arylamidase, valine arylamidase, acid phosphatase, naphthol-AS-BI- phosphohydrolase, a-glucosidase and N-acetyl-b-glucosaminidase, and were negative for lipase (C14), a-chymotrypsin and b-glucuronidase. In API 50CH tests, all strains produced acid from aesculin, D-galactose, D-fructose, D-mannose, maltose and sucrose, but not from erythritol, D-ribose, L- xylose, D-adonitol, methyl b-D-xylopyranoside, L-sorbose, L-rhamnose, dulcitol, inositol, D-mannitol, D-sorbitol, melezitose, xylitol, gentiobiose, D-tagatose, D-fucose, D-arabitol, L-arabitol, potassium gluconate, potassium 2-ketogluconate or potassium 5-ketogluconate.

Characteristic 12345

Anaerobic growth + 2 + 22 Flexirubin pigments 2222+ Catalase 2 ++++ Enzyme activities: Cystine arylamidase (+) 22++ Trypsin 222++ a-Galactosidase 2 ++++ b-Glucosidase 2 + 2 ++ a-Mannosidase + 22++ a-Fucosidase 222++ Acid production from: Glycerol 22+ 22 D-Arabinose 2 + 2 ++ L-Arabinose 22+++ D-Xylose 2 ++++ Methyl a-D-mannopyranoside 2 + 22+ Methyl a-D-glucopyranoside 2 + 22+ Amygdalin 2 + 2 ++ Arbutin 2 + 222 Salicin 2 + 2 ++ Cellobiose 2 + 2 ++ Lactose 22+++ Melibiose 2 ++2 + Trehalose 2 ++2 + Inulin 2222+ Raffinose + 2 + 22 Starch + 2 + 2 + Glycogen + 222+ Turanose 22+ 22 D-Lyxose 2 + 2 + 2 L-Fucose 22++2 Quinone(s) MK-7, MK-6 MK-7* MK-7, MK-6D MK-7, MK-6d MK-7§ DNA G+C content (mol%) 47.2 47.0* 46.1D 43.5d 42.6§

*Data from Baik et al. (2010). DData from Pankratov et al. (2007). dData from Ma¨nnisto¨ et al. (2010). §Data from Kim et al. (2010).

(5 mg), polymyxin B (30 mg) and nitrofurantoin (300 mg). Strain R9-65T grew well at 25 uC on R2A agar, 0.36R2A Any sign of growth inhibition was scored as sensitivity agar, 0.36MB agar and NA, but not on TSB agar or to that antibiotic. Resistance to an antimicrobial drug MacConkey agar. Cells were Gram-staining-negative, facul- was indicated if no inhibition zone was observed. tatively anaerobic, non-motile, non-spore-forming and Additional physiological and biochemical characteristics rod-shaped (0.5–0.761.0–2.0 mm) (Fig. S3). Colonies were were determined by using the API 20E, API 20NE, API pale pink, circular, convex and smooth after growth for 50CH and API ZYM kits (bioMe´rieux) and the GN2 5 days at 25 uC on 0.36R2A agar. Growth occurred at 4– MicroPlate (Biolog) according to the manufacturers’ 32 uC (optimum, 25–28 uC) and at pH 5.0–9.0 (optimum, instructions. pH 6.0–7.0). The range of NaCl for growth was 0–1.0 %

