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Microbiology Department, M. S. Swaminathan Research Foundation, 3rd Cross Street, Taramani Institutional Area, Chennai 600 113, India
Correspondence
Sudha Nair
microbiology{at}mssrf.res.in
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains MSSRF3T and MSSRF10 are DQ847123 and DQ273663, respectively, and those for the recA, rpoA and pyrH gene sequences of strains MSSRF3T, MSSRF10 and Vibrio ruber JCM 11486T are EF523232–EF523240.
Figures showing the colony and cell morphologies of strain MSSRF3T, phylogenetic trees constructed using maximum-likelihood and maximum-parsimony and based on partial 16S rRNA gene sequences, neighbour-joining trees based on partial recA, rpoA and pyrH gene sequences and results of PCR-based fingerprinting analysis using RAPD, GTG5, BOX, PCR-RFLP and ribotyping are available with the online version of this paper.
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), which were isolated from various environments such as aquatic, estuarine and coastal, and from marine sediments (Thompson et al., 2004). Several cultivation-dependent and -independent studies have shown that vibrios appear at particularly high densities in and/or on marine organisms, e.g. corals, fish, molluscs, seagrass, sponges, shrimp and zooplankton (Thompson et al., 2004). Some species are found as symbionts in specialized luminous organs of marine fish and invertebrates, whereas a number of other species are well-known pathogens of humans or marine animals (Thompson et al., 2004). To date, relatively few studies have shown that vibrios can produce antimicrobial substances (Hjelm et al., 2004; Long & Azam, 2001; Sugita et al., 1997). However, these vibrios were not identified at the species level. Herein we report the isolation and polyphasic taxonomic study of two novel Vibrio strains, MSSRF3T and MSSRF10, which inhibit phytopathogenic bacteria. This study was conducted in Pichavaram mangroves, on the south-east coast of India, situated about 250 km south of Chennai (1 ° 27' N 7 ° 47' E). The soil salinity was about 25–30 ppt and the temperature was about 28–32 °C. Strains MSSRF3T and MSSRF10 were isolated from the rhizosphere region of mangrove-associated wild rice (Porteresia coarctata Tateoka) as part of a research programme, the main objective of which was to isolate and screen plant-growth-promoting bacteria, in particular for biocontrol of bacterial phytopathogens. Briefly, the rhizosphere soil samples were obtained by shaking the roots gently to remove loosely attached soil. The soil adhering to the roots was then rinsed with 10 ml sterile water. The resulting rinse solution containing bacteria from the rhizosphere was serially diluted and plated onto half-strength trypticase soy agar (TSA; Difco), supplemented with 2 % NaCl (TSA+NaCl). Colonies that appeared on half-strength TSA+NaCl plates after 1–7 days incubation at 28 °C were selected and purified; two strains, designated MSSRF3T and MSSRF10, were found to have antimicrobial activity against Xanthomonas oryzae, Erwinia carotovora and Pseudomonas syringae, and were chosen for further study. Both strains were maintained on TSA+NaCl at 4 °C or stored at –80 °C in trypticase soy broth (TSB; Difco) containing 2 % NaCl (TSB+NaCl) with 15 % (v/v) glycerol.
Strains MSSRF3T and MSSRF10 were grown in TSB+NaCl at 28 °C with aeration. Cell-free culture fractions were recovered by centrifugation (5000 g for 30 min at 4 °C) of cultures grown in TSB+NaCl for 48 h at 28 °C in flasks without shaking. The cell-free spent culture medium was decanted and sterilized by passing it through a 0.22 µm-pore-size filter, and was maintained at 4 °C for short-term storage or at –80 °C for long-term storage. The antimicrobial activity of the cultures or cell-free culture fractions was determined by using a spot-on-lawn assay. The bacterial phytopathogens X. oryzae, E. carotovora and P. syringae were grown separately in TSB for 72 h at 28 °C. From these cultures, 100 µl (at OD 600 nm, approximately 106 c.f.u. ml–1) was pipetted onto TSB containing 1.5 % (w/v) agar and spread plated. After the plates had been dried for 3 h at room temperature, 5 µl of 24 h cultures of strains MSSRF3T and MSSRF10 was spotted on the target organism lawn, and the spots were allowed to dry. Similarly, a 3 mm well was made in plates containing the target organism; to these wells 100 µl filter-sterilized, cell-free culture supernatants obtained from strains MSSRF3T and MSSRF10 were added. The plates were incubated at 28 °C and examined each day for the appearance of zones of inhibition of microbial growth. The diameter (in mm) of the zones of inhibition was used as a measure of antimicrobial activity.
