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Key Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, State Oceanic Administration, People's Republic of China
Correspondence
Zongze Shao
shaozz{at}163.com
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ABSTRACT |
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-Proteobacteria. Highest similarity values were found with Alcanivorax venustensis (95·2 %), Alcanivorax jadensis (94·6 %) and Alcanivorax borkumensis (94·1 %). Principal fatty acids of both strains were C16 : 0, C16 : 1
7c and C18 : 17c. The chemotaxonomically characteristic fatty acid C19 : 0 cyclo 8c was also detected. On the basis of the above, together with results of physiological and biochemical tests, DNA–DNA hybridization, comparisons of 16S–23S internal transcribed spacer sequences and comparisons of the partial deduced amino acid sequence of alkane hydroxylase, both strains were affiliated to the genus Alcanivorax but were differentiated from recognized Alcanivorax species. Therefore, a novel species, Alcanivorax dieselolei sp. nov., represented by strains B-5T and NO1A is proposed, with the type strain B-5T (=DSM 16502T=CGMCC 1.3690T).
The GenBank/EMBL/DDBJ accession numbers for the nucleotide sequences reported in this study are AY683537 (A. dieselolei B-5T, 16S rRNA gene), AY683538 (B-5T, large ITS), AY683539 (B-5T, small ITS), AY683540 (B-5T, partial alkB gene), AY683531 (A. dieselolei NO1A, 16S rRNA gene), AY683532 (NO1A, large ITS), AY683533 (NO1A, small ITS), AY683534 (NO1A, partial alkB gene), AY683536 (A. jadensis T9T, partial alkB gene) and AY683535 (A. venustensis ISO4T, partial alkB gene).
Transmission electron micrographs of cells of strains B-5T and NO1A and dendrograms showing the phylogenetic positions of the two strains plus recognized members of the genus Alcanivorax based on 16S rRNA, ITS and alkB gene sequences are available as supplementary figures in IJSEM Online, together with a table giving DNA–DNA relatedness values.
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-Proteobacteria that use aliphatic hydrocarbons as the sole source of carbon and energy (Yakimov et al., 1998
). A second species, Alcanivorax venustensis, was subsequently described and the misclassified species [Fundibacter] jadensis was assigned to Alcanivorax jadensis (Fernández-Martínez et al., 2003). Since 1998, the isolation of Alcanivorax species, or detection of their 16S rRNA gene sequences, from diverse habitats worldwide has been reported increasingly. Thus they are regarded as cosmopolitan bacteria. This group of marine bacteria exclusively uses petroleum oil hydrocarbons as sources of carbon and energy, and has been used for bioremediative interventions in polluted marine and coastal systems. In addition, Alcanivorax species have obvious potential to produce biocatalysts in non-polluting industrial processes and to act as a biosensor for in situ monitoring of aromatic or aliphatic compounds (Golyshin et al., 2003). Strain B-5T was isolated from oil-contaminated surface water of the Bohai Sea at the Yellow River dock of Shengli oilfield in November 2001; this dock had suffered a long period of crude oil pollution. A second strain, designated NO1A, was retrieved from a deep-sea sediment sample in the east Pacific Ocean. This was collected by a multi-core sampler from Pacific nodule region A station (7° 13' 46'' N, 153° 52' 19'' W, 5027 m water depth), a specific area with polymetallic nodules abundant on the sea bottom, during cruise DY105-11 of DAYANG Number 1 in 2001. The sediment samples were loaded into sterile Falcon tubes aboard ship and stored at –20 °C until use.