1632 International Journal of Systematic and Evolutionary Microbiology 62 Mucilaginibacter soli sp. nov.

(w/v); optimum growth occurred without NaCl. Other Table 2. Cellular fatty acid composition of strain R9-65T and physiological characteristics of strain R9-65T are summar- type strains of phylogenetically related species ized in the species description. Selected characteristics that T T T Strains: 1, R9-65 ;2,M. rigui NBRC 101115 ;3,M. paludis DSM differentiate strain R9-65 from related species of the genus T T T Mucilaginibacter are shown in Table 1. 18603 ;4,M. lappiensis LMG 25358 ;5,M. dorajii KACC 14556 . All data were obtained in this study. All strains were cultivated on R2A agar The DNA G+C content of strain R9-65T was determined plates at 25 uC, and cells from late-exponential phase growth were used. by HPLC (UltiMate 3000; Dionex) according to the Values are percentages of the total fatty acids. Summed feature 3 method of Mesbah et al. (1989). Respiratory quinones contains C16 : 1v7c and/or C16 : 1v6c; 2, not detected or ,1%. were extracted and identified by HPLC as described by Xie & Yokota (2003). For analysis of cellular fatty acids, strain Fatty acid 1 2 3 4 5 R9-65T and four related strains, M. rigui NBRC 101115T, C 1.0 1.3 1.6 2 1.2 M. paludis DSM 18603T, M. lappiensis LMG 25358T and M. 14 : 0 iso-C 3-OH 2 1.0 222 dorajii KACC 14556T were grown on R2A agar plates at 13 : 0 iso-C15 : 0 20.3 22.2 21.5 23.8 15.7 25 uC, and cells from late-exponential phase growth were anteiso-C15 : 0 2212.5 2 1.0 used in this study. Harvesting, saponification, methylation C16 : 1v5c 7.2 3.7 8.3 5.8 5.4 and extraction of cellular fatty acids were performed C16 : 0 4.9 8.8 8.9 5.3 14.0 following the protocol of the Sherlock Microbial Identifica- iso-C15 : 0 3-OH 2.3 1.8 1.4 2.0 1.7 tion System (MIDI) version 6.0. Separation and identifica- iso-C17 : 0 2.5 2221.3 tion of fatty acid methyl esters was performed using a gas C17 : 1v8c 1.3 2222 chromatograph (6890N; Hewlett Packard) with MIDI C16 : 0 3-OH 2 1.2 2 2.3 2.8 Sherlock TSBA6 (version of the database) (Sasser, 1990). C18 : 0 223.5 1.3 2 T For sphingolipid and polar lipid analysis, strain R9-65 and iso-C17 : 0 3-OH 7.5 6.5 5.4 9.8 8.3 the four reference strains were grown on/in R2A agar iso-C17 : 1v9c 11.0 3.6 2 2.9 1.4 or broth, respectively, at 25 uC. The sphingolipids were Summed feature 3 34.3 41.7 26.7 40.8 43.5 extracted and analysed according to Kato et al. (1995), while the polar lipids were extracted and analysed by two- Cells are Gram-staining-negative, facultatively anaerobic, dimensional TLC (silica gel plates, layer thickness 0.2 mm, non-motile and non-spore-forming rods, approximately Merck) according to Tindall (1990). 0.5–0.7 mm wide and 1.0–2.0 mm long. No cyclic cell shape The DNA G+C content of strain R9-65T was 47.2 mol%. change is noticed during culture. Colonies are pale pink, Strain R9-65T contained MK-7 as the predominant isopre- circular, convex and smooth after growth for 5 days at noid quinone which represented 91.5 % of the total. In 25 uC on 0.36R2A agar. Growth occurs at 25 uC on R2A addition, small amounts of MK-6 (8.5 %) were detected. agar, 0.36R2A agar, 0.36MB agar and NA, but not on The quinone profile was in agreement with that expected TSB agar or MacConkey agar. Growth occurs at 4–32 uC for a member of the genus Mucilaginibacter. The major (optimum, 25–28 uC), at pH 5.0–9.0 (optimum, pH 6.0– cellular fatty acids of strain R9-65T were summed feature 3 7.0) and in the presence of 0–1.0 % (w/v) NaCl (optimum, (C16 : 1v7c and/or C16 : 1v6c) (34.3 %) and iso-C15 : 0 no NaCl). Oxidase-positive and catalase-negative. Flexirubin- (20.3 %). The fatty acid