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Reichenbachia agariperforans gen. nov., sp. nov., a novel marine bacterium in the phylum Cytophaga–Flavobacterium–Bacteroides

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 Tokyo Research Laboratories, Kyowa Hakko Kogyo Co Ltd, 3-6-6 Asahi-machi, Machida-shi, Tokyo 194-8533, Japan
³ Institute of Marine Biology of the Far-Eastern Branch of the Russian Academy of Sciences, Pal'chevskogo St 17, 690032, Vladivostok, Russia

Correspondence
Makoto Suzuki
makoto.suzuki{at}kyowa.co.jp

	ABSTRACT

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A heterotrophic, pigmented, agarolytic, gliding bacterium was isolated from a seawater sample collected from the Gulf of Peter the Great, Sea of Japan, during June 2000. 16S rDNA sequence analysis indicated that the novel bacterium, strain KMM 3525^T, was a member of the phlyum Cytophaga–Flavobacterium–Bacteroides. On the basis of phenotypic, chemotaxonomic, genotypic and phylogenetic data, it is proposed that the marine bacterium represents the sole species of a novel genus, Reichenbachia, the type species of which is Reichenbachia agariperforans (KMM 3525^T =IFO 16625^T =JCM 11238^T).

The GenBank accession number for the 16S rDNA sequence of Reichenbachia agariperforans KMM 3525^T is AB058919.

	MAIN TEXT

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Gliding, Gram-negative, heterotrophic bacteria are widely distributed in marine coastal ecosystems. Historically, bacteria belonging to the phylum Cytophaga–Flavobacterium–Bacteroides (CFB) have been poorly investigated in terms of their phylogeny. During the last decade, many novel taxa belonging to the phylum CFB have been described, and some bacterial species that previously had unclear taxonomic positions within this phylum have been reclassified due to the use of a polyphasic taxonomic approach. Descriptions of genera such as Polaribacter, Gelidibacter, Psychroserpens, Psychroflexus and Salegentibacter have resulted from intensive studies into the microbial communities of Antarctic seas and hypersaline lakes (Gosink et al., 1998; Bowman et al., 1997, 1998; McCammon & Bowman, 2000). Novel bacteria have also been found in shore marine waters in temperate latitudes, and the novel genera Cellulophaga, Tenacibaculum and Arenibacter have been created for these organisms (Johansen et al., 1999; Suzuki et al., 2001; Ivanova et al., 2001). However, many other taxa belonging to the phylum CFB remain to be described. In this study, we have characterized a novel bacterium, strain KMM 3525^T, which was isolated from a seawater sample. On the basis of the results of a polyphasic taxonomic study (i.e. phylogenetic, phenotypic and genotypic analyses, and analyses of menaquinone and cellular fatty acid compositions) on this novel bacterium, we describe a novel genus of the phylum CFB, Reichenbachia, the type species of which is Reichenbachia agariperforans.

Agarolytic strain KMM 3525^T was isolated from a seawater sample collected in the Amursky Bay of the Gulf of Peter the Great, Sea of Japan, during June 2000. The strain was cultured on Marine Agar 2216E (Difco). Flexirubin pigments of the strain were determined by the method of Fautz & Reichenbach (1980). Determinations for the degradation of alginic acids (1 %, w/v) and agar (1·5 %, w/v), growth at different temperatures, NaCl concentrations or pH, production of acid from carbohydrates, and hydrolysis of starch, casein, gelatin, cellulose [carboxymethylcellulose (CM-cellulose) and filter paper], DNA and urea by strain KMM 3525^T were carried out according to the methods of Smibert & Krieg (1994). Hydrolysis of chitin (1 %, w/v) by strain KMM 3525^T was determined by the appearance of clear zones around colonies on chitin agar. Susceptibility of the novel strain to antibacterials was examined by the routine disc-diffusion plate method. Discs were impregnated with the following antibacterials: ampicillin (10 µg); benzylpenicillin (10 µg); carbenicillin (100 µg); gentamicin (10 µg); kanamycin (30 µg); lincomycin (15 µg); neomycin (30 µg); oleandomycin (15 µg); polymyxin B (300 U); streptomycin (10 µg); tetracycline (30 µg).

