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Int J Syst Evol Microbiol 56 (2006), 529-533; DOI  10.1099/ijs.0.64013-0
© 2006 International Union of Microbiological Societies

Yangia pacifica gen. nov., sp. nov., a novel member of the Roseobacter clade from coastal sediment of the East China Sea

Xin Dai1, Bao-Jun Wang1, Qing-Xiang Yang2, Nian-Zhi Jiao2 and Shuang-Jiang Liu1

1 State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Zhong-Guan-Cun, Haidian, Beijing 100080, China
2 State Key Laboratory for Marine Environmental Sciences, Xiamen University, Xiamen, 361005, China

Correspondence
Shuang-Jiang Liu
shuangjiang{at}hotmail.com


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An aerobic, Gram-negative bacterial isolate, strain DX5-10T, was isolated from coastal sediment of the East China Sea. The taxonomy of strain DX5-10T was studied by phenotypic and phylogenetic methods. Strain DX5-10T was motile, formed faint-yellowish colonies and was positive for catalase reaction and weakly positive for oxidase reaction. The nearly complete 16S rRNA gene of strain DX5-10T was obtained and sequence analysis indicated that strain DX5-10T represented an independent lineage within the Roseobacter clade of Alphaproteobacteria. Strain DX5-10T was phylogenetically related to members of the genera Roseobacter, Loktanella, Roseisalinus, Silicibacter, Antarctobacter, Sulfitobacter, Salipiger, Ruegeria and Roseivivax, and the sequence identities among them were less than 95·0 %. The predominant respiratory ubiquinone of strain DX5-10T was Q-10 and the DNA G+C content of strain DX5-10T was 63·3 mol%. Therefore, strain DX5-10T represents a novel species of a novel genus, for which the name Yangia pacifica gen. nov., sp. nov. is proposed, with the type strain DX5-10T (=CGMCC 1.3455T=JCM 12573T).

Abbreviations: Bchl a, bacteriochlorophyll a

Published online ahead of print on 28 October 2005 as DOI 10.1099/ijs.0.64013-0.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Yangia pacifica DX5-10T is AJ877265.


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Members of the Roseobacter clade are aerobic, Gram-negative bacteria and have been widely detected in marine or saline lacustrine samples by ribosomal probing (González & Moran, 1997Go; Zubkov et al., 2001Go) and 16S rRNA gene cloning (Eilers et al., 2000Go; Rappé et al., 2000Go). Bacterial species that belong to the Roseobacter clade have been frequently isolated from such environments. The Roseobacter clade within the order Rhodobacterales contains 33 genera (Garrity et al., 2004Go), and recently several novel genera, including Oceanicola (Cho & Giovannoni, 2004Go), Loktanella (Van Trappen et al., 2004Go), Salipiger (Martínez-Cánovas et al., 2004Go), Roseisalinus (Labrenz et al., 2005Go) and Thalassobacter (Macián et al., 2005Go), have been established. The physiological characterization of described species within these genera indicates that they are metabolically diverse and are potentially important players in the degradation of lignin and aromatic compounds (Buchan et al., 2001Go) and in biogeocycling of organic (González et al., 2003Go) or inorganic sulfur-containing compounds (Sorokin, 1995Go; Pukall et al., 1999Go).

During an ecological survey of microbial diversity of coastal sediments, an aerobic, Gram-negative bacterium, strain DX5-10T, was obtained that is phylogenetically related to members of the genera Roseobacter, Loktanella, Roseisalinus, Roseivivax, Salipiger, Silicibacter and Sulfitobacter. This bacterial strain, together with some uncharacterized marine isolates (Teske et al., 2000Go; Buchan et al., 2001Go), formed a distinct lineage within the Roseobacter clade. In this note, we describe the characterization and classification of strain DX5-10T.

Strain DX5-10T was isolated from coastal sediment of the East China Sea located in Fujian Province. The sample (from 4–6 cm beneath the surface) was diluted with 9 ml sterile saline solution and 0·1 ml 10–3 and 10–4 dilutions were plated onto artificial sea water basal medium with 1 % peptone and 0·5 % yeast extract (Eguchi et al., 1996Go). Routine cultivation of strain DX5-10T was done at 30 °C in marine broth 2216 (MB; Difco). Methods for observation of morphology, physiological and biochemical tests, including catalase and oxidase reactions, nitrate reduction, requirement for NaCl, ranges of temperature and pH for growth, decomposition of gelatin and casein and hydrolysis of starch were described and cited in a previous report (Dai et al., 2005Go).

Biomass for chemotaxonomic analysis was harvested from MB cultures on a rotary shaker (100 r.p.m., 30 °C). Quinones were extracted and purified according to Collins (1985)Go and were analysed by HPLC equipped with a Hewlett Packard 1050 system and a Zorbax ODS column (Agilent Technologies) operating at 40 °C, with Ruegeria gelatinovorans DSM 5887T as reference strain. The mobile phase was a mixture of acetonitrile/2-propanol (2 : 1·2) with a flow rate of 1 ml min–1. The UV detection wavelength was set at 270 nm. The fatty-acid profile of whole cells was analysed by gas chromatography by using a model HP6890GC equipped with a hydrogen-ionization detector. Peaks were identified with pre-installed software, HPCHEM-STATION (version A5.01).

