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Int J Syst Evol Microbiol 57 (2007), 321-325; DOI  10.1099/ijs.0.64716-0
© 2007 International Union of Microbiological Societies

Pontibacter akesuensis sp. nov., isolated from a desert soil in China

Yu Zhou1,{dagger}, Xu Wang1,{dagger}, Huan Liu1, Ke-Yun Zhang1, Yu-Qin Zhang3,4, Ren Lai1,2 and Wen-Jun Li3

1 Key Laboratory of Microbiological Engineering of Agricultural Environment, Ministry of Agriculture, Life Sciences College of Nanjing Agricultural University, Nanjing, Jiangsu 210095, People's Republic of China
2 Biotoxin Department of Key Laboratory of Animal Models and Human Disease Mechanisms, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming Yunnan 650223, People's Republic of China
3 Laboratory for Conservation and Utilization of Bio-Resources, Yunnan Institute of Microbiology and Yunnan University, Kunming, Yunnan 650091, People's Republic of China
4 Institute of Medicinal Biotechnology, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing 100050, People's Republic of China

Correspondence
Ren Lai
rlai72{at}njau.edu.cn
Wen-Jun Li
wjli{at}ynu.edu.cn


   ABSTRACT
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A Gram-negative, non-motile, rod-shaped bacterium, designated strain AKS 1T, was isolated from a desert soil sample collected from Akesu, XinJiang Province, China. A taxonomic study, including phylogenetic analysis based on 16S rRNA gene sequences and phenotypic characteristics, was performed on the novel isolate. The predominant menaquinone of strain AKS 1T was MK-7. The major fatty acids included i-C15 : 0, ai-C17 : 1 B/i-C17 : 1 I and i-C17 : 0 3-OH. The G+C content of the DNA was 51.4 mol%. Based on the results of phenotypic and genotypic characteristics, strain AKS 1T should be assigned as representing a novel species of the genus Pontibacter, for which the name Pontibacter akesuensis is proposed. The type strain is AKS 1T (=KCTC 12758T=CCTCC AB 206086T).

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain AKS 1T is DQ672723.

{dagger}These authors contributed equally to this work. Back


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The genus Pontibacter belongs to the phylum Bacteroidetes and was first described by Nedashkovskaya et al. (2005b)Go based on a single isolate from an unidentified sea anemone. The main characteristics of members of the phylum Bacteroidetes include the ability to move by gliding (many lack motility), a rod-shaped or ring-shaped morphology, possession of Gram-negative cell walls and pigmentation. The majority of the members of the phylum Bacteroidetes have been isolated from seawater, sediment or algae. Some marine bacteria of the phylum Bacteroidetes possess menaquinone 7 (MK-7) as their main respiratory quinone (Bowman et al., 2003Go; Brettar et al., 2004aGo, bGo; Nedashkovskaya et al., 2003Go, 2004Go, 2005aGo, bGo; Raj & Maloy, 1990Go; Van Trappen et al., 2004Go; Yi & Chun, 2004Go; Yoon et al., 2004Go, 2005aGo, bGo, cGo). The present investigation was designed to establish the taxonomic position of a novel isolate that formed a common clade with the genus Pontibacter within the phylum Bacteroidetes. Although the novel isolate has some properties characteristic of the phylum Bacteroidetes, it also has many special properties that are distinct from other members of the phylum. Genotypic and phenotypic data show that the strain represents a novel species of the genus Pontibacter.

Strain AKS 1T was isolated from a desert soil sample collected from Akesu, XinJiang Province, north-west China, by using the traditional dilution plating method. LB agar (Sambrook & Russell, 2002Go) was used for selective isolation and cultures were incubated at 30 °C for 1 week. The novel strain was maintained on LB agar slants at 4 °C and as glycerol suspensions (20 %, v/v) at –80 °C. Biomass for molecular systematic and chemotaxonomic studies was obtained after incubation in LB at 30 °C for 2 days in shake flasks (about 150 r.p.m.), with the pH adjusted to pH 7.8 using NaOH.

Cell morphology of the novel isolate was observed by light microscopy (BH2; Olympus) and by transmission electron microscopy (H-7650; Hitachi) after 24 h growth on LB medium. Acid production from carbohydrates was tested using the media and methods described by Gordon et al. (1974)Go. Sole carbon and sole carbon/nitrogen source utilization was investigated using the Biolog GN2 Microplate system (Nedashkovskaya et al., 2005bGo) according to the manufacturers' instructions. Growth was tested at 4, 10, 27, 30, 36, 37, 40 and 45 °C on LB medium. Requirement for and tolerance of NaCl (1, 4, 7, and 10 %) and pH (3.0, 6.0, 7.0, 7.8, 8.0, 10.0, 11.0, 12.0) were tested using modified LB medium. Susceptibility to antibiotics was examined as described by Nedashkovskaya et al. (2003Go, 2005b)Go with results recorded after incubation at 30 °C for up to 3 days. Gram-staining and other phenotypic characteristics were determined according to the method described by Gerhardt et al. (1994)Go.