The analysis of fatty acid methyl esters of the novel strain was performed by GLC (30 mx0·25 mm Supelcowax 10 column, 205 °C) as described by Svetashev et al. (1995). Isoprenoid quinones were extracted and analysed by the method of Nakagawa & Yamasato (1993). DNA was isolated from strain KMM 3525^T following the method of Marmur (1961) and the G+C content (mol%) of the DNA was determined by the thermal denaturation method (Marmur & Doty, 1962). The 16S rRNA gene sequence of strain KMM 3525^T was determined by PCR amplification and direct sequencing (Hiraishi, 1992). Conditions and reagents used for PCR amplification and sequencing of the 16S rDNA have been described previously (Suzuki et al., 2001). The 16S rDNA sequence of strain KMM 3525^T was aligned with sequences retrieved from the databases by using CLUSTAL W (Thompson et al., 1994). The aligned sequences were modified manually according to the secondary structure of the Escherichia coli 16S rRNA gene sequence (Gutell et al., 1994). The regions in which the secondary structure of the rRNA of the analysed strains varied (positions 194–220, 450–487, 1284–1289, E. coli numbering system) and the sequences before position 111 and after position 1376, for which sequences of some reference organisms had not been determined, were excluded from the analysis. Evolutionary distances were then computed by using DNADIST contained within the PHYLIP package (version 3.572; Felsenstein, 1995) with the Kimura two-parameter correction (Kimura, 1980), and the phylogenetic tree was constructed by using the neighbour-joining method (Saitou & Nei, 1987). To evaluate the stability of the phylogenetic tree, a bootstrap analysis (1000 replications) was performed with the SEQBOOT and CONSENSE programs contained within the PHYLIP package (version 3.572).

Strain KMM 3525^T was a Gram-negative, chemo-organotrophic bacterium with a respiratory-type metabolism. It was motile by gliding and appeared as single, flexible rods of 0·5–0·7 µm in diameter and 5–15 µm in length. On marine agar, colonies were round, 3–5 mm in diameter, orange-pigmented and formed deep hollows in agar plates. The organism had no known resting stages. Strain KMM 3525^T was oxidase-, catalase- and alkaline-phosphatase-positive, and required Na⁺ ions for growth. Growth of the organism occurred in media containing 1–6 % NaCl. The temperature range for growth was 4–35 °C, with optimum growth occurring at 28 °C. The pH range for growth was 5·5–10·0, with optimum growth occurring between pH 7·5 and 8·5. Flexirubin pigments were formed by the novel bacterium. Agar, starch, alginate, gelatin, Tween 20, DNA and urea were degraded by strain KMM 3525^T, but cellulose (CM-cellulose and filter paper), chitin, casein, Tween 40, Tween 60 and Tween 80 were not hydrolysed by the strain. H₂S and indole were not produced by the bacterium and it formed no acid from arabinose, galactose, glucose, lactose, maltose, melibiose, rhamnose, sucrose, xylose, adonitol, dulcitol, inositol or mannitol. Utilization of citrate, fumarate and malate as sole carbon sources was not observed. Nitrate reduction was negative. Strain KMM 3525^T was susceptible to carbenicillin, oleandomycin, lincomycin and tetracycline, but it was not susceptible to ampicillin, benzylpenicillin, streptomycin, gentamicin, neomycin or polymyxin B. Predominant cellular fatty acids were straight-chain unsaturated and branched-chain saturated, namely C_{i15 : 0} (55·6 %) and C_{16 : 1(n-7)} (23·7 %) fatty acids. The DNA G+C content of the novel strain was 44·5 mol%, as determined by the thermal denaturation method.