The artificial sea water medium (ASM) used for enrichment contained (per litre of distilled water) 10 g diesel fuel, 24 g NaCl, 7·0 g MgSO4.7H2O, 1 g NH4NO3, 0·7 g KCl, 2·0 g KH2PO4, 3·0 g Na2HPO4 and 10 ml trace element solution, pH 7·5. Trace element solution contained (per litre of distilled water) 2 mg CaCl2, 50 mg FeCl3.6H2O, 0·5 mg CuSO4, 0·5 mg MnCl2.4H2O and 10 mg ZnSO4.7H2O. Strains B-5T and NO1A were cultivated on HLB and SM1 media. HLB was modified from Luria–Bertani (LB) medium (Sambrook et al., 1989), with the concentration of NaCl increased to 30 g l–1. HLB was also used to check the presence of contaminants because both strains showed limited growth on this medium. SM1 (which was described by Yakimov et al., 1998) was used for routine cultivation of the isolates and most phenotypic tests, when supplemented with 10 g n-alkanes l–1 or 10 g sodium citrate l–1 as the sole carbon source. All cultures were incubated at 28 °C and spun at 200 r.p.m. unless noted otherwise.
General cell morphology was studied under an Olympus inverted microscope using 3-day-old cultures of the strains grown on HLB agar. For electron microscopy, exponential-phase cells were harvested, subsequently suspended and absorbed on a Formvar–carbon-coated grid, then stained with phosphotungstic acid. Cells of both strains were Gram-negative, rod-shaped with lophotrichous flagella, and varied from 0·8 to 2·0 µm in length and from 0·3 to 0·7 µm in width (see Supplementary Fig. A in IJSEM Online). The optimal growth temperature was determined over the temperature range 4–55 °C. Sodium requirement was examined at 0, 0·5, 1, 5, 7, 10, 15 and 20 % (w/v) NaCl. The following physiological and biochemical properties were examined according to standard methods: glucose fermentation, denitrification, catalase and oxidase activities, gelatin liquefaction and Tweenase, agarase, gelatinase, amylase and arginine dihydrolase activities. Results are given in the species description.
Tests for use of various organic substrates as sole carbon sources at a concentration of 0·1 % (w/v) were performed in 5 ml SM1 medium. The strains were characterized using Biolog GN plates as described by Ivanova et al. (1998). These results are also given in the species description. The chain length range of n-alkanes oxidized by strain B-5T was determined according to the method of Smits et al. (2002) except that rhamnolipids and dioctylphthalate were not used. Experiments were repeated at least three times. Tests of surface tension were performed after 7 days incubation on SM1 medium supplemented with n-alkanes using a Du Noüy ring tension meter (McInerney et al., 1990). To test the ability of strain B-5T to produce surface-active glucolipids, total lipid was extracted and fractionated using the method described by Yakimov et al. (1998). Glucolipids were further separated by TLC and analysed using electrospray ionization mass spectrometry (ESI-MS) and tandem mass spectrometry (MSMS). Both strains were able to utilize various n-alkanes as the sole carbon source, ranging in chain length at least from C5 to C36, which was wider than that of A. borkumensis (C6 to C20; van Beilen et al., 2004). Plentiful growth was observed with C8 to C28 n-alkanes, while growth on C5, C6 and C7 n-alkanes was weak, probably because of the high volatility of these compounds, such that they are only poorly available to cells, or because of their toxicity as cell membrane lipid solvents. For the long-chain n-alkanes, without adding any surfactants, both strains could grow slowly on C32 and C36, although they were barely soluble in water. In addition, when strain B-5T utilized C24 as the sole carbon source, the surface tension of the culture was reduced from 71·3 to 42·4 mN m–1 after 7 days cultivation. These results suggested that B-5T produced a biosurfactant. However, ESI-MS and MSMS failed to detect the presence of glucolipid-like compounds (data not shown), which were the typical products of A. borkumensis (Yakimov et al., 1998; Abraham et al., 1998).
Antibacterial activities were assessed as described by Kobayashi et al. (2003). Strain B-5T was sensitive to neomycin, kanamycin, amikacin and polymyxin B, but resistant to fortum, cefuroxime, cephradin, cefazolin, cefalexin, piperacillin, carbenicillin, ampicillin, oxacillin, penicillin, erythromycin, minomycin, vibramycin, tetracycline, gentamicin, cefobid, rocephin, vancomycin, ofloxacin, midecamycin, ciprofloxacin, norfloxacin, furazolidone, clindamycin, chloromycetin and co-trimoxazole. By contrast, strain NO1A was only sensitive to polymyxin B within the above antibiotics.
