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Int J Syst Evol Microbiol 56 (2006), 417-421; DOI  10.1099/ijs.0.02094-0
© 2006 International Union of Microbiological Societies

Roseibacterium elongatum gen. nov., sp. nov., an aerobic, bacteriochlorophyll-containing bacterium isolated from the west coast of Australia

Tomonori Suzuki, Youichirou Mori and Yukimasa Nishimura

Department of Applied Biological Science, Tokyo University of Science, 2641, Yamazaki, Noda, Chiba 278-8510, Japan

Correspondence
Tomonori Suzuki
chijun{at}rs.noda.tus.ac.jp


   ABSTRACT
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A novel aerobic, chemoheterotrophic, bacteriochlorophyll-containing bacterium, strain OCh 323T, was isolated from sand at Monkey Mia, Shark Bay, located on the west coast of Australia. The cells were Gram-negative, non-motile rods of variable length; one or both cell poles was narrower. Bacteriochlorophyll a was synthesized under aerobic conditions. Catalase, oxidase and urease were produced. The ONPG reaction was positive. The major component of the cellular fatty acid was octadecenoic acid (18 : 1). The DNA G+C content was 68·1 mol%. The results of 16S rRNA gene sequence comparisons revealed that strain OCh 323T formed a novel, separate line of descent within the {alpha}-3 group of the Alphaproteobacteria. The similarity value for the 16S rRNA gene sequence of strain OCh 323T and that of the most closely related species, Rhodovulum sulfidophilum, was 91·4 %. It is concluded that strain OCh 323T (=JCM 11220T=CIP 107377T) should be placed in a novel genus, Roseibacterium gen. nov., as the type strain of a novel species Roseibacterium elongatum sp. nov.

Published online ahead of print on 13 October 2005 as DOI 10.1099/ijs.0.02094-0.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain OCh 323T is AB061273.


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Since Sato (1978)Go reported on aerobic methylotrophs containing bacteriochlorophyll a, a variety of aerobic, anoxygenic, phototrophic bacteria have been described (Yurkov & Beatty, 1998Go). Recently, many novel genera of aerobic bacteriochlorophyll-containing bacteria, including Craurococcus (Saitoh et al., 1998Go), Paracraurococcus (Saitoh et al., 1998Go), Roseovarius (Labrenz et al., 1999Go), Rubrimonas (Suzuki et al., 1999aGo), Roseateles (Suyama et al., 1999Go), Roseivivax (Suzuki et al., 1999bGo), ‘Citromicrobium’ (Yurkov et al., 1999Go), Roseinatronobacter (Sorokin et al., 2000Go), Staleya (Labrenz et al., 2000Go), Acidisphaera (Hiraishi et al., 2000Go) and Roseibium (Suzuki et al., 2000Go), have been described.

Aerobic and chemoheterotrophic bacteriochlorophyll-containing bacteria have been isolated from specimens from a variety of marine environments on the east and west coasts of Australia (Shiba et al., 1991Go). Most of these isolates have been divided into several groups on the basis of phenotypic characteristics and DNA–DNA relatedness (Nishimura et al., 1994Go). On the basis of phenotypic characteristics and phylogenetic considerations, we have previously proposed three novel genera, Rubrimonas, Roseivivax and Roseibium, for three groups of those isolates (Suzuki et al., 1999aGo, bGo, 2000Go). The genera Rubrimonas and Roseivivax belong to the {alpha}-3 group, while the genus Roseibium belongs to the {alpha}-2 group of the Proteobacteria.

In the present study, the phenotypic characteristics and the phylogeny of strain OCh 323T, which has not previously been included in any group of these isolates, were investigated. On the basis of the results of these investigations, a novel genus and novel species are proposed.

Strain OCh 323T was previously isolated from sand at Monkey Mia, Shark Bay, located on the west coast of Australia, by Shiba et al. (1991)Go. The strain was cultivated on PPES-II medium (Taga, 1968Go) at 27 °C. The pH was adjusted to 7·8 with 10 % NaOH. Colonies of strain OCh 323T were circular, smooth, convex, entire, glistening, opaque and pink. Cells were stained with 1 % (w/v) aqueous uranyl acetate and examined under a JEOL model JEM-1200 EX electron microscope at an accelerating voltage of 80 kV. Cells were Gram-negative, non-motile rods (with one or both cell poles narrower) and of variable length (Fig. 1Go). Cell growth appeared to be monopolar, since one cell end was usually narrower and shorter than the other, possibly indicating a budding process (Hirsch, 1974Go). Cells of strain OCh 323T were 0·5–0·8x1·6–10·0 µm.


Figure 1
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  		Fig. 1. Electron micrograph of negatively stained cells of strain OCh 323T. Bar, 500 nm.

 
Physiological and biochemical characteristics were examined according to the methods of Shiba & Simidu (1982)Go. Acid production from D-fructose, D-glucose and lactose was tested on ZOF medium (Lemos et al., 1985Go) supplemented with a 1 % (w/v) carbohydrate source.