A phylogenetic analysis of the 16S rDNA sequence data revealed that strain KMM 3525^T formed a distinct lineage within the phylum CFB and belonged to a cluster containing Persicobacter diffluens and marine flexibacteria (Fig. 1), but this was without significant bootstrap support. The members of this cluster share many phenotypic traits. Features useful for distinguishing strain KMM 3525^T from related members of the phylum CFB are listed in Table 1. The marine flexibacteria were separated from the genus Flexibacter and placed into the genus Microscilla by Pringsheim (1951); the taxonomy of this polyphyletic group was studied by Lewin (1969). More recently, on the basis of 16S rRNA gene sequence data, Nakagawa et al. (1997) have suggested that the genus Microscilla be restricted to a single species, Microscilla marina, the type species and only member of this taxon, which occupies a separate phylogenetic lineage within the phylum CFB. The taxonomic positions of other species of marine flexibacteria belonging to different rDNA branches are unclear and need further investigation (Bernardet et al., 1996; Nakagawa et al., 1997; Sly et al., 1998). The 16S rDNA sequence of strain KMM 3525^T was most similar to that of ‘Microscilla sericea’ (89·5 %). Its level of 16S rDNA sequence similarity with other members of the phylum CFB ranged from 79·1 to 89·1 %. Such low levels of sequence similarity of strain KMM 3525^T with other marine flexibacteria clearly demonstrate that the novel bacterium described in this study represents a novel genus within the phylum CFB. This conclusion, supported by the polyphasic data presented in this study, demonstrates that strain KMM 3525^T could not be assigned to any of the currently recognized genera included in the phylum CFB. Thus, we propose that strain KMM 3525^T be placed into a novel genus, Reichenbachia, as Reichenbachia agariperforans.

View larger version (61K): [in this window] [in a new window]   Fig. 1. Phylogenetic relationship of Reichenbachia agariperforans KMM 3525T with other species of the phylum CFB on the basis of 16S rDNA sequence comparisons. The phylogenetic tree was generated by the neighbour-joining method (Saitou & Nei, 1987), and the 16S rDNA sequence of Rhodothermus marinus was used as the outgroup. The numbers shown at the nodes indicate the percentage bootstrap values (based on 1000 replications; only values of 70 % are shown). Bar, genetic distance of 0·02 (Knuc).

Rod-shaped cells with gliding motility. Gram-negative. Does not form endospores or resting stages. Requires Na⁺ ions for growth. Strictly aerobic. Produces non-diffusible orange pigment. Flexirubins are synthesized. Chemo-organotroph. Cytochrome-oxidase-, catalase- and alkaline-phosphatase-positive. Major respiratory quinone is MK-7. The main cellular fatty acids are straight-chain unsaturated and branched-chain saturated fatty acids, C_{i15 : 0} and C_{16 : 1(n-7)}. As determined by 16S rDNA sequence analysis, the genus Reichenbachia is a member of the phylum CFB. The type species is Reichenbachia agariperforans.

Description of Reichenbachia agariperforans sp. nov
Reichenbachia agariperforans [a.ga.ri.per.fo'rans. Malayan n. agar agar; N.L. n. agarum agar (algal polysaccharide); L. part. adj. perforans perforating (making holes); N.L. part. adj. agariperforans making holes in agar, bacterium making deep hollows in agar].

Main characteristics are those given for the genus. In addition to the above data, cells are 0·5–0·7 µm in width and 5–15 µm in length. Colonies are 3–5 mm in diameter, circular, sunken into agar and shiny with entire edges on solid media containing high-nutrient components. Growth occurs at 4–35 °C; optimal temperature range for growth is 25–28 °C. Growth occurs in presence of 1–6 % NaCl. Decomposes agar, starch, alginate, gelatin, DNA, urea and Tween 20. Does not hydrolyse cellulose (CM-cellulose and filter paper), chitin, casein, Tween 40, Tween 60 or Tween 80. Forms no acid from arabinose, galactose, glucose, lactose, maltose, melibiose, rhamnose, sucrose, xylose, adonitol, dulcitol, inositol or mannitol. Does not utilize citrate, fumarate or malate. Nitrate is not reduced. Does not produce H₂S or indole. DNA G+C content is 44·5 mol%. Type strain is KMM 3525^T (=IFO 16625^T =JCM 11238^T). Isolated from a seawater sample collected in the Amursky Bay of the Gulf of Peter the Great, Sea of Japan.

	ACKNOWLEDGEMENTS

 
We gratefully thank Dr Chantal Bizet (Collection de Bacteries de l'Institute Pasteur, Paris, France) and Dr Danielle Janssens (Culture Collection of the Laboratory of Microbiology, University of Gent, Belgium) for the type strains used in this study. This research was supported by grants from the Foundation of the Ministry for Industry and Science of the Russian Federation (MIS RF) (95-01/03-19), the Biodiversity Programme of the Russian Academy of Science and MIS RF, and the Russian Foundation for Basic Research (02-04-49517).

