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1 Zentrum für Infektionsforschung, Universität Würzburg, Röntgenring 11, D-97070 Würzburg, Germany
2 Lehrstuhl für Organische Chemie 1, Am Hubland, D-97074 Würzburg, Germany
Correspondence
Ute Hentschel
ute.hentschel{at}mail.uni-wuerzburg.de
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ABSTRACT |
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 TOP ABSTRACT MAIN TEXTREFERENCES |
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain Pol012T is DQ302104, and those for verrucomicrobial 16S rRNA gene sequences from sponges and seawater are DQ302105–DQ302120.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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; Vandekerckhove et al., 2000). While more than 500 different verrucomicrobial 16S rRNA gene sequences have been identified using 16S rRNA gene-based techniques, only a handful of them represent cultivated strains (Schlesner, 1987; Chin et al., 2001; Joseph et al., 2003; Sangwan et al., 2004). In fact, only two marine ‘Verrucomicrobia’ species, Alterococcus agarolyticus (Shieh & Jean, 1998; Sangwan et al., 2004) and ‘Fucophilus fucoidanolyticus’ (Sakai et al., 2003), have been cultivated so far; both belong to subphylum 4. The epixenosomes, ectosymbionts of marine ciliates of the genus Euplotidium, also belong to this subphylum (Petroni et al., 2000). In addition, verrucomicrobial 16S rRNA gene sequences have been recovered from marine animals and plants (Weidner et al., 2000; Alain et al., 2002; Bowman & Nowak, 2004), from bacterioplankton (Bano & Hollibaugh, 2002; Harris et al., 2004; O'Sullivan et al., 2004), from coastal Antarctic sediments (Bowman et al., 2000; Bowman & McCuaig, 2003; Powell et al., 2003) and from seawater (Schäfer et al., 2000; Madrid et al., 2001; Suzuki et al., 2001; Bano & Hollibaugh, 2002; O'Sullivan et al., 2004). The respective organisms are mainly affiliated with subphyla 1 and 4. In this study, we describe the cultivation and analysis of strain Pol012T, the first marine member of subphylum 1 of the phylum ‘Verrucomicrobia’. In addition, 16S rRNA gene sequences of various members of the ‘Verrucomicrobia’ were isolated from sponges and seawater.
Strain Pol012T was isolated from the Mediterranean sponge Axinella polypoides on M1 agar (Mincer et al., 2002). Sponges of the species Axinella polypoides, Axinella damicornis and Aplysina aerophoba were collected by means of scuba-diving offshore from Banyuls-sur-Mer, France (42° 29' N 03° 08' E) in May 2003. Sponges of the species Agelas conifera and Aplysina fistularis were collected in July 2000 offshore from Little San Salvador Island in the Bahamas (GPS: 24° 34.39' N 75° 58.00' W) at depths of 5–15 m. Mechanical separation of the sponge tissue and storage of the bacterial cells were performed as described by Fieseler et al. (2004). For further cultivation of strain Pol012T, Verrucomicrobium spinosum medium 607 (Deutsche Sammlung von Mikroorganismen und Zellkulturen, Braunschweig, Germany) was modified to contain the following: 1.5 g yeast extract, 1.5 g peptone, 1.5 g glucose, 20 ml Hutner's basal salts solution (Cohen-Bazire et al., 1957), 5 ml Tris/HCl (1 M, pH 7.5) and 975 ml artificial seawater (ASW) (Lyman & Fleming, 1940). The new medium designed for the cultivation of marine members of the phylum ‘Verrucomicrobia’ was named ‘Ver100’. Strain Pol012T was incubated at 30 °C on plates and in liquid cultures shaken at 200 r.p.m. On the newly designed marine medium (Ver100), strain Pol012T formed soft, red colonies, while the liquid cultures were pink to red in colour. Growth was observed at temperatures between 8 and 30 °C, but not at 4 or 35 °C. Cell growth was optimal at temperatures between 25 and 30 °C. Strain Pol012T was not able to grow on Ver100 agar plates incubated in an anaerobic jar. Vitamins were not required for growth.
