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Reinekea marinisedimentorum gen. nov., sp. nov., a novel gammaproteobacterium from marine coastal sediments

¹ Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, 690022 Vladivostok, Prospekt 100 Let Vladivostoku, 159, Russia
² DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Mascheroder Weg 1b, D-38124 Braunschweig, Germany
³ GBF – Gesellschaft für Biotechnologische Forschung GmbH, D-38124 Braunschweig, Germany

Correspondence
Erko Stackebrandt
erko{at}dsmz.de

	ABSTRACT

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A Gram-negative, oxidase- and catalase-positive, rod-shaped bacterium, designated strain KMM 3655^T, was isolated from a coastal marine sediment sample. The novel bacterium required sodium ions for growth and grew between 0·5 and 5 % NaCl and at 4–37 °C, but not at 40 °C. It reduced nitrate, formed acids from glucose under aerobic and anaerobic conditions, utilized a limited spectrum of organic substrates and did not produce gelatinase, caseinase, amylase or chitinase. The major isoprenoid quinone was Q8. Polar lipids consisted of phosphatidylglycerol, diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylinositol and an unknown phospholipid. Fatty acid analysis of strain KMM 3655^T revealed C_{16 : 0}, C_{16 : 1}7c and C_{18 : 1}7c as predominant components. The G+C content of the DNA was 51·1 mol%. Phylogenetic analysis of the 16S rDNA sequence placed the new isolate within the -Proteobacteria as a separate deep branch, with about 90 % sequence similarity to representatives of the genus Oceanospirillum and other remotely related genera. Combined phylogenetic and physiological data show that the new marine sediment isolate, KMM 3655^T, represents a novel genus and species, for which the name Reinekea marinisedimentorum gen. nov., sp. nov. is proposed. The type strain is KMM 3655^T (=DSM 15388^T).

	MAIN TEXT

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During a survey of the biodiversity of micro-organisms that are associated with marine sediments, the Gram-negative, rod-shaped, non-pigmented bacterium KMM 3655^T was isolated from a marine coastal sediment sample and characterized by using phenotypic and phylogenetic analyses.

Sediment samples were collected from the coastal sea water area of Reineke Island, Peter the Great Bay, Sea of Japan, Russia, in June 2002. A sediment sample was obtained at a depth of 0·2 m by using a sterile tube and was serially diluted with sterile sea water. An aliquot of each dilution was spread on marine agar 2216 (MA; Difco) and incubated at 28 °C for 7 days. The bacterium was cultivated aerobically in marine broth (MB; Difco) and on MA or half-strength MA supplemented with yeast extract (0·5 %, w/v) and NaCl (1·5 %, w/v) at 35–37 °C and stored at –80 °C in liquid medium supplemented with 30 % (v/v) glycerol.

Cell morphology of cells grown on MA for 30 h was examined by transmission and scanning electron microscopy (Fig. 1). Cells were fixed with 1 % (v/v) glutaraldehyde and negatively stained with 45 % (w/v) aqueous uranyl acetate and carbon film. Samples were examined by a Zeiss model TEM910 transmission electron microscope at an acceleration voltage of 80 kV at calibrated magnifications. Gram-reaction was determined by the KOH lysis method of Gregersen (1978). Standard phenotypic properties were examined according to Smibert & Krieg (1994). Arginine dihydrolase, lysine decarboxylase and ornithine decarboxylase activities were tested by using the procedures described by Baumann et al. (1984b). Hydrolysis of starch was determined after 3 days incubation on nutrient agar medium that contained 10 % (w/v) soluble starch by flooding the plates with 1 % (w/v) iodine solution. Formation of H₂S from thiosulfate was tested with lead acetate paper. Ability to grow at different temperatures was examined on MA at 4, 10, 15, 28, 30, 35, 37, 40 and 42 °C. The pH range for growth (5·0–10·0) was tested in MB. Sodium ion requirement and tolerance of various NaCl concentrations (0–12 %) were examined on glucose/peptone medium that was prepared with an artificial sea water base, supplemented with an appropriate amount of NaCl. Leifson's oxidation/fermentation medium for marine bacteria was used for testing acid production from carbohydrates, with 1 % (w/v) of each compound (Leifson, 1963). Other biochemical tests were carried out by using API 20NE test kits (bioMérieux) according to the manufacturer's instructions, except that the culture was suspended in 2 % (w/v) NaCl solution, and by a Biolog GN MicroPlate panel. Biolog microtitre plates were inoculated with cells that were suspended in 2 % (w/v) NaCl solution. Results were read automatically with a spectrophotometer after 24 and 48 h incubation at 37 °C. For lipid analysis, the strain was cultivated on MA at 35 °C for 3 days. Whole-cell fatty acids were analysed according to Sasser (1990) and isoprenoid quinones and phospholipids were examined according to Schumann et al. (1997). DNA G+C content was determined by using the HPLC method described by Mesbah et al. (1989).