Strains MSSRF3T and MSSRF10 inhibited a wide range of bacterial phytopathogens (Fig. 1 and Table 1). The antibacterial activity of both strains did not require the presence of living cells, because antibacterial activity was demonstrated using filter-sterilized, cell-free culture fractions of both strains grown in TSB+NaCl, as shown in Table 1, indicating that the antibacterial compound produced by both strains was extracellular. Purification and characterization of the antibacterial substance produced by strains MSSRF3T and MSSRF10 has still to be undertaken.
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) and the recA, pyrH and rpoA genes were amplified and sequenced as described by Thompson et al. (2005). The sequences of these genes were compared against sequences available from GenBank using the BLAST program (Altschul et al., 1997) and were aligned manually using CLUSTAL W version 1.6 (Thompson et al., 1994). Distance matrices for the aligned sequences were determined using the Kimura two-parameter method (Kimura, 1980). The distance matrices were then used to reconstruct phylogenetic trees using neighbour-joining (Saitou & Nei, 1987), maximum-likelihood (Felsenstein, 1981) and maximum-parsimony (Felsenstein, 1996). The robustness of individual branches was estimated by bootstrapping with 1000 replicates (Felsenstein, 1985).
Nearly complete 16S rRNA gene sequences for strains MSSRF3T (1424 bp) and MSSRF10 (1392 bp) were obtained. Comparison with 16S rRNA gene sequences of recognized Vibrio species held in GenBank indicated that the two strains were related phylogenetically to members of this genus. Phylogenetic trees based on almost-complete sequences and using neighbour-joining, maximum-likelihood and maximum-parsimony methods were all in agreement and showed that strains MSSRF3T and MSSRF10 are closely related to V. ruber JCM 11486T (98.3 and 98.5 % similarity, respectively) and Vibrio gazogenes LMG 19540T (95.7 and 95.5 % similarity, respectively) (Fig. 2; see also Supplementary Fig. S1a, b, available in IJSEM Online). The level of 16S rRNA gene sequence similarity between strains MSSRF3T and MSSRF10 was 98.0 %, and below 95.7 % with other Vibrio species. The values obtained from the 16S rRNA gene sequence analysis for strains MSSRF3T and MSSRF10 were above the cut-off value of 97 % for the definition of bacterial species (Stackebrandt & Goebel, 1994) and, hence, as limitations of 16S rRNA gene sequencing for differentiating closely related species have been documented (Fox et al., 1992), we analysed other housekeeping genes that are useful for differentiation of Vibrio species as described previously (Thompson et al., 2005).
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). A pairwise analysis of the recA sequence of strain MSSRF3T showed low levels of similarity with that of strain MSSRF10 (91.2 %), V. ruber JCM 11486T (90.2 %), V. gazogenes LMG 19540T (88.5 %) and less than 88.5 % with other Vibrio species. Nevertheless, strain MSSRF10 showed high recA sequence similarity with V. ruber JCM 11486T (99.8 %) (Supplementary Fig. S2b, in IJSEM Online). This result is in agreement with those obtained from the pyrH gene sequence analysis and the lower similarity values found between these two genes (recA and pyrH) of V. ruber JCM 11486T and strain MSSRF3T confirm that this strain does not belong to V. ruber whereas strain MSSRF10 does belong to V. ruber, according to Thompson et al. (2005).