Strain Pol012T showed a strict requirement for seawater. Growth was possible in liquid culture with media formulations containing 60–160 % (v/v) ASW, while growth was inhibited below 40 % or above 180 % ASW. Replacement of ASW with NaCl was not possible, since no growth could be observed in medium containing 0, 200, 400, 510, 610, 800, 1070 or 1600 mM NaCl. Growth was possible at pH values between 6.8 and 8.2, but not at 6.0; pH values above 8.2 could not be measured, since unknown salts precipitated in Ver100 culture medium. The cells grew poorly on ZoBell agar (Oppenheimer & ZoBell, 1952) and slightly better on M1 agar (Mincer et al., 2002), on which strain Pol012T was originally isolated. In liquid culture, strain Pol012T was able to grow in minimal Ver100 medium (lacking peptone, yeast extract and glucose) with glucose, xylose, melibiose, cellobiose, lactose, pyruvate or pectin serving as the sole energy source. Growth was not possible with galactose, fructose, mannose, mannitol, arabinose, sucrose, ribose, sorbose, fucose, rhamnose, melitose, ethanol, methanol, glycerol, galacturonic acid, malate, tartrate, citrate, glycine, alanine, leucine, isoleucine, proline, lysine, glutamate, starch, xylan or chitin. The polysaccharides were tested at 0.1 % (w/v). All other substances were tested at a concentration of 10 mM.
For further phenotypic testing, Pol012T was grown on Ver100 agar plates for 48 h at 30 °C and resuspended in either ASW or Ver100 minimal medium. Using the API ZYM system (bioMérieux), the enzymes alkaline phosphatase, esterase (C4), esterase lipase (C8), leucine arylamidase, trypsin, acid phosphatase and naphthol-AS-BI-phosphohydrolase gave positive results. Using the API 20NE system (bioMérieux), 
-glucosidase activity on aesculin, -galactosidase activity on 4-nitrophenyl -D-galactopyranoside and oxidase activity were found. Furthermore, reduction of nitrate to nitrite was measurable. Using Biolog GN2 microplates, strain Pol012T was shown to oxidize dextrin, D-cellobiose, D-fructose, D-galactose, 
-D-glucose, D-mannose, D-melibiose, acetic acid and formic acid. Here, cells were suspended in Ver100 minimal medium to an OD600 of 0.3. All results were read after incubation at 30 °C (n=3).
Strain Pol012T was able to grow in Ver100 culture medium supplemented with vancomycin, kanamycin, streptomycin, gentamicin, neomycin or tetracycline (each at a concentration of 100 µg ml–1), but not with chloramphenicol, ampicillin, lincomycin, erythromycin or oxacillin (each at a concentration of 10 µg ml–1). Strain Pol012T was tested for antimicrobial activity against Gram-positive Staphylococcus aureus and Gram-negative Escherichia coli reference strains. Neither soft-agar overlays performed with Pol012T following growth on agar plates nor ethyl acetate extracts of liquid cultures provided evidence of antimicrobial activity.