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				O. I. Nedashkovskaya, S. B. Kim, A. M. Lysenko, M. S. Park, V. V. Mikhailov, K. S. Bae, and H. Y. Park Roseivirga echinicomitans sp. nov., a novel marine bacterium isolated from the sea urchin Strongylocentrotus intermedius, and emended description of the genus Roseivirga Int J Syst Evol Microbiol, September 1, 2005; 55(5): 1797 - 1800. [Abstract] [Full Text] [PDF]

				L. A. O'Sullivan, J. Rinna, G. Humphreys, A. J. Weightman, and J. C. Fry Fluviicola taffensis gen. nov., sp. nov., a novel freshwater bacterium of the family Cryomorphaceae in the phylum 'Bacteroidetes' Int J Syst Evol Microbiol, September 1, 2005; 55(5): 2189 - 2194. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, M. Vancanneyt, P. Dawyndt, K. Engelbeen, K. Vandemeulebroecke, I. Cleenwerck, B. Hoste, J. Mergaert, T.-L. Tan, G. M. Frolova, et al. Reclassification of [Cytophaga] marinoflava Reichenbach 1989 as Leeuwenhoekiella marinoflava gen. nov., comb. nov. and description of Leeuwenhoekiella aequorea sp. nov. Int J Syst Evol Microbiol, May 1, 2005; 55(3): 1033 - 1038. [Abstract] [Full Text] [PDF]

				J.-H. Yoon, S.-J. Kang, C.-H. Lee, and T.-K. Oh Marinicola seohaensis gen. nov., sp. nov., isolated from sea water of the Yellow Sea, Korea Int J Syst Evol Microbiol, March 1, 2005; 55(2): 859 - 863. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, S. K. Han, C. Snauwaert, M. Vancanneyt, J. Swings, K.-O. Kim, A. M. Lysenko, M. Rohde, G. M. Frolova, et al. Winogradskyella thalassocola gen. nov., sp. nov., Winogradskyella epiphytica sp. nov. and Winogradskyella eximia sp. nov., marine bacteria of the family Flavobacteriaceae Int J Syst Evol Microbiol, January 1, 2005; 55(1): 49 - 55. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, K. H. Lee, K. S. Bae, G. M. Frolova, V. V. Mikhailov, and I. S. Kim Pibocella ponti gen. nov., sp. nov., a novel marine bacterium of the family Flavobacteriaceae isolated from the green alga Acrosiphonia sonderi Int J Syst Evol Microbiol, January 1, 2005; 55(1): 177 - 181. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, A. M. Lysenko, G. M. Frolova, V. V. Mikhailov, K. H. Lee, and K. S. Bae Description of Aquimarina muelleri gen. nov., sp. nov., and proposal of the reclassification of [Cytophaga] latercula Lewin 1969 as Stanierella latercula gen. nov., comb. nov. Int J Syst Evol Microbiol, January 1, 2005; 55(1): 225 - 229. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, D. H. Lee, A. M. Lysenko, L. S. Shevchenko, G. M. Frolova, V. V. Mikhailov, K. H. Lee, and K. S. Bae Roseivirga ehrenbergii gen. nov., sp. nov., a novel marine bacterium of the phylum 'Bacteroidetes', isolated from the green alga Ulva fenestrata Int J Syst Evol Microbiol, January 1, 2005; 55(1): 231 - 234. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, A. M. Lysenko, V. V. Mikhailov, K. S. Bae, and I. S. Kim Salegentibacter mishustinae sp. nov., isolated from the sea urchin Strongylocentrotus intermedius Int J Syst Evol Microbiol, January 1, 2005; 55(1): 235 - 238. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, K. H. Lee, V. V. Mikhailov, and K. S. Bae Gillisia mitskevichiae sp. nov., a novel bacterium of the family Flavobacteriaceae, isolated from sea water Int J Syst Evol Microbiol, January 1, 2005; 55(1): 321 - 323. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, A. M. Lysenko, G. M. Frolova, V. V. Mikhailov, and K. S. Bae Bizionia paragorgiae gen. nov., sp. nov., a novel member of the family Flavobacteriaceae isolated from the soft coral Paragorgia arborea Int J Syst Evol Microbiol, January 1, 2005; 55(1): 375 - 378. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, A. M. Lysenko, G. M. Frolova, V. V. Mikhailov, K. S. Bae, D. H. Lee, and I. S. Kim Gramella echinicola gen. nov., sp. nov., a novel halophilic bacterium of the family Flavobacteriaceae isolated from the sea urchin Strongylocentrotus intermedius Int J Syst Evol Microbiol, January 1, 2005; 55(1): 391 - 394. [Abstract] [Full Text] [PDF]

