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Int J Syst Evol Microbiol 55 (2005), 177-181; DOI  10.1099/ijs.0.63251-0
© 2005 International Union of Microbiological Societies

Pibocella ponti gen. nov., sp. nov., a novel marine bacterium of the family Flavobacteriaceae isolated from the green alga Acrosiphonia sonderi

Olga I. Nedashkovskaya1, Seung Bum Kim2,{dagger}, Kang Hyun Lee2, Kyung Sook Bae2, Galina M. Frolova1, Valery V. Mikhailov1 and In Seop Kim3

1 Pacific Institute of Bioorganic Chemistry of the Far-Eastern Branch of the Russian Academy of Sciences, Pr. 100 Let Vladivostoku 159, 690022, Vladivostok, Russia
2 Korean Collection for Type Cultures, Biological Resources Center, Korea Institute of Bioscience and Biotechnology, 52 Oun Dong, Yusong, Daejon 305-333, Republic of Korea
3 Department of Biological Sciences, Hannam University, 133 Ojung Dong, Daejon 306-791, Republic of Korea

Correspondence
Olga I. Nedashkovskaya
olganedashkovska{at}piboc.dvo.ru
or
olganedashkovska{at}yahoo.com


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A marine, heterotrophic, Gram-negative, aerobic, yellow-pigmented, bacterium that was motile by gliding, isolated from the green alga Acrosiphonia sonderi, was studied by polyphasic taxonomic methods. 16S rRNA gene sequence analysis indicated that strain KMM 6031T formed a distinct lineage within the family Flavobacteriaceae. On the basis of phenotypic, chemotaxonomic, genotypic and phylogenetic analyses, the novel bacterium was classified as Pibocella ponti gen. nov., sp. nov. The type strain is KMM 6031T (=KCTC 12262T=NBRC 100591T=LMG 22573T).

Published online ahead of print on 30 July 2004 as DOI 10.1099/ijs.0.63251-0.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Pibocella ponti KMM 6031T is AY576654.

{dagger}Present address: Department of Microbiology, School of Bioscience and Biotechnology, Chungnam National University, Yusong, Daejon 305-764, Republic of Korea. Back


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The bacteria belonging to the family Flavobacteriaceae are one of the dominant groups of microbial populations inhabiting shallow marine environments and Antarctic meromictic lakes of marine origin (Bowman et al., 1997Go; Glöckner et al., 1999Go; Bano & Hollibaugh, 2002Go; Kirchman, 2002Go; Van Trappen et al., 2002Go). Among flavobacteria, there are both halotolerant and moderately halophilic micro-organisms. The representatives of the genera Chryseobacterium, Flavobacterium, Formosa and Gillisia grow in the absence of NaCl or sea water in the nutrient medium (Vandamme et al., 1994Go; Bernardet et al., 1996Go; Ivanova et al., 2004Go; Van Trappen et al., 2004Go). However, the majority of members of the family Flavobacteriaceae require Na+ ions for growth (Bernardet et al., 2002Go).

During investigation of the taxonomic diversity of the microbial population of the common green alga Acrosiphonia sonderi inhabiting the Sea of Japan, a novel moderately halophilic bacterium was isolated. Phylogenetic analysis based on 16S rRNA gene sequencing, supported by polyphasic taxonomic study, revealed that strain KMM 6031T is a member of the family Flavobacteriaceae and represents a new genus and species, for which the name Pibocella ponti gen. nov., sp. nov. is proposed.

The strain KMM 6031T was isolated from a sample of the green alga Acrosiphonia sonderi collected in Troitsa Bay, Gulf of Peter the Great, Sea of Japan, during June 2000. For strain isolation, 0·1 ml homogenates of algal fronds were transferred onto plates of marine agar 2216. After primary isolation and purification, strains were cultivated at 28 °C on the same medium and stored at –80 °C in marine broth supplemented with 20 % (v/v) glycerol.

Genomic DNA extraction, PCR and sequencing of the 16S rRNA gene followed previous procedures (Kim et al., 1998Go). The sequence data obtained were aligned together with those of representative members of the family Flavobacteriaceae by using PHYDIT version 3.2 (http://plaza.snu.ac.kr/~jchun/phydit/). Phylogenetic trees were inferred by using suitable programs of the PHYLIP package (Felsenstein, 1993Go). Phylogenetic distances were calculated from the models of Kimura (1980)Go and the trees were constructed on the basis of the neighbour-joining (Saitou & Nei, 1987Go), least-squares (Fitch & Margoliash, 1967Go) and maximum-likelihood (Felsenstein, 1993Go) algorithms. Bootstrap analysis was performed with 1000 resampled datasets, using SEQBOOT and CONSENSE programs of the PHYLIP package.