In addition to the pyrH and recA genes, the rpoA gene has also been proposed as an alternative marker for bacterial classification and as a chronometer in the family Vibrionaceae (Thompson et al., 2005). Sequence comparisons of the rpoA sequence of strain MSSRF3T showed 98.3 % similarity with V. ruber JCM 11486T, 98.4 % with V. gazogenes LMG 19540T and 98.0 % with strain MSSRF10. However, strain MSSRF10 shared high rpoA sequence similarity with V. ruber JCM 11486T (99.7 %) (Supplementary Fig. S2c, in IJSEM Online). Strains MSSRF3T and MSSRF10 showed less than 91.0 % similarity with other Vibrio species. This result correlates well with the 16S rRNA gene analysis and shows that rpoA gene sequences were slightly less discriminatory than recA and pyrH sequences, supporting the fact that species with >98 % rpoA sequence similarity will have <97 % recA and pyrH gene sequence similarities (Thompson et al. 2005).
Based on sequence analysis of four different genetic loci, it is evident that analysis of recA and pyrH gene sequences was more discriminatory than analysis based on rpoA and 16S rRNA gene sequences, similar to results obtained by other workers, indicating that rpoA and 16S rRNA gene sequences have similar discriminatory powers (Thompson et al., 2004, 2005). Therefore, considering the results of the overall phylogenetic analysis, the genealogical positions of strains MSSRF3T and MSSRF10 were further examined together with V. ruber JCM 11486T by using a polyphasic approach, as described by Thompson et al. (2004) and Stackebrandt et al. (2002).
Restriction analysis of the 16S rRNA gene was performed according to Behrendt et al. (1999). 16S rRNA genes were amplified using primers described previously (Loganathan & Nair, 2004), resulting in amplification of a single fragment of approximately 1500 bp. Digestion of the PCR products was performed using a set of endonucleases (AccI, AluI, DdeI and RsaI), which were selected on the basis of the 16S rRNA gene sequence of V. ruber JCM 11486T using NEBcutter version 2.0 software. Ribotyping was performed with the enzymes HindIII and HaeIII. The electrophoresis conditions, blotting procedures, hybridization with a 32P-labelled 16S rRNA probe of V. ruber JCM 11486T using a rediprime DNA-labelling kit (Amersham) at 65 °C and detection procedures were carried out as described by Sambrook et al. (1989). Random amplified polymorphic DNA (RAPD) analysis was performed using two random 10-mer universal primers, OPD5 (5'-TGAGCGGACA-3') and OPD6 (5'-ACCTGAACGG-3'), as described previously (Loganathan et al., 1999). Repetitive extragenic palindromic PCR (rep-PCR) fingerprinting using GTG5 and BOX primers was performed as described by Ben-Haim et al. (2003). V. ruber JCM 11486T was used as a reference strain in studies related to PCR-based fingerprinting analysis.
From the 16S rRNA gene restriction analysis, it was found that, using the enzymes AccI, AluI and RsaI, strain MSSRF3T could be differentiated from strain MSSRF10 and V. ruber JCM 11486T, whereas use of the enzyme DdeI enabled differentiation of V. ruber JCM 11486T from strains MSSRF3T and MSSRF10 (Supplementary Fig. S3a, in IJSEM Online), suggesting that strain MSSRF10 was very closely related to V. ruber JCM 11486T when compared with strain MSSRF3T at the 16S rRNA gene level. These results were in good agreement with the phylogenetic analysis of the 16S rRNA gene, showing that V. ruber JCM 11486T and strain MSSRF10 form a distinct cluster and that, within that cluster, strain MSSRF3T represents a separate branch, as shown in Fig. 2
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Ribotype patterns obtained with HaeIII and HindIII and fingerprints obtained with RAPD primers (OPD5, OPD6) and with BOX and GTG5 primers clearly indicate that strains MSSRF3T, MSSRF10 and V. ruber JCM 11486T are distinct from each other (see Supplementary Fig. S3b, c, in IJSEM Online). From these results, it is suggested that strains MSSRF3Tand MSSRF10 are not clonal in origin, that they should be recognized as a distinct genotype and are different from V. ruber JCM 11486T.
