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1 Department of Biomedical Sciences, University of Maryland at Baltimore, 666 W. Baltimore Street, Baltimore, MD 21201, USA
2 Center of Marine Biotechnology, University of Maryland Biotechnology Institute, 701 East Pratt Street, Baltimore, MD 21202, USA
Correspondence
Marcie L. Baer
mlbaer{at}ship.edu
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; Snyder et al., 2002). This has resulted in reclassification of Bdellovibrio stolpii and Bdellovibrio starrii into the newly constructed genus Bacteriovorax (Baer et al., 2000). In this study, examination of marine isolates of Bdellovibrio (designated SJT, AQ and JS5T) has revealed them to be related more closely to the newly designated genus Bacteriovorax. Phylogenetic analysis of 16S rRNA gene sequences revealed that marine isolates SJT, AQ and JS5T clustered in a separate clade from Bdellovibrio bacteriovorus 100T as part of the clade that contains Bacteriovorax spp., indicating a much closer taxonomic relationship to the latter. DNA–DNA hybridization experiments also demonstrated <5 % similarity between Bdellovibrio bacteriovorus 100T and the marine isolates. Distinct differences between the salt-water group and Bdellovibrio spp. were also observed by determination of DNA G+C content, salinity growth testing and antibiotic sensitivity analysis. On the basis of the results from the studies described above, it is proposed that marine isolates SJT (=ATCC BAA-682T=DSM 15412T) and JS5T (=ATCC BAA-684T=DSM 15409T) should be classified within the genus Bacteriovorax as the type strains of Bacteriovorax marinus sp. nov. and Bacteriovorax litoralis sp. nov., respectively.
Published online ahead of print on 3 October 2003 as DOI 10.1099/ijs.0.02458-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of Bacteriovorax marinus SJT, Bacteriovorax marinus AQ and Bacteriovorax litoralis JS5T are AF084854, AF084855 and AF084859, respectively.
Present address: Shippensburg University, Biology Department, 1871 Old Main Drive, Shippensburg, PA 17257, USA. 
Present address: The Institute for Genomic Research, 9712 Medical Center Drive, Manassas, VA 20850, USA.
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), two groups of Bdellovibrio were recognized. The freshwater/terrestrial group can only tolerate sodium chloride concentrations of <0·5 % and is found in soil and freshwater (Varon & Shilo, 1968). Marine or halophilic organisms require sodium chloride at concentrations of >0·5 % and are found in oceans, seas, estuaries and other salt or brackish waters (Taylor et al., 1974; Marbach et al., 1976; Williams, 1979, 1987; Williams & Falkler, 1984; Sutton & Besant, 1994). In addition, marine bdellovibrios have DNA G+C contents of <38 mol% (Schoeffield, 1990), whereas those of freshwater/terrestrial organisms range from 47 to 51 mol% (Seidler et al., 1972; Marbach et al., 1976). The DNA G+C contents of members of the genus Bacteriovorax (Baer et al., 2000) that were classified previously as Bdellovibrio range from 41 to 44 mol% (Seidler et al., 1972). Few studies have described the properties of the marine bdellovibrios (Taylor et al., 1974; Marbach et al., 1976; Sutton & Besant, 1994) and these have typically included a limited number of characters, as traditional laboratory-based tests cannot be used to characterize the predators because they do not grow in pure culture. The most common properties that are used to distinguish the predators are those in which BALO can be grown with their prey and include salinity and temperature growth ranges and prey susceptibility patterns. Although marine and terrestrial predators are quite distinct in these properties and their DNA G+C content, they have continued to be assigned to the same genus, Bdellovibrio. This suggests, misleadingly, that they are closely related and share many similar properties. In this study, we have shown that marine and terrestrial Bdellovibrio sp. are genetically and phenotypically diverse, as shown by comparison of 16S rDNA sequences, DNA–DNA similarity studies, determination of DNA G+C content and culture-based methods. We report the first evaluation of the taxonomic classification for three marine isolates (SJT, AQ and JS5T) of Bdellovibrio.