Strain OCh 323T grew chemoheterotrophically under aerobic conditions but could not grow phototrophically under anaerobic conditions in the light. Optimum growth occurred at pH 7·5–8·0 and at 27–30 °C. The strain required NaCl, with growth occurring in 0·5–7·5 % NaCl. The biochemical and physiological characteristics of strain OCh 323T are given in Table 1Go.


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  		Table 1. Comparative physiological and biochemical characteristics of aerobic, chemoheterotrophic, bacteriochlorophyll-containing bacteria

Strains: 1, strain OCh 323T; 2, Roseivivax halodurans OCh 239T; 3, Roseivivax halotolerans OCh 210T; 4, Rubrimonas cliftonensis OCh 317T; 5, Roseobacter litoralis OCh 149T; 6, Roseobacter denitrificans OCh 114T. +, Positive; –, negative; W, weakly positive. All strains are positive for catalase and oxidase and for growth in the presence of 0·5 % NaCl. All strains are negative in the Voges–Proskauer test, for H2S production and for the hydrolysis of alginateand starch.

 
Cells were washed and sonicated for 3 min in 30 mM Tris/HCl (pH 7·5). The absorption spectrum of cell extracts was recorded with a Shimadzu UV-VIS recording spectrophotometer (model UV-160). Ultrasonically disrupted cells in buffer had absorption peaks in the near-infrared region at 879 and 800 nm (Fig. 2Go), indicating the presence of bacteriochlorophyll a in light-harvesting complex I and the photochemical reaction centre.


Figure 2
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  		Fig. 2. Absorption spectrum of ultrasonically disrupted membrane of strain OCh 323T, showing the presence of the photosynthetic reaction centre (minor peak at 800 nm) and light-harvesting complex I (major peak at 879 nm).

 
Strain OCh 323T was grown in PPES-II broth at 27 °C with shaking. Cells were washed with distilled water and freeze-dried. A 100 mg portion of lyophilized cells was methylated with 3 ml 5 % (v/v) HCl/methanol at 100 °C for 3 h. Fatty acid methyl esters were extracted with hexane three times. The hexane fraction was washed with distilled water, dehydrated with anhydrous Na2SO4 and then concentrated by using a rotary evaporator. Hydroxylated fatty acid methyl esters were separated from non-polar fatty acid methyl esters by TLC (silica gel 60 F254; Merck) using hexane/diethylether (85 : 15, v/v) as the developing solvent. The spots were visualized by spraying with 0·02 % (w/v) 2',7'-dichlorofluorescein ethanol solution and then scraped off the TLC plate under UV light. Hydroxylated fatty acid methyl esters were extracted with diethylether. After removal of the diethylether from the extracted solution, the sample was dissolved in a small volume of hexane. To verify the presence of cyclopropanic and unsaturated acids, they were saturated with hydrogen. The analysis was performed in a GC-8A gas chromatograph (Shimadzu) equipped with an FFS ULBON HR-1 capillary column (0·25 mmx50 m; Shinwa Chemical Industries), at 170–230 °C (rate: 4 °C min–1). The detector used was flame-ionized. The chromatogram was processed by using Chromatopac C-R3A (Shimadzu).

The cellular fatty acids of strain OCh 323T are described in Table 2Go; the major cellular fatty acid is octadecenoic acid (18 : 1).


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  		Table 2. Fatty acid compositions (%) of whole-cell hydrolysates of aerobic, chemoheterotrophic, bacteriochlorophyll-containing bacteria

Strains: 1, strain OCh 323T; 2, Roseivivax halodurans OCh 239T; 3, Roseivivax halotolerans OCh 210T; 4, Rubrimonas cliftonensis OCh 317T; 5, Roseobacter litoralis OCh 149T; 6, Roseobacter denitrificans OCh 114T. –, Not detected; tr, trace.

 
The cells were suspended in saline EDTA (0·15 M NaCl, 0·1 M EDTA, pH 8·5) and then lysed at 60 °C for 10 min with 0·5 % SDS (final concentration). Chromosomal DNA was purified according to standard procedures (Sambrook et al., 1989Go).

The DNA G+C content was determined by the HPLC method (Katayama-Fujimura et al., 1984Go). Chromosomal DNA was denatured to the single stranded form by means of heating at 95 °C for 5 min. The single-stranded DNA was hydrolysed to nucleotides with P1 nuclease (DNA-GC kit; Seikagaku Kogyo) in 40 mM sodium acetate and 2 mM ZnSO4 (pH 5·3) at 50 °C for 2 h. The nucleotide composition was analysed by HPLC, which was performed in a Shimadzu high-performance liquid chromatograph (model LC-6A) equipped with an octadecyl-silica column (YMC pack AQ-312, 6 mmx150 mm), and detected at 260 nm. The mobile phase was 10 mM phosphate buffer (pH 3·5). The DNA G+C content was corrected by dividing the value of the peak area of the sample nucleotide by the peak area of the standard nucleotide. The G+C content of the DNA from strain OCh 323T was 68·1 mol%.