A phylogenetic analysis of the almost-complete 16S rRNA gene sequence (1447 nucleotide positions) revealed that strain KMM 6031T formed a distinct lineage within a cluster group including members of the family Flavobacteriaceae such as Aequorivita, Vitellibacter, Muricauda, Arenibacter, Zobellia and Maribacter (Fig. 1Go). The 16S rRNA gene sequence similarity values of strain KMM 6031T and its close relatives Maribacter aquivivus, Maribacter orientalis and Maribacter ulvicola were 95·8, 95·7 and 95 %, respectively. The low levels of sequence similarity of the strain tested with the other members of the family Flavobacteriaceae described to date (88·9–93 %) clearly demonstrate that the bacterium isolated in this study represents a new genus.



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  		Fig. 1. Phylogenetic tree based on the 16S rRNA gene sequences of strain KMM 6031T and representative members of related genera in the family Flavobacteriaceae. The phylogenetic tree was generated by a neighbour-joining method (Saitou & Nei, 1987Go). Numbers at nodes indicate bootstrap values (%) and asterisks indicate branches that were also recovered in Fitch–Margoliash and maximum-likelihood trees. Bar, 0·01 substitutions per nucleotide position.

 
The DNA was extracted following the method of Marmur (1961)Go and the G+C content of the DNA (mol%) was determined by the thermal denaturation method (Marmur & Doty, 1962Go). The DNA G+C content of strain KMM 6031T was 35·5 mol%.

The analysis of fatty acid methyl esters was carried out according to the standard protocol of the Microbial Identification System (Microbial ID). Isoprenoid quinones were extracted from lyophilized cells and analysed as described by Akagawa-Matsushita et al. (1992)Go. Isoprenoid quinone composition was characterized by HPLC (Shimadzu instruments) using a reverse-phase type Zorbax ODS column (250x4·6 mm) and acetonitrile/2-propanol (65 : 35, v/v) as a mobile phase at a flow rate of 0·5 ml min–1. The column was kept at 40 °C. Menaquinones were detected by monitoring absorbance at 270 nm and were identified by comparison with known quinones from reference strain Salegentibacter salegens DSM 5424T.

The predominant cellular fatty acids of KMM 6031T were branched-chain saturated and unsaturated, namely i-15 : 0 (8·7 %), a-15 : 0 (5·4 %), i-15 : 1 (11·7 %), i-16 : 1 (6·2 %), i-16 : 0 (12·1 %), i-17 : 1{omega}9c (5·2 %), i-16 : 0 3-OH (5·9 %) and i-17 : 0 3-OH (5·6 %) fatty acids (Table 1Go). The major respiratory quinone is MK-6.


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  		Table 1. Whole-cell fatty acid profiles (percentage content) of Pibocella ponti gen. nov., sp. nov. KMM 6031T and Maribacter species

Strains: 1, Pibocella ponti KMM 6031T; 2, Maribacter sedimenticola KMM 3903T; 3, Maribacter aquivivus KMM 3949T; 4, Maribacter ulvicola KMM 3951T; 5, Maribacter orientalis KMM 3947T. Data from Nedashkovskaya et al. (2004a)Go and this study. Values over 5 % are in bold; –, not detected.

 
Phenotypic analysis was performed by using previously described methods (Nedashkovskaya et al., 2003aGo, bGo). Gliding motility was determined as described by Bowman (2000)Go.

The physiological and biochemical characteristics of strain KMM 6031T are listed in the species description and Table 2Go. The phenotypic features that separate the strain studied from close relatives of the family Flavobacteriaceae are shown in Table 2Go. The results of phenotypic examination demonstrated that the strain studied has many traits in common with Maribacter species. However, strain KMM 6031T grew at 12 % NaCl and degraded casein, in contrast to Maribacter species. Significant differences in the cellular fatty acid compositions of the strain studied and the type strains of the genus Maribacter were found (Table 1Go). For example, fatty acids a-15 : 1, i-16 : 1, a-17 : 1{omega}9c, 15 : 0 2-OH and 17 : 0 2-OH are present in KMM 6031T (2·1, 6·2, 2·3, 1·8 and 2·8 %, respectively), but are absent in Maribacter species. The fatty acids i-16 : 0 and 17 : 1{omega}6c were present at significant levels in the cell extract of KMM 6031T (12·1 and 4·7 %, respectively), but are only minor components in type strains of Maribacter species (0·3–1·1 and 0·5–1·7 %, respectively). The hydroxy fatty acid i-15 : 0 3-OH was only found in minor quantities in the strain KMM 6031T (0·9 %), while in Maribacter species this component was more abundant, present at 2·9–5·4 %. In addition, 15 : 0 3-OH, present at 1·5–2·4 % in Maribacter type strains, was not detected in KMM 6031T.