Strains AQ, SJT and JS5T were isolated by Schoeffield (1990) from water samples from the National Aquarium in Baltimore, St John's Island in the Caribbean and the Chesapeake Bay estuary, respectively. Marine, prey-dependent (PD) strains were grown in prey/sea water (PS) medium with Vibrio parahaemolyticus P-5 (Williams, 1987; Schoeffield, 1990; Williams et al., 1995), whilst freshwater/terrestrial PD strains were grown in dilute nutrient broth (DNB) medium (Starr & Seidler, 1971) with Escherichia coli ML35. Prey-independent (PI) mutants were isolated from wild-type PD cultures by using the methods described by Seidler & Starr (1969) for freshwater/terrestrial strains or by Schoeffield (1990) for marine strains. Suspensions of PD isolates were prepared by filtration through a 0·3 µm filter (Millipore) for marine strains or a 0·45 µm filter (Nucleopore) for freshwater/terrestrial strains. After centrifugation at 27 000 g for 60 min, predator cells were resuspended in sterile 70 % artificial sea water (ASW) or DNB for marine and freshwater/terrestrial strains, respectively. Predator concentrations (cells ml–1) were determined by the acridine orange direct-count method (Hobbie et al., 1977). Bdellovibrio genomic DNA was purified by CsCl density gradients that were prepared as described by Ausubel et al. (1987). 16S rRNA genes were amplified by using primers 8–27F (5'-AGAGTTTGATCCTGGCTCAG-3', modified from FD1) (Weisburg et al., 1991) and 1492R (5'-GGTTACCTTGTTACGACTT-3'; Weisburg et al., 1991; Reysenbach et al., 1992). Both strands of the resulting amplicon from each isolate were sequenced completely and aligned with sequences that were published previously for members of the genus Bacteriovorax and closely related micro-organisms (Baer et al., 2000) by using the PHYDIT program (Chun, 1995). Evolutionary trees were inferred by using four treeing algorithms that are implemented in the PHYLIP package: Fitch–Margoliash (Fitch & Margoliash, 1967), maximum-likelihood (Felsenstein, 1981; Olsen et al., 1994), maximum-parsimony (Kluge & Farris, 1969) and neighbour-joining (Saitou & Nei, 1987). Evolutionary distance matrices for the neighbour-joining and Fitch–Margoliash methods were generated by the method of Jukes & Cantor (1969). The final unrooted tree (Fig. 1) was evaluated by neighbour-joining bootstrap analyses, based on 1000 reassembled datasets. 16S rRNA gene sequences for isolates SJT (GenBank accession no. AF084854), AQ (AF084855) and JS5T (AF084859) were compared with the sequences for Bdellovibrio bacteriovorus 100T (AF084850, a gift from J. Tudor), Bacteriovorax stolpii Uki2T=ATCC 27052T (M34125) and Bacteriovorax starrii A3.12T=ATCC 15145T (AF084852) in GenBank. Subsequently, a similarity analysis was performed to compare the BALO 16S rDNA sequences with those of related taxa in the 
-Proteobacteria. The level of similarity found between 1155 nucleotide sites of Bdellovibrio bacteriovorus 100T and marine isolates SJT, AQ and JS5T was 81·7, 81·8 and 81·5 %, respectively. Bdellovibrio bacteriovorus 100T had greater similarity to other genera in the -Proteobacteria, such as Desulfovibrio desulfuricans, 82·1 %; Myxococcus xanthus, 83·5 %; Geobacter metallireducens, 84·7 % and Desulfomonile tiedjei, 85·1 %. In contrast, 16S rDNA sequence similarity between the marine isolates (SJT and JS5T) and Bacteriovorax stolpii Uki2T was significantly higher (91·0 and 91·1 %, respectively). Similarity values between the marine isolates and Bacteriovorax starrii A3.12T ranged from 88·6 (JS5T) to 88·8 (SJT) %. Similarity between SJT and JS5T was determined to be much higher (>93 %). The distant relationship between the marine isolates and other Bdellovibrio spp. is apparent from the unrooted evolutionary tree (Fig. 1). The marine isolates did not cluster with the Bdellovibrio bacteriovorus clade, but within a larger group that is divided into two branches, one of which contains Bacteriovorax spp. and the second the marine strains. Data generated by the maximum-parsimony, maximum-likelihood and Fitch–Margoliash methods produced similar results.