				S. Van Trappen, I. Vandecandelaere, J. Mergaert, and J. Swings Algoriphagus antarcticus sp. nov., a novel psychrophile from microbial mats in Antarctic lakes Int J Syst Evol Microbiol, November 1, 2004; 54(6): 1969 - 1973. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, M. Suzuki, M. Vancanneyt, I. Cleenwerck, A. M. Lysenko, V. V. Mikhailov, and J. Swings Zobellia amurskyensis sp. nov., Zobellia laminariae sp. nov. and Zobellia russellii sp. nov., novel marine bacteria of the family Flavobacteriaceae Int J Syst Evol Microbiol, September 1, 2004; 54(5): 1643 - 1648. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, M. Vancanneyt, S. Van Trappen, K. Vandemeulebroecke, A. M. Lysenko, M. Rohde, E. Falsen, G. M. Frolova, V. V. Mikhailov, and J. Swings Description of Algoriphagus aquimarinus sp. nov., Algoriphagus chordae sp. nov. and Algoriphagus winogradskyi sp. nov., from sea water and algae, transfer of Hongiella halophila Yi and Chun 2004 to the genus Algoriphagus as Algoriphagus halophilus comb. nov. and emended descriptions of the genera Algoriphagus Bowman et al. 2003 and Hongiella Yi and Chun 2004 Int J Syst Evol Microbiol, September 1, 2004; 54(5): 1757 - 1764. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, M. Suzuki, M. Vancanneyt, I. Cleenwerck, N. V. Zhukova, M. V. Vysotskii, V. V. Mikhailov, and J. Swings Salegentibacter holothuriorum sp. nov., isolated from the edible holothurian Apostichopus japonicus Int J Syst Evol Microbiol, July 1, 2004; 54(4): 1107 - 1110. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, S. K. Han, A. M. Lysenko, V. V. Mikhailov, and K. S. Bae Arenibacter certesii sp. nov., a novel marine bacterium isolated from the green alga Ulva fenestrata Int J Syst Evol Microbiol, July 1, 2004; 54(4): 1173 - 1176. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, S. K. Han, M.-S. Rhee, A. M. Lysenko, M. Rohde, N. V. Zhukova, G. M. Frolova, V. V. Mikhailov, and K. S. Bae Algibacter lectus gen. nov., sp. nov., a novel member of the family Flavobacteriaceae isolated from green algae Int J Syst Evol Microbiol, July 1, 2004; 54(4): 1257 - 1261. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, M. Suzuki, A. M. Lysenko, C. Snauwaert, M. Vancanneyt, J. Swings, M. V. Vysotskii, and V. V. Mikhailov Cellulophaga pacifica sp. nov. Int J Syst Evol Microbiol, March 1, 2004; 54(2): 609 - 613. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, S. K. Han, M. S. Rhee, A. M. Lysenko, E. Falsen, G. M. Frolova, V. V. Mikhailov, and K. S. Bae Ulvibacter litoralis gen. nov., sp. nov., a novel member of the family Flavobacteriaceae isolated from the green alga Ulva fenestrata Int J Syst Evol Microbiol, January 1, 2004; 54(1): 119 - 123. [Abstract] [Full Text] [PDF]

				O. I. Nedashkovskaya, S. B. Kim, S. K. Han, A. M. Lysenko, M. Rohde, N. V. Zhukova, E. Falsen, G. M. Frolova, V. V. Mikhailov, and K. S. Bae Mesonia algae gen. nov., sp. nov., a novel marine bacterium of the family Flavobacteriaceae isolated from the green alga Acrosiphonia sonderi (Kutz) Kornm Int J Syst Evol Microbiol, November 1, 2003; 53(6): 1967 - 1971. [Abstract] [Full Text] [PDF]

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