Menaquinones were extracted from lyophilized cells and determined using the procedures reported by Akagawa-Matsushita et al. (1992)Go and Hu et al. (2001)Go. Biomass for the quantitative fatty acid analysis was prepared by collecting growth from shake flasks of LB medium that had been incubated for 2 days at 30 °C. Fatty acids were extracted, methylated and analysed using the standard MIDI (Microbial Identification) system as described by Sasser (1990)Go.

For the determination of G+C composition, genomic DNA was prepared according to the method of Marmur (1961)Go. The DNA G+C content of strain AKS 1T was determined using the thermal denaturation method (Mandel & Marmur, 1968Go).

PCR amplification of the 16S rRNA gene was performed as described by Xu et al. (2003)Go. Phylogenetic analysis was performed using the PHYLIP (Felsenstein, 1993Go) and MEGA version 3.1 (Kumar et al., 2001Go) software packages after multiple alignment of data by using CLUSTAL_X (Thompson et al., 1997Go). Distances (distance options according to the Kimura two-parameter model; Kimura, 1980Go, 1983Go) and clustering were based on the neighbour-joining (Saitou & Nei, 1987Go) and maximum-likelihood (Felsenstein, 1981Go) methods. Bootstrap analysis was used to evaluate the tree topology of the neighbour-joining data by performing 1500 resamplings (Felsenstein, 1985Go).

Cells of strain AKS 1T were collected for morphological observations after being cultured on LB agar for 24 h. Cells were prepared for transmission electron microscopy as described by Nedashkovskaya et al. (2005b)Go. Cells of strain AKS 1T ranged from 0.7 to 0.75 µm in width and from 1.5 to 1.6 µm in length and an unknown ropy substance was observed around the cells (Fig. 1Go).


Figure 1
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  		Fig. 1. Transmission electron micrographs of cells of strain AKS 1T grown on LB agar medium for 2 days at 30 °C. Bars, 500 nm (a, d) and 1 µm (b, c).

 
Colonies of strain AKS 1T were circular, convex, shiny, smooth and pink-coloured with diameters of 1–2 mm on LB agar for 48 h. Colonies of strain AKS 1T were ropy and wet. Other physiological and biochemical characteristics are given in Table 1Go and in the species description.


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  		Table 1. Phenotypic characteristics that differentiate strain AKS 1T from Pontibacter actiniarum KMM 6156T

Both strains have a similar colony colour (pink) and give a positive result in tests for beta-galactosidase activity. Both strains are able to hydrolyse aesculin and trypsin, but not Tweens 40 or 80. +, Positive; –, negative. Data are from Nedashkovskaya et al. (2005bGo) and this study.

 
The predominant menaquinone was MK-7. The major fatty acids of strain AKS 1T were i-C15 : 0, ai-C17 : 1 B/i-C17 : 1 I and i-C17 : 0 3-OH; detailed fatty acid profiles are shown in Table 2Go. The G+C content of the DNA was 51.4 mol%.


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  		Table 2. Cellular fatty acid content (%) of strain AKS 1T and its closest relative, Pontibacter actiniarum KMM 6156T

Summed fatty acids are those could not be separated by the Microbial Identification System. Data are from Nedashkovskaya et al. (2005b)Go and this study. Values are percentages of total fatty acids and values of <1 % are not shown.

 
The almost complete 16S rRNA gene sequence (1408 bp) of strain AKS 1T was determined and was used to construct a phylogenetic tree with reference sequences selected from the GenBank database following BLAST searches (unidentified and unpublished sequences were not considered). Phylogenetic analyses revealed that strain AKS 1T belongs to the phylum Bacteroidetes and is most closely related to the type strain of the only recognized species of the genus Pontibacter, Pontibacter actiniarum KMM 6156T (Fig. 2Go). The two strains formed a common group supported by a high bootstrap value (100 %).


Figure 2
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  		Fig. 2. Neighbour-joining phylogenetic tree based on the 16S rRNA gene sequences of strain AKS 1T and representative members of the phylum Bacteroidetes. Numbers at nodes indicate bootstrap values (%). Bar, 0.02 substitutions per nucleotide position.

 
Although P. actiniarum KMM 6156T and strain AKS 1T shared up to 95 % 16S rRNA gene sequence similarity and had similar menaquinone fingerprints (MK-7), they could be differentiated by their habitats and physiological and biochemical characteristics (Table 1Go). Strain AKS 1T was isolated from a desert soil, but P. actiniarum KMM 6156T was isolated from a marine habitat. Biolog GN2 tests indicated that about 70 different compounds could be utilized as sole carbon or sole carbon/nitrogen sources by strain AKS 1T, while P. actiniarum KMM 6156T could only use 20 different compounds. Strain AKS 1T was resistant to kanamycin and sensitive to neomycin and gentamicin, but strain KMM 6156T was sensitive to kanamycin and resistant to neomycin and gentamicin. The features that differentiate strain AKS 1T from its nearest phylogenetic neighbour, P. actiniarum KMM 6156T, are shown in Table 1Go.

In conclusion, genotypic, chemotaxonomic and phenotypic data demonstrate that strain AKS 1T represents a novel species of the genus Pontibacter, for which we propose the name Pontibacter akesuensis sp. nov.