Cells of strain Pol012T produced a red pigment that did not diffuse into the agar and which could be easily extracted with methanol or ethanol. Cell-free ethanol extracts displayed an absorption maximum at 495 nm. Cells were catalase-negative and oxidase-positive. Quinones MK-8 (23 %) and MK-9 (77 %) could be detected. This is consistent with other members of the phylum ‘Verrucomicrobia’, in which menaquinones have also been identified (Sittig & Schlesner, 1993; Hedlund et al., 1996; Sakai et al., 2003; Sangwan et al., 2004). The G+C content of the genomic DNA was 50.9 mol%. The peptidoglycan structure of strain Pol012T contained direct cross-linkages of the A1
meso-diaminopimelic acid type that is also present in ‘Chthoniobacter flavus’ from subphylum 2 of the phylum Verrrucomicrobia (Sangwan et al., 2004); meso-diaminopimelic acid has also been isolated from Prosthecobacter strains (Hedlund et al., 1996). The major cellular fatty acids were hexadecanoic acid (C16 : 0; 23 % of the total), 12-methyltridecanoic acid (i-C14 : 0; 22 % of the total), cis-9-hexadecenoic acid and/or 2-hydroxy-13-methyltetradecanoic acid (C16 : 1
7c and/or 2-OH i-C15 : 0; 21.5 % of the total), 12-methyltetradecanoic acid (a-C15 : 0; 6 % of the total) and pentadecanoic acid (C15 : 0; 4.5 % of the total). Extraction and analysis of the cellular fatty acids and the isoprenoid quinones, analysis of the peptidoglycan structure and determination of the G+C content of the genomic DNA were performed by the Deutsche Sammlung von Mikroorganismen und Zellkulturen.
Transmission electron microscopy of ultrathin sections of strain Pol012T was performed essentially as described by Pimentel-Elardo et al. (2003). For transmission electron microscopy of negatively stained whole cells, bacteria were grown in liquid culture and fixed with 2.5 % glutaraldehyde. A drop of culture was incubated on a copper grid, the liquid was removed and the cells were stained with a drop of 0.5 % uranyl acetate for 5 min. The cells were examined under an EM 10 electron microscope (Zeiss). For scanning electron microscopy, colonies with surrounding material were fixed in 6.25 % glutaraldehyde, washed three times with 0.1 M cacodylate buffer and dehydrated with increasing concentrations of acetone (from 30 to 100 %). After critical-point drying and platinum coating of the dried material, colonies were examined with a DSM 962 scanning electron microscope (Zeiss). Strain Pol012T grew in various forms including almost coccoid cells ranging from 0.5 to 1.1 µm in diameter and rod-shaped cells ranging in length from 0.6 to 1.8 µm and in width from 0.4 to 1.0 µm (Figs 1 and 2). Electron microscopic images of 35 negatively stained cells were used to measure cell size. Single cells and cell clusters were found. Cell division might occur by budding (see arrows in Fig. 1d, e). Motile cells, flagella and prosthecae were not observed. Strain Pol012T stained Gram-negative, and two separate membranes could be detected by electron microscopy (see arrow in Fig. 1b).
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, using universal bacterial primers 27f and 1492r (Lane, 1991). For the amplification of verrucomicrobial 16S rRNA genes, the ‘Verrucomicrobia’-specific forward primer Ver53F (Stevenson et al., 2004) and the reverse primer 1492r were used. Sequences were checked for chimaeras (Huber et al., 2004), and phylogenetic analyses were performed using the ARB software package (Strunk et al., 2000) after alignment of the sequences by using CLUSTAL W. All sequences contained at least 1250 nt. Phylogenetic-tree construction was performed using the neighbour-joining method with bootstrap values based on 1000 replications. Phylogenetic analysis of the 16S rRNA gene sequence of strain Pol012T revealed a sequence similarity of 83 % with respect to its closest cultured relative, Akkermansia muciniphila (Derrien et al., 2004), and a sequence similarity of 95 % with respect to the closest environmental clone, Arctic96BD-2 (Bano & Hollibaugh, 2002). It was concluded that strain Pol012T is affiliated to verrucomicrobial subphylum 1. This clade includes the freshwater isolate V. spinosum (Schlesner, 1987), four freshwater Prosthecobacter species (Hedlund et al., 1997), the human intestinal isolate Akkermansia muciniphila (Derrien et al., 2004) and several environmental 16S rRNA gene sequences. Strain Pol012T represents the first cultivated marine isolate of this subphylum (Fig. 3).