Genomic DNA of strain DX5-10T was extracted according to Marmur (1961)Go and G+C content was determined by thermal denaturation. The 16S rRNA gene of strain DX5-10T was amplified and sequenced as described previously (Zhang et al., 2003Go). Alignments of 16S rRNA gene sequences of strain DX5-10T and species of the Roseobacter clade (Fig. 1Go) were carried out with CLUSTAL X program (version 1.8; Thompson et al., 1997Go). Phylogenetic trees were constructed using the neighbour-joining method (Saitou & Nei, 1987Go) with the Kimura two-parameter model (Kimura, 1980Go) by using the programs of TREECON (Van de Peer & De Wachter, 1994Go).


Figure 1
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  		Fig. 1. Neighbour-joining tree based on 16S rRNA gene sequence analysis indicates that strain DX5-10T, hydrothermal vent strains NF18 and AG33, and marine isolate SE45 (Buchan et al., 2001Go; Teske et al., 2000Go) form a coherent cluster within the Roseobacter clade, representing the novel genus Yangia. Rubrimonas cliftonensis OCh 317T (D85834) was used as the outgroup. Bootstrap confidence values obtained from 1000 bootstrap replications are given at nodes. Bar, 0·05 substitutions per nucleotide position.

 
Bacteriochlorophyll a (Bchl a) was detected spectrophotometrically in vivo and in vitro. For in vivo measurements, 5 ml of strain DX5-10T culture in MB incubated under a natural daylight rhythm was collected, washed and resuspended in 5 ml PBS (137 mmol NaCl l–1, 2·7 mmol KCl l–1, 4·3 mmol Na2HPO4.7H2O l–1, 1·4 mmol KH2PO4 l–1, pH 7·8). For in vitro measurements, 5 ml liquid culture was centrifuged at 5000 g for 10 min. The cells were lysed in liquid nitrogen and Bchl a was extracted using 5 ml ice-cold acetone/methanol solution (7 : 2, v/v) in the dark at –20 °C for 12 h. Cell fragments were then removed by centrifugation. Spectrophotometric measurements were performed with an HP8453 UV/Vis spectrometer by scanning the wavelength range 400–900 nm. Pigments were detected using HPLC Angilent (ODS column: 5 µm, 4x250 mm; UV2000 detector {lambda}=362 nm) as described by Koblízek et al. (2003)Go. Roseobacter litoralis DSM 6996T was used as a control.

Strain DX5-10T formed faint-yellowish colonies on MB agar. Cells of strain DX5-10T were motile, Gram-negative rods (0·8x1·0–1·5 µm in size). The catalase reaction was positive and oxidase reaction was weakly positive. Growth occurred at temperatures of 22–40 °C and at pH 5·0–10·0, with optima at 37 °C and pH 7·5. NaCl was required but concentrations greater than 13 % were inhibitory to growth. Maximal growth was observed at 5 % NaCl. Bchl a was not detected either in vivo or in vitro. Additional phenotypic properties are given in the following genus and species description. The cells of strain DX5-10T contained ubiquinone 10 (Q-10). The fatty-acid profile of strain DX5-10T grown in MB is detailed in the species description and in Table 1Go. The genomic DNA G+C content was 63·3 mol%. A list of properties that differentiate strain DX5-10T from some related members of the Roseobacter clade is provided in Tables 1 and 2GoGo. In brief, strain DX5-10T was different from members of the genera Roseivivax and Salipiger in that Bchl a was not detected either in vivo or in vitro (Table 2Go). Furthermore, strain DX5-10T contained 17 : 1{omega}8c (3·93 %) and 17 : 0 (1·44 %), which were not detected in any other genera as listed in Table 1Go, and the fatty acid methyl ester 11-methyl 18 : 1{omega}7c and cyclo-substituted fatty acid 19 : 0 cyclo {omega}8c that were present in Salipiger mucosus A3T were not detected in strain DX5-10T.


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  		Table 1. Comparison of fatty-acid compositions of strain DX5-10T with some type species of the family Rhodobacteraceae

Values are percentages of total fatty acids and only percentages higher than 1 % are shown; –, negative or percentages lower than 1 %; ND, no data available. Species/strains: 1, Yangia pacifica sp. nov. DX5-10T; 2, Salipiger mucosus A3T (data from Martínez-Cánovas et al., 2004Go); 3, Roseivivax halodurans OCh 239T (Suzuki et al., 1999Go; Martínez-Cánovas et al., 2004Go); 4, Loktanella salsilacus (10 strains) (Van Trappen et al., 2004Go); 5, Oceanicola granulosus HTCC 2516T (Cho & Giovannoni, 2004Go); 6, Roseisalinus antarcticus EL-88T (Labrenz et al., 2005Go); 7, Ketogulonicigenium vulgare DSM 4025T (Urbance et al., 2001Go); 8, Antarctobacter heliothermus EL-219T (Labrenz et al., 1998Go).