View larger version (127K): [in this window] [in a new window]   Fig. 1. Scanning electron micrographs of cells of strain KMM 3655T grown on MA for 30 h, showing (a) single cells and (b) aggregates.

View larger version (46K): [in this window] [in a new window]   Fig. 2. Dendrogram of 16S rRNA gene sequence relatedness, showing the phylogenetic position of strain KMM 3655T within the radiation of representative species of some distantly related genera of the -Proteobacteria. Numbers at branching points refer to bootstrap values (percentage of 500 resamplings). *, Branching point of strain KMM 3655T and clone 18, determined on the basis of 1000 bp, was added after generation of the branching pattern of the other reference sequences, determined on the basis of almost-complete sequences (Felsenstein, 1993). #, Sequence taken from the Ribosomal Database Project (Maidak et al., 1999). Bar, 5 inferred nucleotide substitutions per 100 nt.

View this table: [in this window] [in a new window]   Table 1. Main phenotypic characteristics that differentiate strain KMM 3655T from some marine members of the -Proteobacteria Genera and species are designated as: 1, KMM 3655T; 2, Oceanospirillum spp.; 3, Oleiphilus messinensis; 4, Ferrimonas balearica; 5, Shewanella amazonenis; 6, Shewanella algae; 7, Alteromonas spp. All bacteria are motile and negative for arginine dihydrolase production. Data were obtained from the following references: Baumann et al. (1984b), Rosselló-Mora et al. (1995), Venkateswaran et al. (1998, 1999), Golyshin et al. (2002), Mikhailov et al. (2002) and Satomi et al. (2002). +, Positive; –, negative; W, weak; V, variable reaction between strains or species of the genus; ND, not determined.

Comparative 16S rDNA gene sequence analysis data confirmed the affiliation of the new isolate to the -Proteobacteria (Fig. 2). Strain KMM 3655^T stands phylogenetically isolated, but is related remotely to members of a broad range of taxa (Oceanospirillum, Oleiphilus, Marinobacter, Alcanivorax and Vibrionaceae) (<90 % sequence similarity). Slightly different phylogenetic trees were obtained by applying different algorithms and outgroup reference organisms (not shown), but in no case was the branching pattern supported by high bootstrap values. Highest sequence similarity of strain KMM 3655^T was obtained to a partial sequence (1000 bp, GenBank no. AY172302) of an as yet uncultured organism, clone 18, which was recovered from DNA from a standard Petri dish (S. Epstein, K. Lewis and T. Kaeberlein, unpublished data) (Fig. 2).

The distinct phylogenetic position of strain KMM 3655^T is supported by its physiological and biochemical properties. The new isolate differed from marine, Gram-negative, strictly aerobic, non-fermentative, heterotrophic and halophilic -Proteobacteria that belong to the genera Alteromonas, Pseudoalteromonas (Baumann et al., 1972, 1984b; Gauthier et al., 1995), Marinomonas (Van Landschoot & De Ley, 1983), Glaciecola (Bowman et al., 1998), Idiomarina (Ivanova et al., 2000) and Thalassomonas (Macián et al., 2001) in the ability to ferment glucose anaerobically, maximum and minimum growth temperatures, narrow salinity range for growth and a limited spectrum of compounds utilized. In addition, members of the genus Idiomarina are characterized by iso-C_{15 : 0} and iso-C_{17 : 0} as major fatty acids and members of the genus Thalassomonas differ by abundance of the fatty acids C_{15 : 0}, C_{16 : 0} and C_{17 : 1}8c. The major phenotypic differences between strain KMM 3655^T and facultative anaerobes of the genus Shewanella [Shewanella algae and Shewanella amazonensis (Venkateswaran et al., 1998, 1999)], were as follows: sodium chloride concentration required for growth, minimal and maximal growth temperatures, inability to hydrolyse many compounds, assimilation pattern and fatty acid composition (Table 1). Strain KMM 3655^T is phylogenetically distant from members of the genera Vibrio (Baumann et al., 1984a), Photobacterium (Baumann & Baumann, 1984) and Aeromonas (Popoff, 1984). Representatives of these genera are able to ferment glucose, reduce nitrate and produce acid from carbohydrates, but they can be differentiated from strain KMM 3655^T by arginine dihydrolase production, broad spectrum of assimilation compounds, fatty acid composition and low DNA G+C contents for Vibrio and Photobacterium (38–51 mol% and 40–44 mol%, respectively) or high DNA G+C contents (57–63 mol%) for Aeromonas. Characteristics that differentiate strain KMM 3655^T from other marine gammaproteobacteria are listed in Table 1. Based on phenotypic, morphological and physiological dissimilarities and significant distance in 16S rRNA gene sequence, strain KMM 3655^T could not be assigned to any known species or genus within the -Proteobacteria; it is therefore proposed to classify strain KMM 3655^T as the type strain of the type species of a novel genus, Reinekea gen. nov., as Reinekea marinisedimentorum sp. nov.