profile of strain R9-65T was type pigments are absent. Negative in tests for hydrolysis of similar to those of species of the genus Mucilaginibacter, pectin, chitin, CM-cellulose, alginate, casein, starch, tyrosine, but differed in the relative amounts of iso-C17 : 1v9c. xylan, Tweens 20, 40, 60 and 80. Acid is produced from Detailed fatty acid composition data are shown in Table 2. galactose, maltose, mannose, sucrose and glucose, but not The major polar lipid of strain R9-65T and the four from lactose, rhamnose or xylan. In the API ZYM test, there reference strains was phosphatidylethanolamine (PE), and are positive reactions for alkaline phosphatase, esterase (C4), several unknown polar lipids were also detected. In parti- esterase lipase (C8), leucine arylamidase, valine arylamidase, cular, the larger proportions of an unknown phospholipid acid phosphatase, naphthol-AS-BI-phosphohydrolase, a- (PL1) distinguished the novel isolate from the four glucosidase, N-acetyl-b-glucosaminidase and a-mannosidase; reference strains. All five strains contained sphingolipid, weakly positive reactions for cystine arylamidase; and the characteristic polar lipid of members of the family negative reactions for lipase (C14), trypsin, a-chymotrypsin, Sphingobacteriaceae (Fig. S4). a-galactosidase, b-glucuronidase, b-glucosidase and a-fucosidase. On API 20E and 20NE strips, there are positive results On the basis of the data presented, isolate R9-65T should be in tests for aesculin hydrolysis; b-galactosidase and gelatinase classified as a member of a novel species of the genus activities; utilization of citrate; and assimilation of glucose, Mucilaginibacter, for which the name Mucilaginibacter soli mannose, N-acetylglucosamine, potassium gluconate, malate sp. nov. is proposed. and trisodium citrate, but negative reactions for arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, Description of Mucilaginibacter soli sp. nov. urease and tryptophan deaminase activities; production of Mucilaginibacter soli (so9li. L. neut. gen. n. soli of soil, the H2S, indole and acetoin; nitrate reduction; oxidation of isolation source of the type strain). mannitol, inositol, sorbitol, rhamnose, sucrose, melibiose, http://ijs.sgmjournals.org 1633 F. Jiang and others amygdalin and arabinose; fermentation of glucose; and Facility Development Program from the Ministry of Science and Tech- assimilation of mannitol, capric acid, adipic acid and nology of the People’s Republic of China (grant no. 2005DKA21208), phenylacetic acid. In the API 50CH test, acid is produced and State Oceanic Administration, PR China (project no. 10/11YR06). from aesculin, D-galactose, D-fructose, D-mannose, maltose, sucrose, raffinose, starch and glycogen; but not from glycerol, References erythritol, D-arabinose, L-arabinose, D-ribose, D-xylose, L-xylose, D-adonitol, methyl b-D-xylopyranoside, L-sorbose, An, D.-S., Yin, C.-R., Lee, S.-T. & Cho, C.-H. (2009). Mucilaginibacter L-rhamnose, dulcitol, inositol, D-mannitol, D-sorbitol, methyl daejeonensis sp. nov., isolated from dried rice straw. Int J Syst Evol a-D-mannopyranoside, methyl a-D-glucopyranoside, amyg- Microbiol 59, 1122–1125. dalin, arbutin, salicin, cellobiose, lactose, melibiose, trehalose, Baik, K. S., Park, S. C., Kim, E. M., Lim, C. H. & Seong, C. N. (2010). inulin, melezitose, xylitol, gentiobiose, turanose, D-lyxose, Mucilaginibacter rigui sp. nov., isolated from wetland freshwater, and D-tagatose, D-fucose, L-fucose, D-arabitol, L-arabitol, pot- emended description of the genus Mucilaginibacter. Int J Syst Evol assium gluconate, potassium 2-ketogluconate or potassium Microbiol 60, 134–139. 