Cellular fatty acid analysis was carried out at the identification service laboratories of the DSMZ (Deutsche Sammlung von Mikroorganismen und Zellkulturen, Braunschweig, Germany). The fatty acid profiles of both strains are shown in Table 1. The three major components, fatty acids C16 : 0, C16 : 17c and C18 : 17c, found in both strains and recognized Alcanivorax species were also the principal fatty acids in members of the genera Comamonas, Delftia (Tamaoka et al., 1987) and Hydrogenophaga (Willems et al., 1989) as well as in species of the genera Alicycliphilus (Mechichi et al., 2003) and Oceanisphaera (Romanenko et al., 2003). No conclusions could thus be drawn from the major fatty acid profiles. The minor fatty acid profiles of the two strains were more similar to A. venustensis ISO4T than to A. borkumensis SK2T or A. jadensis T9T. Fatty acid C19 : 0 cyclo 8c, which was suggested as a characteristic chemotaxonomic marker of A. venustensis (Fernández-Martínez et al., 2003), was also detected in substantial amounts in strains B-5T and NO1A.
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. The G+C content of the DNA was determined by HPLC after digestion of the DNA with nuclease P1 (Tamaoka & Komagata, 1984; Mesbah & Whitman, 1989). The 16S rRNA gene was amplified by PCR using the following primers: 16SF (positions 8–27 of the Escherichia coli numbering; 5'-AGAGTTTGATCCTGGCTCAG-3') and 16SR (positions 1512–1493, 5'-ACGGCTACCTTGTTACGACT-3'). The 16S–23S internally transcribed spacer (ITS) regions of strains B-5T and NO1A were amplified with primers as described by García-Martínez et al. (1996, 1999). To amplify the partial fragment of the putative alkane hydroxylase gene (alkB), highly degenerate primers, MonF (positions 401–419, Pseudomonas putida GPo1 alkB numbering; 5'-TCAAYACMGSNCAYGARCT-3') and MonR (positions 820–801; 5'-CCGTARTGYTCNAYRTARTT-3'), were generated based on the conserved regions of several alkane hydroxylase gene sequences available in the GenBank database. The thermal cycles were taken in a T3 thermal cycler (Biometra). PCR products were purified and recovered by using a UNIQ-5 Column DNA Gel Extraction Kit (Sangon). Sequencing of the fragments was carried out on a model 377 automated DNA sequencer using a BigDye Terminators Cycle Sequencing Kit (Applied Biosystems). Sequence data were manually aligned with nucleotide sequences obtained from GenBank by using DNAMAN (version 5.1; Lynnon Biosoft). Alignments and phylogenetic analysis of ITS and alkB sequences were also carried out by using the DNAMAN program. Phylogenetic dendrograms of 16S rRNA gene sequences were constructed by three different algorithms: the neighbour-joining method (Saitou & Nei, 1987) using DNAMAN, and the maximum-likelihood (Felsenstein & Churchill, 1996) and maximum-parsimony (Fitch, 1971) methods using the PHYLIP package (version 3.6a2.1; Felsenstein, 2004). Bootstrapping analysis was used to evaluate the tree topology of the data obtained from the three algorithms based on 1000 resamplings.
Nearly full-length 16S rRNA gene sequences (1504 nt) of strains B-5T and NO1A were determined. Sequence similarity between the two strains was 99·6 %. Their closest relatives were A. venustensis ISO4T (95·2 %), A. jadensis T9T (94·6 %) and A. borkumensis SK2T (94·1 %). In all the three phylogenetic trees, strains B-5T and NO1A were included in the Alcanivorax cluster, whose integrity was supported in 100 % of the trees generated. The topology of the phylogenetic tree, shown in Fig. 1 (a more complete tree is available as Supplementary Fig. B in IJSEM Online), was reconstructed by using the neighbour-joining method. In Fig. 1, both strains branched with A. venustensis, but this branching point was only recovered in 570 trees out of 1000 generated in the bootstrap analysis. Similarly, the bootstrap value of this branch point was 52 % for maximum-parsimony analysis and 58 % for maximum-likelihood analysis, which indicated that the branching pattern was not stable.