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) with [
-32P]dCTP-labelled probes on membranes (Denhardt, 1966). Intensity of hybridization was measured by using a STORM 840 PhosphoImager (Perkin-Elmer). Reciprocal experiments were performed for each pair of strains. DNA–DNA hybridization results revealed low similarity (<3·5 %) between Bdellovibrio bacteriovorus 100T [and also strains 109J (a gift from M. Thomashow) and 2484Se2 (=ATCC 25635)] and marine isolate SJT. Bdellovibrio bacteriovorus strains E (=ATCC 25634) and Ox9-2 (=ATCC 25635) showed a slightly higher degree of DNA–DNA similarity to SJT (5·7 and 5·2 %, respectively). Marine isolate JS5T also demonstrated low similarity (<3·6 %) to all Bdellovibrio bacteriovorus strains (100T, 109J, Ox9-2, E and 2484Se2). A previous study (Baer et al., 2000) demonstrated low similarity (<4 %) between strains of Bdellovibrio bacteriovorus and the Bacteriovorax species (<3–4 %). Isolate SJT demonstrated slightly higher similarity to Bacteriovorax stolpii Uki2T and Bacteriovorax starrii A3.12T (7·7 and 3·5 %, respectively). DNA–DNA similarity between JS5T and Bacteriovorax species was slightly lower (4·9 and 3·1 %, respectively).
The DNA G+C content of PI isolates AQ and SJT was determined by thermal melting curves (Schoeffield, 1990). The HPLC method was used for PD isolate JS5T (Mesbah et al., 1989). The DNA G+C contents of SJT, AQ and JS5T were 37·7, 38·3 and 37·8 mol%, respectively; these values are lower than the range of 47–51 mol% that has been reported for freshwater/terrestrial Bdellovibrio (Seidler et al., 1972; Marbach et al., 1976) and also than the range for the genus Bacteriovorax (41–44 mol%) (Seidler et al., 1972).
Comparisons of the phenotypic properties of the marine and terrestrial Bdellovibrio strains confirmed the differences that were revealed by molecular methods. The enzymic reactions of each PD isolate and its PI derivative were examined by using the API ZYM test system (bioMérieux), according to the manufacturer's recommendations. The results reported in Table 1 were consistent for both PI and PD isolates, except where noted. Of the 19 enzyme substrates against which the isolates were tested, only four (valine and cystine aminopeptidases, trypsin and chymotrypsin) yielded differential reactions (Table 1). Reactions to valine and chymotrypsin differentiated salt-water from freshwater Bdellovibrio. A positive reaction for cystine differentiated isolates SJT and 109J (negative). Isolates AQ and JS5T yielded variable results. Lack of trypsin activity distinguished the estuarine isolate, JS5T, from all other isolates, which were positive.
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) and, for PI strains, by the typical spread-plate method, as described by Guether & Williams (1993). Freshwater/terrestrial PD strains were tested on dilute (1/10) PYE (peptone/yeast extract) medium with E. coli ML35 as prey. For marine Bdellovibrio, dilute (1/10) SWYE (sea water/yeast extract/agar) medium was used with the prey, V. parahaemolyticus P-5. A second prey, Pseudomonas fluorescens, was used for testing both marine and terrestrial PD strains. The antibiotics tested are listed in Table 1
. A resistant reaction was observed by growth of the predators up to the disc, as indicated by clearing or lysis of the prey lawn. In a sensitive reaction, the predators did not grow to the edge of the discs and there remained a turbid zone of prey cell growth. Control tests with only the prey lawn and without the predators were included. Tests were repeated three times for each isolate. The results reported in this study represent antibiotic susceptibilities that were consistent for both PD and PI isolates. The results revealed that susceptibility to methicillin yielded a clear distinction between marine (resistant) and freshwater (susceptible) BALO strains. Kanamycin was observed to distinguish between isolates SJT (susceptible) and JS5T (resistant). No difference was found between the pattern susceptibilities of isolates SJT and AQ (Table 1).
The temperature growth range for each isolate was determined. For PD strains, double-agar overlay plates were incubated in humidified chambers for up to 2 weeks at 10, 15, 20, 25, 30, 35 and 40 °C. Plates incubated at 10 and 15 °C were incubated for up to 2 months. For these plates, the prey cell concentration in the top agar was increased to compensate for the slower growth rate of the prey. Mean plaque count and standard deviation (SD) were calculated from three replicate experiments. For testing PI strains, suspensions were prepared in sterile 70 % ASW for marine isolates and sterile distilled water for freshwater/terrestrial strains. Aliquots of the suspensions (0·1 ml) were spread-plated onto SWYE agar or PYE agar. Plates were incubated under the same conditions and mean counts were calculated, as for the PD predators. The results revealed that the temperature growth range was 15–35 °C for freshwater strains (with a few exceptions), 15–30 °C for marine strains AQ and SJT and 15–35 °C for isolate JS5T (Table 1).