Amplification of the 16S rRNA gene was performed on a Quick Thermo Personal QTP-1 thermocycler (Nippon Genetics) in a 100 µl reaction volume, as described previously (Suzuki et al., 1999aGo, bGo). The amplified DNA fragments were purified by gel electrophoresis on 1 % agarose S (Nippon Gene) and recovered with glass powder, using Prep-A-Gene DNA purification systems (Bio-Rad Laboratories). Sequencing was carried out as described previously (Suzuki & Yamasato, 1994Go).

The sequences of strain OCh 323T and of reference bacterial species were aligned with the CLUSTAL X program, version 1.64b (Thompson et al., 1997Go); the alignment was checked manually. The phylogenetic analysis was performed with PHYLIP, version 3.57c (Felsenstein, 1995Go). A distance matrix was calculated with DNADIST, using the Kimura two-parameter method, and a phylogenetic tree was reconstructed using NEIGHBOR. The stability of the clusters was ascertained by performing bootstrap analyses (1000 replications) with SEQBOOT, DNADIST, NEIGHBOR and CONSENSE.

The 16S rRNA gene sequence of strain OCh 323T was determined and aligned with other available 16S rRNA gene sequences. A comparison of the 16S rRNA gene sequences, for which a phylogenetic tree was reconstructed (Fig. 3Go), revealed that strain OCh 323T belonged to the {alpha}-3 group of the Proteobacteria, forming a separate line of descent. The 16S rRNA gene sequence similarity values between strain OCh 323T and other strains belonging to this group were low: 91·4 % for Rhodovulum sulfidophilum, 90·7 % for Ruegeria algicola, 90·5 % for Rhodovulum adriaticum, 90·2 % for Rhodobacter sphaeroides and 90·0 % for Rhodovulum iodosum.


Figure 3
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  		Fig. 3. Neighbour-joining phylogenetic tree derived from analysis of the 16S rRNA gene sequences of Roseibacterium elongatum OCh 323T and other members of the {alpha}-3 group of the Proteobacteria. Numbers at nodes indicate levels of bootstrap support based on 1000 resamplings; only values above 500 are considered as significant and are indicated.

 
Aerobic bacteriochlorophyll-containing, budding bacteria are known, e.g. Porphyrobacter neustonensis (Fuerst et al., 1993Go), Roseovarius tolerans (Labrenz et al., 1999Go) and Staleya guttiformis (Labrenz et al., 2000Go). Phylogenetically, Porphyrobacter neustonensis is located in the {alpha}-4 group, whereas Roseovarius tolerans and S. guttiformis belong to the {alpha}-3 group of the Proteobacteria. Strain OCh 323T is distantly related to Roseovarius tolerans and S. guttiformis. It has been demonstrated previously that phenotypic characteristics are not necessarily reflected in phylogenetic relationships; this inconsistency was also apparent in the present study.

The phylogenetic analysis supports the need for a novel genus, Roseibacterium gen. nov., to be created for strain OCh 323T, and we propose that strain OCh 323T should be described as the type strain of Roseibacterium elongatum gen. nov., sp. nov.

Description of Roseibacterium gen. nov.
Roseibacterium (Ro.sei.bac.te'ri.um. L. adj. roseus rose, pink; Gr. neut. n. bakterion rod; N.L. neut. n. Roseibacterium pink, rod-shaped bacterium).

Cells are Gram-negative, non-motile rods that multiply by monopolar growth, i.e. by an apparent budding process. Aerobic chemoheterotrophs. Cells exhibit catalase and oxidase activities. Bacteriochlorophyll a is synthesized under aerobic conditions. The major cellular fatty acid is octadecenoic acid (18 : 1). The genus Roseibacterium belongs to the {alpha}-3 group of the Proteobacteria. The type species is Roseibacterium elongatum.

Description of Roseibacterium elongatum sp. nov.
Roseibacterium elongatum (e.lon.ga'tum. L. part. neut. adj. elongatum elongated, stretched out).

Colonies are circular, smooth, convex, entire, glistening, opaque and pink. Cells are 0·5–0·8x1·6–10·0 µm. Optimum growth occurs at pH 7·5–8·0 and at 27–30 °C. Growth occurs in the presence of 0·5–7·5 % NaCl, but not in the absence of NaCl. Cells exhibit urease activity, but not nitrate reductase or phosphatase activities. Negative in the Voges–Proskauer test. The ONPG reaction is positive. Cells do not produce indole or H2S. Gelatin is hydrolysed, but alginate, starch and Tween 80 are not. Cells do not utilize D-glucose, acetate, citrate, DL-malate, pyruvate, succinate or ethanol. Acid is not produced from D-fructose, D-glucose or lactose. The absorption spectrum of ultrasonically disrupted cells in the near-infrared region has maxima at 879 nm and 800 nm. The G+C content of the DNA is 68·1 mol%.

The type strain, strain OCh 323T (=JCM 11220T=CIP 107377T), was isolated from sand at Monkey Mia, Shark Bay, located on the west coast of Australia.


   ACKNOWLEDGEMENTS
 
We are grateful to Dr Tsuneo Shiba (National Fisheries University, Shimonoseki, Japan) for providing the bacterial strains.


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