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  		Table 2. Differential characteristics of Pibocella gen. nov. and other related genera of the family Flavobacteriaceae

Data from Barbeyron et al. (2001)Go, Bruns et al. (2001)Go, Ivanova et al. (2001)Go, Bowman & Nichols (2002)Go, Nedashkovskaya et al. (2003bGo, cGo, 2004aGo, bGo, c)Go and this study. +, Positive; –, negative; V, variable; ND, not determined. Members of all genera require Na+ or sea water for growth.

 
It is therefore evident from phylogenetic distinctness in combination with significant differences in cellular fatty acid composition and phenotypic findings, that the strain studied should be differentiated from its nearest neighbours Maribacter aquivivus, Maribacter orientalis and Maribacter ulvicola.

Thus, the results of the polyphasic analysis presented in this work demonstrate that the bacterium studied could not be assigned to any of the currently described taxa of the family Flavobacteriaceae and support the placement of strain KMM 6031T in a new genus, Pibocella gen. nov., as Pibocella ponti sp. nov.

Description of Pibocella gen. nov.
Pibocella [Pi.bo.cel'la. N.L. fem. n. Pibocella arbitrary name, derived from the acronym PIBOC (Pacific Institute of Bioorganic Chemistry, FEB RAS), where the type species was first isolated and examined].

Rod-shaped cells. Gram-negative. Do not form endospores. Motile by gliding. Strictly aerobic. Produce non-diffusible yellow–orange pigments. No flexirubins are formed. Chemo-organotrophs. Cytochrome oxidase-, catalase- and alkaline phosphatase-positive. The major respiratory quinone is MK-6. The main cellular fatty acids are straight-chain unsaturated and branched-chain unsaturated fatty acids i-15 : 0, a-15 : 0, i-15 : 1, i-16 : 1, i-16 : 0, i-16 : 0 3-OH, i-17 : 1{omega}9c, i-17 : 0 3-OH and summed feature 3, consisting of i15 : 0 2-OH and/or 16 : 1{omega}7c. As determined by 16S rRNA gene sequence analysis, the genus Pibocella is a member of the family Flavobacteriaceae. The type species is Pibocella ponti.

Description of Pibocella ponti sp. nov.
Pibocella ponti (pon'ti. L. gen. n. ponti of the sea, a sea dweller).

Main characteristics are as given for the genus. In addition, cells range from 0·4 to 0·5 µm in width and from 1·6 to 2·3 µm in length. On marine agar colonies are 2–4 mm in diameter, circular, shiny, convex with entire edges, yellow in colour. Grows at 4–33 °C; optimum temperature for growth is 21–23 °C. Growth occurs at 1–13 % NaCl. Decomposes gelatin, casein, starch and Tweens 20, 40 and 80; does not hydrolyse agar, DNA, urea, cellulose (CM-cellulose and filter paper) or chitin. Forms acid from D-maltose, but not from L-arabinose, D-cellobiose, L-fucose, D-galactose, D-glucose, D-lactose, D-melibiose, L-raffinose, L-rhamnose, D-sucrose, DL-xylose, citrate, adonitol, dulcitol, glycerol, inositol or mannitol. Utilizes L-arabinose, D-glucose, D-mannose and D-sucrose, but not D-lactose, mannitol, inositol, sorbitol, malonate or citrate. Nitrate is not reduced. Indole, H2S and acetoin (Voges–Proskauer reaction) production are negative. Susceptible to ampicillin, carbenicillin, lincomycin, oleandomycin, streptomycin and tetracycline; resistant to benzylpenicillin, gentamicin, kanamycin, neomycin and polymyxin B. The predominant cellular fatty acids of KMM 6031T are branched-chain saturated and unsaturated, namely i-15 : 0 (8·7 %), a-15 : 0 (5·4 %), i-15 : 1 (11·7 %), i-16 : 1 (6·2 %), i-16 : 0 (12·1 %), i-17 : 1{omega}9c (5·2 %), i-16 : 0 3-OH (5·9 %), i-17 : 0 3-OH (5·6 %) and summed feature 3 (11·4 %), consisting of i-15 : 0 2-OH and/or 16 : 1{omega}7c. The major respiratory quinone is MK-6. The G+C content of the DNA is 35·5 mol%.

The type strain is KMM 6031T (=KCTC 12262T=NBRC 100591T=LMG 22573T), isolated from the green alga Acrosiphonia sonderi collected in Troitsa Bay, Gulf of Peter the Great, Sea of Japan.


   ACKNOWLEDGEMENTS
 
This research was supported by grants from the Federal Agency for Sciences and Innovations of the Ministry for Education and Sciences of the Russian Federation (no. 2-2.16), the Russian Foundation for Basic Research (no. 05-04-48211) and the Programme of Fundamental Investigations of the Presidium of the Russian Academy of Sciences ‘Molecular and Cell Biology’. K. H. L. and S. B. K. are also grateful for support from the KRIBB Research Initiative Programme.


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