Description of Reinekea gen. nov.
Reinekea (Rei.ne.ke'a. N.L. fem. n. Reinekea derived from Reineke, geographical name of Reineke Island, Peter the Great Bay, Sea of Japan, Russia, the place where the bacterium was first isolated).

Gram-negative, heterotrophic, oxidase- and catalase-positive, rod-shaped and motile. Sodium ions are essential for growth. Growth occurs in 0·5–5 % NaCl and between 4 and 37 °C. No growth is observed in >5 % NaCl or at 40 °C. Facultatively anaerobic; acid is produced from some carbohydrates under anaerobic and aerobic conditions. Predominant isoprenoid quinone is Q8. Polar lipids include phosphatidylglycerol, diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylinositol and an unknown phospholipid. Major fatty acids are C_{16 : 0}, C_{16 : 1}7c and C_{18 : 1}7c. Represents a main phylogenetic sublineage within the -Proteobacteria, showing remote relatedness to other marine and non-marine members of this class. The type species is Reinekea marinisedimentorum.

Description of Reinekea marinisedimentorum sp. nov.
Reinekea marinisedimentorum (ma.ri.ni.se.di.men.to'rum. L. adj. marinus of the sea; L. n. sedimentum settlings, sediment; N.L. gen. pl. n. marinisedimentorum from marine sediments).

In addition to properties given in the genus description, the species is characterized as follows. Cells are 0·4–0·5 µm in diameter and 1·5–1·7 µm in length. Motile by single polar flagella. Cells grown on agar slants occur singly or as cell aggregates without flagella. Gelatinase, caseinase, amylase and chitinase are not produced. Aerobic formation of acid occurs from glucose, sucrose, lactose, maltose, galactose, glycerol and mannitol; no acid is formed aerobically from arabinose, rhamnose or N-acetylglucosamine. Under anaerobic conditions, acid is produced from glucose and maltose, but not from acetate, citrate, peptone, ethanol or glycerol. Negative for arginine dihydrolase, lysine decarboxylase and ornithine decarboxylase activities. Positive for nitrate reduction, PNPG (p-nitrophenyl -D-glucopyranoside) test and utilization of D-glucose, D-mannitol and maltose, according to the API 20NE system (bioMérieux); negative for indole production, arginine dihydrolase, urease production and utilization of aesculin, gelatin, L-arabinose, D-mannose, N-acetylglucosamine, D-gluconate, caprate, adipate, L-malate, citrate and phenylacetate. Positive for D-mannitol utilization in Biolog GN tests; weakly positive for utilization of Tweens 40 and 80, L-arabinose, psicose, D-sorbitol, sucrose, -ketobutyric acid and L-alanylglycine; other organic substrates included in the Biolog GN substrate panel are not utilized. Positive for alkaline phosphatase, leucine arylamidase and naphthol-AS-BI-phosphohydrolase, according to API ZYM tests; negative for esterase C4, esterase lipase C8, lipase C14, valine arylamidase, cystine arylamidase, trypsin, -chymotrypsin, acid phosphatase, -galactosidase, -glucuronidase, -glucosidase, -glucosidase, N-acetyl--glucosaminidase, -mannosidase and -fucosidase. Major fatty acid methyl esters are C_{16 : 0} (31·61 %), C_{16 : 1}7c (26·72 %) and C_{18 : 1}7c (19·04 %); C_{15 : 0} (4·11 %), C_{17 : 0} (5·94 %), C_{14 : 0} (1·99 %), C_{14 : 0} 3-OH (2·35 %), C_{17 : 1}8c (1·29 %), C_{17 : 1}6c (1·89 %), C_{16 : 0} N alcohol (1·21 %) and C_{16 : 1}7c alcohol (1·09 %) are present as minor acids; C_{17 : 0} 10-methyl, C_{18 : 0} and C_{12 : 0} ALDE are detected at a level of <1 %. The DNA G+C content of the type strain is 51·1 mol%.

The type strain is KMM 3655^T (=DSM 15388^T). Isolated from marine coastal sediments offshore from Reineke Island, Peter the Great Bay, Sea of Japan, Russia.

	ACKNOWLEDGEMENTS

 
This study was supported by grant no. 02-04-49517 from the Russian Foundation for Basic Research and by grant no. 95-01/03-19 from the Russian State Committee for Science and Technologies. We thank Anja Frühling, Ina Kramer, Gabriele Pötter and Jolantha Swiderski for excellent technical assistance.

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