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; Fernández-Martínez et al., 2003).
In the alkane hydroxylase (AlkB) sequence comparisons, a 420 nt DNA fragment was obtained from strain B-5T and encoded a polypeptide that showed 49·6 and 64·5 % similarity to the corresponding internal region of the Pseudomonas putida GPo1 AlkB and Burkholderia cepacia RR10 AlkB sequence, respectively. The amplified fragment contained two histidine motifs and a fourth motif (NYXEHYG[L/M]) conserved among the alkane hydroxylases (Shanklin et al., 1994; Smits et al., 1999). Similarly, the partial putative alkB genes were amplified from strain NO1A, A. venustensis ISO4T and A. jadensis T9T, but failed from A. borkumensis SK2T (AlkB sequence data for A. borkumensis used in alignment were from van Beilen et al., 2004). Alignment of deduced partial AlkB sequences was generated on the basis of these 420 nt internal gene fragments. The result showed that the AlkB sequences of strains B-5T and NO1A were nearly identical and closely related to that of A. venustensis ISO4T. The AlkB sequences of A. jadensis T9T and A. borkumensis SK2T formed a deep cluster and a separate group from the other taxa investigated (see Supplementary Fig. D in IJSEM Online). According to van Beilen et al. (2003), there was no clear linkage between the diversity of the alkB genes and phylogenetic lines. Nevertheless, when a particular genus, such as Mycobacterium or Burkholderia, was analysed independently, the phylogenetic tree of its partial AlkB was highly coincident with that of its 16S rRNA gene sequence (data not shown), as was the case for Alcanivorax.
DNA–DNA relatedness was determined using genomic DNA from the two strains and type strains of all Alcanivorax species using the method described by Coram & Rawlings (2002) and Tonjum et al. (1998). The genomic DNA of Escherichia coli DH5
was used as an outgroup sample. Each membrane contained salmon sperm DNA (Sigma) as a negative control. Quantification of hybridization signals was carried out on a White/ultraviolet transilluminator (UVP) using Grab-IT 2.51 and GelBase/GelBlot-Pro 3.00 (Synoptics). The results are shown in Supplementary Table A in IJSEM Online. Each value was the mean of at least two hybridization experiments. Strains B-5T and NO1A showed high DNA–DNA relatedness with each other (92 %), but were distinct from the type strains of Alcanivorax species based on low levels of DNA–DNA relatedness (13–45 %). Notably, all strains had very low levels of DNA–DNA relatedness with E. coli DH5 (
7 %). DNA–DNA relatedness among A. borkumensis SK2T, A. jadensis T9T and A. venustensis ISO4T fell in the range 17–49 %. A comparatively high level of DNA–DNA relatedness (36–45 %) was found between A. venustensis ISO4T and the two novel strains.
According to the present results, strains B-5T and NO1A shared high similarities in phenotypic and genotypic characteristics, such as 99·6 % 16S rRNA gene sequence similarity and 92 % DNA–DNA relatedness. Although isolated from two completely different marine habitats, the two strains should be classified as representing a single species. Phylogenetic analysis based on 16S rRNA gene sequence comparison showed that strains B-5T and NO1A represented a novel species of the -Proteobacteria, branching within the clade of Alcanivorax and forming a distinct branch with A. venustensis. We initially considered that the two strains and A. venustensis should be classified in a new genus based on their close relationship in 16S rRNA, ITS and alkB gene sequence data and fatty acid composition. However, this hypothesis was precluded for the following reasons. Firstly, there were no distinct and decisive traits to differentiate them from other members of the genus Alcanivorax. Secondly, the two strains and recognized species of the genus Alcanivorax shared comparatively high DNA–DNA relatedness values (13–45 %). Thirdly, the branching point of the cluster consisting of strains B-5T and NO1A and A. venustensis was statistically insignificant. Lastly, insufficient data regarding the fatty acids profiles of A. borkumensis and A. jadensis, as discussed by Fernández-Martínez et al. (2003), made it difficult to draw any definitive conclusions.