 

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  		Table 2. Characteristics that differentiate Yangia pacifica gen. nov., sp. nov. from related genera

Genera: 1, Salipiger (data from Martínez-Cánovas et al., 2004Go); 2, Roseivivax (Suzuki et al., 1999Go); 3, Loktanella (Van Trappen et al., 2004Go); 4, Oceanicola (Cho & Giovannoni, 2004Go); 5, Roseisalinus (Labrenz et al., 2005Go); 6, Ketogulonicigenium (Urbance et al., 2001Go); 7, Antarctobacter (Labrenz et al., 1998Go). +, Positive; –, negative; W, weakly positive; ND, no data available.

 
The nearly complete 16S rRNA gene of strain DX5-10T was amplified and partially sequenced (1351 bp). A BLASTN search with the 16S rRNA gene sequence of strain DX5-10T in the GenBank database and phylogenetic analysis based on 16S rRNA gene sequence identities showed that strain DX5-10T was related to species of various genera: Roseobacter gallaeciensis BS107T (95·0 %), Loktanella hongkongensis JCM 12479T (94·7 %), Roseisalinus antarcticus EL-88T (94·5 %), Silicibacter pomeroyi DSS-3T (94·5 %), Antarctobacter heliothermus EL-219T (94·2 %), Sulfitobacter dubius KMM 3554T (94·2 %), Salipiger mucosus A3T (94·1 %), Ruegeria atlantica IAM 14463T (94·0 %) and Roseivivax halodurans OCh 210T (93·9 %). Following these discoveries, a detailed phylogenetic analysis on the species with validly published names of the Roseobacter clade and strain DX5-10T was performed, and the phylogenetic tree based on the nearly complete 16S RNA gene sequence (1324 bp) similarity indicates that strain DX5-10T, together with previously isolated but not taxonomically described strains NF18, AG33 and SE45 (Teske et al., 2000Go; Buchan et al., 2001Go), formed an independent lineage representing a novel genus within the Roseobacter clade (Fig. 1Go). This lineage represented by strain DX5-10T is the neighbour to the clade of the species of Roseivivax and Salipiger mucosus A3T (Fig. 1Go), and the 16S rRNA gene identities of strain DX5-10T between them ranged from 93·7 to 94·1 %.

Combining the phenotypic and phylogenetic studies, we propose that strain DX5-10T represents a novel species of a novel genus, Yangia pacifica gen. nov., sp. nov.

Description of Yangia gen. nov.
Yangia (Yan'gi.a. N.L. fem. n. Yangia after the Chinese microbiologist H.-F. Yang, who founded the research of environmental microbiology in the early 1960s in China).

Gram-negative rods, motile. Aerobic heterotroph. When grown on marine agar 2216 plates, small, wettish, shiny, faint-yellowish colonies develop within 3–5 days. Cells do not form spores. Growth requires NaCl. Catalase reaction is positive and oxidase reaction is weakly positive. The predominant respiratory quinone is Q-10. Major fatty acids are 18 : 1 and 16 : 0. Cells also contain 3-hydroxylated 12 : 0. The type species is Yangia pacifica.

Description of Yangia pacifica sp. nov.
Yangia pacifica (pa.ci'fi.ca N.L. fem. adj. pacifica pertaining to the Pacific Ocean, the origin of the type strain).

In addition to the properties described above for the genus, the following properties are observed. Cells are 0·8x1·0–1·5 µm in size and tend to aggregate after cell division. Strictly aerobic; does not grow under anaerobic conditions. Cells grow at 22–40 °C and at pH 5·0–10·0, with optima at 37 °C and pH 7·5. NaCl is required and the species grows in the NaCl concentration range of 1–10 % (optimal growth occurs at 5 % NaCl). Bchl a is not detected either in vivo or in vitro. Nitrate reduction, hydrolysis of starch, gelatin liquefaction and indole formation are negative. Accumulates poly-(3-hydroxybutyric) acids. Urease formation is positive. Citric acid is not assimilated. Tests for methyl red and Voges–Proskauer are negative. Maltose, lactate, malate, arginine and glutamate support growth as sole carbon sources. Glucose, lactose, mannitol, sorbitol, inositol, arabinose, fructose, sucrose, L-lysine, L-leucine and L-phenylalanine do not support growth. The cellular fatty-acid profile is outlined in Table 1Go. DNA G+C content is 63·3 mol%.

The type strain, DX5-10T (=CGMCC 1.3455T=JCM 12573T), was isolated from a sample of coastal sediment from the East China Sea of the Pacific Ocean.


   ACKNOWLEDGEMENTS
 
Dr Y.-N. Wang, currently at the Tsinghua University, Beijing, PR China, was involved in the isolation of strain DX5-10T. This work was supported by grants from National Natural Science Foundation of China (3040 0007) and Chinese Academy of Sciences (KSCX2-SW-113). This paper is dedicated to the memory of Professor Hui-Fang Yang, who passed away in March 2005.


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