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; Vandekerckhove et al., 2000) and as being associated with marine animals and plants (Alain et al., 2002; Bowman & Nowak, 2004; Weidner et al., 2000). In this study, a novel marine isolate, strain Pol012T, was isolated from a marine sponge. In addition, several verrucomicrobial 16S rRNA gene sequences were recovered from marine sponges and seawater, thus extending the range of environmental sources from which these bacteria can be isolated.
Sponges are filter-feeders that are capable of efficiently removing bacteria and small eukaryotes from seawater and translocating the food particles into their interior, where they are digested by means of phagocytosis. Sponges are also known to contain phylogenetically complex microbial communities within their tissues: these communities can amount to up to 40 % of the animal's biomass (Hill, 2004; Hentschel et al., 2006; Scheuermayer et al., 2006). The formation of monophyletic, sponge-specific sequence clusters in at least eight different bacterial phyla has been taken as evidence of a stable, and possibly symbiotic, association between the corresponding micro-organisms and their sponge host (e.g. Hentschel et al., 2002; Fieseler et al., 2004; Montalvo et al., 2005). In contrast to previous studies on sponge–microbe associations, monophyletic cluster formation is not evident for the verrucomicrobial sequences recovered in this study (Fig. 3
; sequences indicated by diamond symbols). Instead, the Pol012T 16S rRNA gene sequence is most closely related to a seawater 16S rRNA gene sequence from the collection site (>98 % sequence similarity). Similarly, other sponge-derived verrucomicrobial 16S rRNA gene sequences were also more closely related to seawater sequences than to those from various sponges. This indicates that marine members of the phylum ‘Verrucomicrobia’ can principally be isolated from sponges, but that seawater is also a likely source for this novel clade of micro-organisms. Further investigation is needed to determine whether the association of marine strain Pol012T with Axinella polypoides is coincidental or whether Pol012T and related strains should be considered symbionts.
Description of Rubritalea gen. nov.
Rubritalea (Ru.bri.ta'lea. L. adj. ruber red; L. fem. n. talea a rod, staff; N.L. fem. n. Rubritalea a red-coloured rod).
Cells are Gram-negative, non-motile, coccoid or rod-shaped, obligately marine and red in colour. Metabolism is aerobic and chemo-organotrophic.
Description of Rubritalea marina sp. nov.
Rubritalea marina (ma.ri'na. L. fem. adj. marina of or belonging to the sea, marine).
Cells are Gram-negative, non-motile, coccoid or rod-shaped, and red in colour. Able to grow with glucose, xylose, melibiose, cellobiose, lactose, pyruvate or pectin as the sole energy source under aerobic conditions. Does not grow anaerobically. The DNA G+C content is 50.9 mol%. The major cellular fatty acids are hexadecanoic acid, 12-methyltridecanoic acid, cis-9-hexadecenoic acid and/or 2-hydroxy-13-methyltetradecanoic acid, 12-methyltetradecanoic acid and pentadecanoic acid. Menaquinones MK-8 and MK-9 are present. The peptidoglycan of the cell wall contains direct cross-linkages of the A1 meso-diaminopimelic acid type. Strain Pol012T tests negative for catalase and positive for oxidase, alkaline phosphatase, esterase (C4), esterase lipase (C8), leucine arylamidase, trypsin, acid phosphatase, naphthol-AS-BI-phosphohydrolase, -glucosidase and -galactosidase. Strain Pol012T is capable of nitrate reduction to nitrite and oxidation of dextrin, D-cellobiose, D-fructose, D-galactose, -D-glucose, D-mannose, D-melibiose, acetic acid and formic acid. Strain Pol012T is able to grow in medium containing 60–160 % ASW, at pH values between 6.8 and 8.2 and at temperatures between 8 and 30 °C.
The type strain, Pol012T (=DSM 177716T=CIP 108984T), was isolated from the Mediterranean sponge Axinella polypoides.
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ACKNOWLEDGEMENTS |
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