Thus, according to their phylogenetic relationships, DNA–DNA hybridization, ITS and alkB gene sequence comparisons and phenotypic traits, strains B-5T and NO1A exhibited characteristics that defined the genus Alcanivorax. In addition, both strains have a number of distinct phenotypic features that allow them to be distinguished from other Alcanivorax species (Table 2), such as the ability to grow at 45 °C and to utilize citrate, succinate and long-chain n-alkanes. Therefore, we consider that the species represented by strains B-5T and NO1A belongs to a novel species of the genus Alcanivorax, for which the name Alcanivorax dieselolei sp. nov. is proposed.
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Cells are 0·8–2·0 µm long and 0·3–0·7 µm wide, motile, lophotrichous, non-spore-forming, Gram-negative rods. Colonies on HLB agar are characteristically small, translucent, non-pigmented and slightly raised in the centre, with irregular, transparent and halo-like peripheries. Mesophilic. Growth temperature ranges from 15 to 45 °C (optimum 28 °C). NaCl is required for growth; cells grow in 1–15 % NaCl (optimum 3–7·5 %). Actively degrades Tween 80; catalase- and oxidase-positive, but negative for agarase, arginine dihydrolase, amylase and gelatinase. Nitrate is reduced to nitrite. Among the 95 carbon sources in the Biolog system, positive for Tweens 40 and 80, methyl pyruvate, mono-methyl succinate, acetic acid, citric acid, 
-hydroxybutyric acid, -hydroxybutyric acid, p-hydroxy phenyl acetic acid, DL-lactic acid, propionic acid, bromo succinic acid and 2,3-butanediol. Negative for all carbohydrates using Biolog GN. Good growth occurs in SM1 medium with citrate, p-hydroxyphenylacetate, pyruvate, lactate or n-alkane as carbon source. Sensitive to neomycin, kanamycin, amikacin and polymyxin B. Cells are able to degrade n-alkanes with chain length C5 to C36. Cellular fatty acids are C16 : 0, C18 : 17c, C16 : 17c, C19 : 0 cyclo 8c, C12 : 0 and C12 : 0 3OH. G+C content of the DNA is 62·1–62·5 mol%. Table 2
shows characteristics used to distinguish strain B-5T from other members of the genus Alcanivorax.
The type strain, B-5T (=DSM 16502T=CGMCC 1.3690T), was isolated from an oil-contaminated sea water at the Yellow River dock of Shengli oilfield, Bohai Sea. Strain NO1A was isolated from a deep-sea sediment sample in the Pacific nodule region A station (5027 m water depth).
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ACKNOWLEDGEMENTS |
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H. Kim, Y.-J. Choo, and J.-C. Cho Litoricolaceae fam. nov., to include Litoricola lipolytica gen. nov., sp. nov., a marine bacterium belonging to the order Oceanospirillales Int J Syst Evol Microbiol, August 1, 2007; 57(8): 1793 - 1798. [Abstract] [Full Text] [PDF]
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R. Rivas, P. Garcia-Fraile, A. Peix, P. F. Mateos, E. Martinez-Molina, and E. Velazquez Alcanivorax balearicus sp. nov., isolated from Lake Martel Int J Syst Evol Microbiol, June 1, 2007; 57(6): 1331 - 1335. [Abstract] [Full Text] [PDF]
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C. Liu, Y. Wu, L. Li, Y. Ma, and Z. Shao Thalassospira xiamenensis sp. nov. and Thalassospira profundimaris sp. nov. Int J Syst Evol Microbiol, February 1, 2007; 57(2): 316 - 320. [Abstract] [Full Text] [PDF]
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D. Yu. Sorokin, T. P. Tourova, E. A. Galinski, C. Belloch, and B. J. Tindall Extremely halophilic denitrifying bacteria from hypersaline inland lakes, Halovibrio denitrificans sp. nov. and Halospina denitrificans gen. nov., sp. nov., and evidence that the genus name Halovibrio Fendrich 1989 with the type species Halovibrio variabilis should be associated with DSM 3050 Int J Syst Evol Microbiol, February 1, 2006; 56(2): 379 - 388. [Abstract] [Full Text] [PDF]
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