Cells of strains MSSRF3T and MSSRF10 were grown in TSB+NaCl for 24 h and their morphology and motility were examined using phase-contrast and electron microscopy. For electron microscopy, fresh bacterial cells were transferred to a 300-mesh, carbon-coated copper grid, stained with 2 % (w/v) phosphotungstic acid solution (pH 6.5) for 1 min and then observed with a JEM-1200EX electron microscope (JOEL). Classical phenotypic tests were performed as described by Baumann et al. (1984), Farmer & Hickman-Brenner (1992), Leifson (1963) and Shieh et al. (2000). The ability to utilize various carbon compounds as the sole carbon source was investigated by testing 0.5 % carbon compounds in minimal base medium containing 2.0 % (w/v) NaCl, 1.0 % (w/v) K2HPO4, 0.45 % (w/v) KH2PO4, 0.14 % (w/v) CaCl2, 0.15 % (w/v) MgCl2, 0.075 % (w/v) KCl, 0.1 % (w/v) (NH4)2SO4 and 1.5 % (w/v) agar. The results were recorded after 7 days incubation at 28 °C, with V. ruber JCM 11486T being used as a reference. For in vitro pigment analysis, strains MSSRF3T, MSSRF10 and V. ruber JCM 11486T were grown aerobically on TSA+NaCl at 28 °C, extracted with acetone/methanol (7 : 2, v/v) and analysed spectrophotometrically (Shieh et al., 2003).
According to the data, strains MSSRF3T and MSSRF10 were characterized as mesophilic, halophilic, facultative anaerobic, Gram-negative rods that are motile by means of single polar flagella (Supplementary Fig. S4a, in IJSEM Online), indicating that the strains probably represent a species of Vibrio in the family Vibrionaceae (Baumann et al., 1984). Both strains produced non-diffusible, cellular red pigments, regardless of the presence of light (see Supplementary Fig. S4b, in IJSEM Online). Acetone/methanol extracts of the red pigments produced by strains MSSRF3T, MSSRF10 and V. ruber JCM 11486T showed maximum absorption at about 535 nm, which is identical to the absorption spectrum of prodigiosin (Allen, 1967). Strain MSSRF3T was phenotypically related to strain MSSRF10, and could be differentiated from it by not being able to reduce nitrate. Unusually, we observed that strains MSSRF3T and MSSRF10 could utilize substrates (trehalose, adonitol, dulcitol, inositol, sorbitol, L-alanine, L-arginine, L-lysine, L-ornithine, L-threonine and L-glycine) very well when they were grown on minimal salt base agar medium rather than in liquid medium. Interestingly, negative results were obtained for V. ruber JCM 11486T for utilization of the above substrates when grown on minimal salt base agar medium and in minimal salt base liquid medium, under the same conditions as for strains MSSRF3T and MSSRF10. Differential phenotypic characteristics of strain MSSRF3T, the phylogenetically closest species V. ruber JCM 11486T and other phenotypically and phylogenetically related Vibrio species are shown in Table 2. Additional phenotypic characteristics of strain MSSRF3T are given in the species description.
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), as already reported (Delorme et al., 2002). The DNA G+C content of strain MSSRF3T was 51.3 mol%, which is slightly higher than the values reported for other species of the genus Vibrio, and 51.0 mol% for strain MSSRF10, which was in good agreement with values for the genus Vibrio (Baumann et al., 1984) but was considerably higher than the value of 45.8 mol% for V. ruber JCM 11486T (Shieh et al., 2003).