Description of Pontibacter akesuensis sp. nov.
Pontibacter akesuensis (a.ke.su.en'sis. N.L. masc. adj. akesuensis pertaining to Akesu, a city of XinJiang Province in the north-west of China from where the type strain was isolated).

Cells range from 0.7 to 0.75 µm in width and from 1.5 to 1.6 µm in length. Colonies are circular, 1–2 mm in diameter, convex, shiny, pink and smooth on nutrient agar plates. Gram-negative. Cells are non-motile, non-spore-forming, aerobic and chemoorganotrophic. A ropy substance is observed around cells. Grows well in very dry environmental conditions, does not require Na+ or other special substances for growth. Growth occurs at between 4 and 36 °C, with an optimum at 28–30 °C. Growth occurs at pH 7–11, with optimal growth at pH 7.6–8.0. Growth occurs at 0–4 % NaCl. Pigment can be extracted with organic solvents. Gelatin, DNA and starch are decomposed, but casein, Tweens 20, 40 and 80, cellulose and chitin are not hydrolysed. Forms acid from aesculin, D-fructose, D-sucrose, inositol, L-raffinose, D-maltose, N-acetylglucosamine, L-fucose and D-glucose, but not from D-cellobiose, D-galactose, D-lactose, D-melibiose, L-rhamnose, L-sorbose or DL-xylose. In Biolog GN tests, the type strain utilizes {alpha}-cyclodextrin, dextrin, glycogen, N-acetyl-D-galactosamine, L-arabinose, D-arabitol, N-acetyl-D-glucosamine, D-cellobiose, D-fructose, L-fucose, L-alanine, D-galactose, gentiobiose, {alpha}-D-glucose, myo-inositol, maltose, D-mannitol, D-melibiose, methyl beta-D-glucoside, D-psicose, D-raffinose, L-rhamnose, D-sorbitol, sucrose, D-trehalose, turanose, lactulose, xylitol, methyl pyruvate, monomethyl succinate, acetic acid, D-galactonic acid lactone, cis-aconitic acid, D-galacturonic acid, D-gluconic acid, D-glucuronic acid, D-glucosaminic acid, {alpha}-hydroxybutyric acid, beta-hydroxybutyric acid, {gamma}-hydroxybutyric acid, itaconic acid, {alpha}-ketobutyric acid, {alpha}-ketoglutaric acid, {alpha}-ketovaleric acid, DL-lactic acid, propionic acid, quinic acid, D-saccharic acid, succinic acid, bromosuccinic acid, succinamic acid, L-alaninamide, L-alanyl glycine, L-asparagine, L-aspartic acid, L-glutamic acid, glycyl L-aspartic acid, glycyl L-glutamic acid, L-histidine, hydroxy-L-proline, L-leucine, L-ornithine, L-phenylalanine, L-proline, L-pyroglutamic acid, L-serine, L-threonine, DL-carnitine, {gamma}-aminobutyric acid, inosine, thymidine, putrescine, 2,3-butanediol and glucose 6-phosphate. However, it does not utilize Tweens 20, 40, or 80, adonitol, i-erythritol, uridine, urocanic acid, {alpha}-D-lactose, D-mannose, citric acid, formic acid, p-hydroxyphenylacetic acid, malonic acid, sebacic acid, glucuronamide, D-alanine, D-serine, phenylethylamine, 2-aminoethanol, DL-{alpha}-glycerol phosphate or glucose 1-phosphate. Nitrate is not reduced. Indole and H2S (triple sugar iron reaction) are negative. Susceptible to the following antibiotics: ampicillin, benzylpenicillin, chloramphenicol, neomycin, gentamicin, erythromycin, carbenicillin, lincomycin and tetracycline. Resistant to kanamycin, polymyxin B and streptomycin. The predominant menaquinone is MK-7. The fatty acid profile contains i-C15 : 0 (25.08 %), ai-C17 : 1 B/i-C17 : 1 I (19.97 %), i-C17 : 0 3-OH (11.46 %), i-C17 : 1{omega}9c (7.69 %), i-C17 : 0 (6.06 %), i-C15 : 0 3-OH (3.33 %), C17 : 1{omega}6c (2.87 %), i-C15 : 1 F (1.97 %), i-C15 : 0 2-OH/C16 : 1{omega}7c/C16 : 1{omega}7t (1.94 %), C15 : 0 (1.77 %), i-C15 : 1 I/C13 : 0 3-OH (1.72 %), C18 : 0 (1.71 %), C16 : 0 (1.68 %), and i-C16 : 0 (1.46 %). The DNA G+C content is 51.4 mol%.

The type strain, AKS 1T (=KCTC 12758T=CCTCC AB 206086T), was isolated from the surface layer of a desert soil from Akesu, XinJiang Province, China.


   ACKNOWLEDGEMENTS
 
This work was supported by grants from National Natural Science Foundation of China (Project no. 30600001), Jiangsu Natural Science Foundation (BK2005422) and Yunnan Science and Technology Commission (2005C0054M). W.-J. L. was also supported by the Program for New Century Excellent Talent in University (NCET).


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