5-ketogluconate. Positive result for the following Biolog GN2 Barrow, G. I. & Feltham, R. K. A. (editors) (1993). Cowan and Steel’s Manual for the Identification of Medical Bacteria, 3rd edn. Cambridge: MicroPlate substrates: D-galactose, sucrose, DL-lactic acid and Cambridge University Press. 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Description of Cellulophaga algicola sp. nov., trehalose, turanose, xylitol, pyruvic acid methyl ester, succinic isolated from the surfaces of Antarctic algae, and reclassification of acid monomethyl ester, acetic acid, cis-aconitic acid, citric Cytophaga uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as acid, formic acid, D-galactonic acid lactone, D-galacturonic Cellulophaga uliginosa comb. nov. Int J Syst Evol Microbiol 50, 1861– acid, D-gluconic acid, D-glucosaminic acid, D-glucuronic 1868. acid, a-, b-andc-hydroxybutyric acids, p-hydroxyphenyl- Chun, J., Lee, J.-H., Jung, Y., Kim, M., Kim, S., Kim, B. K. & Lim, Y. W. acetic acid, itaconic acid, a-ketobutyric acid, a-ketoglutaric (2007). EzTaxon: a web-based tool for the identification of acid, a-ketovaleric acid, malonic acid, propionic acid, quinic prokaryotes based on 16S ribosomal RNA gene sequences. 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Confidence limits on phylogenies: an approach amine, putrescine, 2-aminoethanol, 2,3-butanediol, glycerol, using the bootstrap. Evolution 39, 783–791. DL-a-glycerol phosphate, a-D-glucose 1-phosphate and a-D- Felsenstein, J. (2005). PHYLIP (Phylogeny Inference Package), Version glucose 6-phosphate. Sensitive to cefepime, streptomycin, 3.6. Distributed by the author, Department of Genome Sciences, kanamycin, piperacillin, gentamicin, penicillin G, vancomy- University of Washington, Seattle. cin, clindamycin, chloramphenicol, amikacin, tetracycline, Fitch, W. M. (1971). Toward defining the course of evolution: polymyxin B and nitrofurantoin, but resistant to ampicillin, minimum change for a specific tree topology. Syst Zool 20, 406–416. aztreonam, ceftriaxone, ceftazidime, oxacillin, erythromycin Jeon, Y., Lee, S.-S., Chung, B. S., Kim, J. M., Bae, J.-W., Park, S. K. & and ciprofloxacin. The predominant isoprenoid quinone is Jeon, C. O. (2009). Mucilaginibacter oryzae sp. nov., isolated from soil MK-7 and the major cellular fatty acids are summed feature 3 of a rice paddy. Int J Syst Evol Microbiol 59, 1451–1454. (C v7c and/or C v6c) and iso-C . The major polar 16 : 1 16 : 1 15 : 0 Joung, Y. & Joh, K. (2011). Mucilaginibacter myungsuensis sp. nov., lipid is PE; three unknown phospholipids and four polar isolated from mesotrophic artificial lake in Korea. Int J Syst Evol lipids are also detected. Sphingolipid is present. Microbiol 61, 1506–1510. The type strain, R9-65T (5CCTCC AB 2010331T5NRRL Kang, S. J., Jung, Y. T., Oh, K. H., Oh, T. K. & Yoon, J. H. (2011). B-59458T), was isolated from a tundra soil near Ny- Mucilaginibacter boryungensis sp. nov., isolated from soil. Int J Syst A˚ lesund, Svalbard Archipelago, Norway. The DNA G+C Evol Microbiol 61, 1549–1553. content of the type strain is 47.2 mol%. Kato, M., Muto, Y., Tanaka-Bandoh, K., Watanabe, K. & Ueno, K. (1995). Sphingolipid composition in Bacteroides species. Anaerobe 1, 135–139. Acknowledgements Kim, B. C., Lee, K. H., Kim, M. N., Lee, J. & Shin, K. S. (2010). This work was supported by the National Basic Research Program of Mucilaginibacter dorajii sp. nov., isolated from the rhizosphere of China (973 Program) (2011CB808800), the R & D Infrastructure and Platycodon grandiflorum. FEMS Microbiol Lett 309, 130–135.

1634 International Journal of Systematic and Evolutionary Microbiology 62 Mucilaginibacter soli sp. nov.

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