To confirm the results obtained from the biochemical, genotyping and phylogenetic analyses, DNA–DNA hybridization was performed between strains MSSRF3T, MSSRF10 and their closest relative V. ruber JCM 11486T, by using the membrane filter method (Tourova & Antonov, 1987) as described previously (Shivaji et al., 1992; Reddy et al., 2000). Hybridizations were performed on four replicates. Each DNA–DNA relatedness value is the mean of reciprocal and non-reciprocal reactions. The results showed that, at the DNA–DNA level, there was 44 % relatedness between strains MSSRF3T and MSSRF10, 80 % between strain MSSRF10 and V. ruber JCM 11486T and 45 % between strain MSSRF3T and V. ruber JCM 11486T. These values are the means of four replicate experiments, which did not differ by more than 2 %. These results indicate that strain MSSRF3T does not belong to Vibrio ruber JCM11486T, whereas strain MSSRF10 is considered to be a member of Vibrio ruber JCM11486T when the recommendation of a threshold value of 70 % DNA–DNA relatedness for the definition of species is considered (Wayne et al., 1987).
In conclusion, strain MSSRF3T can be differentiated from strain MSSRF10 and its closest relative V. ruber JCM 11486T with respect to its genomic fingerprinting analysis (RAPD, GTG5, BOX, PCR-restriction fragment length polymorphism and ribotyping), phylogenetic analysis (16S rRNA, recA, pyrH, rpoA), phenotypic characteristics, high DNA G+C content and the fact that it shows <60 % relatedness at the DNA–DNA level with these species. Thus, based on phenotypic, genotypic and phylogenetic characteristics, strain MSSRF3T represents the type strain of a novel species of the genus Vibrio, for which the name Vibrio rhizosphaerae sp. nov. is proposed.
Description of Vibrio rhizosphaerae sp. nov.
Vibrio rhizosphaerae (rhi.zo'sp.hae.rae. Gr. fem. n. rhiza root; L. fem. n. sphaera -ae ball, any globe, sphere; N.L. gen. n. rhizosphaerae of the rhizosphere).
Cells are Gram-negative rods (approx. 1.8–3.2 µm long and 0.4–0.5 µm wide) and motile by means of single polar flagella. Catalase-positive and oxidase-negative. Colonies on agar media are red–pink, non-luminescent and circular, with entire margins. Swarming is not detected. Can inhibit a range of bacterial phytopathogens. Facultative anaerobe capable of both aerobic and anaerobic fermentative growth. Acid and gas are produced from fermentation of glucose. Other carbohydrates such as cellobiose, galactose, lactose, mannose, sucrose, xylose, mannitol and salicin are also fermented. Trehalose, dulcitol, sorbitol and inositol are not fermented. Voges–Proskauer, amylase, gelatinase, caseinase and lipase tests are positive, but arginine dihydrolase, lysine and ornithine decarboxylase tests are negative. Indole is not produced. Nitrate is not reduced. Optimum growth occurs at 25–30 °C and pH 7 and in 2 % NaCl. Growth occurs between 20 and 42 °C, but not at 4 or 45 °C. Growth occurs in 0.1–10 % NaCl; no growth occurs in the absence of NaCl. Grows in mineral medium containing glucose and NH4Cl. Cellobiose, galactose, glucose, lactose, mannose, melibiose, sucrose, xylose, mannitol, acetate, citrate, fumarate, pyruvate, L-aspartate, L-glutamate, L-serine and L-cysteine are utilized as sole carbon and energy sources. Utilizes trehalose, adonitol, dulcitol, inositol, sorbitol, proline, L-alanine, L-arginine, L-lysine, L-ornithine, L-threonine and L-glycine as sole sources of carbon and energy, only when grown on minimal salt agar medium, not in liquid medium. The DNA G+C content of the type strain is 51.3 mol%.
The type strain, MSSRF3T (=LMG 23790T=DSM 18581T), was isolated from the rhizosphere of mangrove-associated wild rice (Porteresia coarctata Takeoka).
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ACKNOWLEDGEMENTS |
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