Salinity growth range is not only a distinctive feature between marine and terrestrial BALO, but also among marine isolates. Those organisms that were isolated from the upper and mid-regions of the Chesapeake Bay estuary, where salinities range from 0·5 to 2 %, tended to grow at lower salinities than isolate SJT, which was recovered from ocean waters (salinity of approximately 3 %). Differences between ocean and estuarine isolates were also revealed by 16S rDNA sequence analysis. These differences warrant the separation of these organisms into different species within the same genus.
The results of this study provide conclusive evidence that the genus Bdellovibrio consists of molecularly diverse groups of micro-organisms that are not related closely to each other. The use of a predatory lifestyle as the sole criterion for classification of these organisms has resulted in the inclusion of phylogenetically diverse groups within the same genus. A change in the taxonomic status of marine Bdellovibrio is clearly warranted, based on the phylogenetic 16S rDNA sequence analysis, DNA–DNA similarity results, DNA G+C contents and phenotypic properties that are described in this investigation. Phylogenetic analysis of BALO 16S rRNA gene sequences revealed that marine isolates SJT, AQ and JS5T clustered in a separate clade from Bdellovibrio bacteriovorus 100T, as part of the clade that contains Bacteriovorax spp., indicating a much closer taxonomic relationship to the latter. Results from other studies confirm that all marine Bdellovibrio isolates analysed to date fall into the same clade (Snyder et al., 2002). It is appropriate, therefore, that salt-water Bdellovibrio should be reassigned to the genus Bacteriovorax. Here, we propose that marine isolates SJT and JS5T should be moved from the genus Bdellovibrio and assigned to the genus Bacteriovorax, as the type strains of Bacteriovorax marinus sp. nov. and Bacteriovorax litoralis sp. nov., respectively. Marine strain AQ should also be placed within Bacteriovorax marinus, due to its genetic similarities to isolate SJT. However, phenotypic and biochemical differences suggest that it may be a separate strain; this requires further study.
Description of Bacteriovorax marinus sp. nov.
Bacteriovorax marinus (ma'ri.nus. L. masc. adj. marinus of the sea, marine).
Cultural, biochemical and molecular characteristics of Bacteriovorax marinus are listed in Table 1. Optimal temperature range for growth is 15–30 °C. Salinity range is 10–60 parts per thousand (p.p.t.), with optimal growth between 20 and 30 p.p.t. Resistant to methicillin, nalidixic acid, colistin sulfate and vancomycin, but susceptible to kanamycin, carbenicillin, ampicillin/sublactam, gentamicin and polymyxin B (Guether & Williams, 1993). Enzyme activities for trypsin, alkaline phosphatase, esterase (C4), esterase lipase (C8), leucine aminopeptidase, valine aminopeptidase, acid phosphatase and phosphoamidase are detected. Closely related phylogenetically to both Bacteriovorax stolpii Uki2T and Bacteriovorax starrii A3.12T, as determined by 16S rDNA sequence analysis. DNA G+C content is 37·7–38·3 mol%.
The type strain of Bacteriovorax marinus is SJT (=ATCC BAA-682T=DSM 15412T). Isolated from the surrounding waters of St John's Island, US Virgin Islands. Reference strain is AQ.
Description of Bacteriovorax litoralis sp. nov.
Bacteriovorax litoralis (li.to.ra'lis. L. masc. adj. litoralis pertaining to the coast).
Cultural, biochemical and molecular characteristics of Bacteriovorax marinus are listed in Table 1. Optimal temperature range for growth is 15–35 °C. Salinity range is 0·25–30 p.p.t., with optimal growth at 5 p.p.t. Resistant to a range of antibiotics (methicillin, kanamycin, colistin sulfate and vancomycin), but susceptible to ampicillin/sublactam (Guether & Williams, 1993). No trypsin activity is detected (unlike Bacteriovorax marinus and Bdellovibrio bacteriovorus 109J), but enzyme activities are demonstrated for alkaline phosphatase, esterase (C4), esterase lipase (C8), leucine aminopeptidase, valine aminopeptidase, acid phosphatase and phosphoamidase. Closely related phylogenetically to both Bacteriovorax stolpii Uki2T and Bacteriovorax starrii A3.12T, as determined by 16S rDNA sequence analysis. DNA G+C content is 37·8 mol%.
The type strain (and only strain to date) is JS5T (=ATCC BAA-684T=DSM 15409T). Isolated from the gills of a crab captured on the Patuxent River, an estuary of the Chesapeake Bay.
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ACKNOWLEDGEMENTS |
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