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Department of Microbiology, Bose Institute, P-1/12, CIT Scheme VII-M, Kolkata – 700 054, India
Correspondence
Wriddhiman Ghosh
Wriman{at}rediffmail.com
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ABSTRACT |
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88 %) gene sequence similarities to all existing species of the most closely related genera, a unique fatty acid profile, a distinct G+C content (59·6 mol%) and phenotypic characteristics all suggested that strain SJTT represents a novel species. DNA–DNA hybridization and SDS-PAGE analysis of whole-cell proteins also confirmed the taxonomic uniqueness of SJTT. It is therefore proposed that isolate SJTT (=LMG 22697T=MTCC 7001T) be classified as the type strain of a novel species, Mesorhizobium thiogangeticum sp. nov.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA and recA gene sequences of the strain SJTT are AJ864462 and AM040610, respectively.
Fatty acid profiles, a phenogram derived from UPGMA/SSM analysis and SDS-PAGE analysis of whole-cell proteins of strain SJTT and related species are available as supplementary material in IJSEM Online.
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; Rogel et al., 2001) existing as significant components of rhizobial populations in the soil has been indicated (Sullivan et al., 1996).
From soil adjacent to the root of Clitoria ternatea, a slender leguminous herb (family Papilionaceae) that occurs on almost every piece of waste ground and in village forests of the Lower Gangetic plains of India, the mesophilic, neutrophilic, facultatively sulfur-oxidizing chemolithotrophic bacterial strain SJTT was isolated by enrichment, along with 15 other sulfur-oxidizing strains, on reduced sulfur compounds as the sole energy and electron source. Numerous plants were uprooted from a single plot of land and soil that adhered loosely to the roots was dislodged by gently striking the roots with sterile forceps. The collected pool of loose soil that was devoid of any root nodules was supplemented with Na2S2O3.5H2O (5 %), Na2S (1 %) and elemental sulfur powder (5 %) and incubated at 30 °C for 2 weeks with intermittent sprinkling of sterile water. Enriched soil samples were added (1 %, w/v) to MS-thiosulfate-yeast extract (MSTY; 20 mM Na2S2O3.5H2O supplemented with 5·0 g yeast extract l–1) liquid medium (pH 7·0–7·5) based on a modified basal and mineral salts (MS) solution that contained the following (l–1 distilled water): 1 g NH4Cl, 4 g K2HPO4, 1·5 g KH2PO4, 0·5 g MgSO4.7H2O and 5·0 ml trace metals solution (Vishniac & Santer, 1957). Mixtures were incubated at 30 °C on a rotary shaker until the colour of the phenol red indicator added to the medium changed to yellow. Serial dilutions from the soil-MSTY broth mixture were plated on MSTY agar and incubated at 30 °C. Strain SJTT, which could be distinguished in terms of colony morphology and the rate and extent of acid production in chemolithoautotrophic MS-thiosulfate (MST; 20 mM Na2S2O3.5H2O plus 50 mg yeast extract l–1 as growth factor supplement) and mixotrophic MSTY media, was isolated as a pure culture.
All growth experiments were performed at 30 °C and yeast extract (50 mg l–1) or a vitamin mixture (10 mg each of nicotinic acid, pantothenic acid, pyridoxine, thiamin, p-aminobenzoic acid, riboflavin and biotin l–1) was always added to the medium. Cells were tested for their ability to use thiosulfate (12–20 mM), sulfide (2 mM), sulfite (3 mM), thiocyanate (2 or 5 mM), elemental sulfur (0·5 and 1·0 %, w/v) or tetrathionate (10 mM) as a substrate for chemolithotrophic growth. For testing mixotrophic utilization of sulfur compounds, yeast extract (2·5 or 5·0 g l–1) was added to the above formulations. The level of thiosulfate or tetrathionate in the medium was estimated by the cyanolytic method described by Kelly & Wood (1994). Strain SJTT was facultatively chemolithotrophic and could grow on 12–20 mM thiosulfate as the sole energy and electron source, but not on soluble sulfide, thiocyanate, tetrathionate or sulfite under the experimental conditions used. It also utilized elemental sulfur (10 g l–1) for chemolithotrophic growth, with a corresponding increase in the OD600 of the broth cultures by an order of 0·2, which is attributable to oxidation and the disappearance of colloidal sulfur, along with lowering of the pH of the medium from 7·5 to 6·2 over an incubation period of 5 days. Details of chemolithotrophic growth and thiosulfate consumption by SJTT in MST or MSTY medium containing 20 mM sodium thiosulfate, equivalent to 40 µg sulfur atoms ml–1, are shown in Table 1.
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). The bacterium could grow in complex media like Luria–Bertani (LB) broth, nutrient broth (NB) and MS-peptone casein hydrolysate. Poor growth was observed on yeast extract-mannitol agar (YMA). In synthetic heterotrophic media, i.e. MS solution plus one organic carbon source (5 g l–1) supplemented with vitamin mixture, the isolate could utilize only a few carbon compounds.
The 16S rRNA gene was amplified and its sequence was determined from PCR products using universal primers (Gerhardt et al., 1994). Evolutionary distances were calculated by pairwise comparison of the aligned 16S rRNA gene sequences (Jukes & Cantor, 1969) by the program DNADIST. A consensus neighbour-joining tree (Saitou & Nei, 1987) was constructed following majority rule and strict consensus out of 100 phylogenetic trees produced using the program NEIGHBOR in PHYLIP version 3.572c (Felsenstein, 1993). Bootstrap values (100 replicates) were calculated by the method of Felsenstein (1985) to validate the reproducibility of the branching pattern of the tree. 16S rRNA gene sequence-based phylogenetic analysis of SJTT showed that the strain had maximum 16S rRNA gene sequence similarity (96·2–96·8 %) to species of Mesorhizobium, e.g. Mesorhizobium loti, Mesorhizobium plurifarium, Mesorhizobium amorphae and Mesorhizobium chacoense, and occupied the same phylogenetic branch as Mesorhizobium species (Fig. 1). Species of other genera, i.e. Sinorhizobium fredii (96 %), Aminobacter aminovorans (95·7 %), Aminobacter aganoensis (95·6 %) and Aminobacter niigataensis (95·6 %), had still lower 16S rRNA gene sequence similarity to SJTT, whereas strains of Pseudaminobacter salicylatoxidans exhibited 94 % rRNA gene sequence similarity to SJTT. Strain KCT001, a thiosulfate- and tetrathionate-oxidizing facultatively chemolithotrophic member of Pseudaminobacter salicylatoxidans (Deb et al., 2004) exhibited 94 % 16S rRNA gene sequence similarity to SJTT. A Mexican soil isolate, designated Ls29 and identified as a strain of M. plurifarium, showed slightly higher 16S rRNA gene sequence similarity (97·1 %) to SJTT.
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; Weir et al., 2004; Vinuesa et al., 2005) has been shown to be congruent with that of the small-subunit rRNA genes with well-supported clades for members of Mesorhizobium species having unequivocal bootstrap supports (Gaunt et al., 2001). Moreover, large-scale phylogenies of recA in the Bacteria as a whole have been found to be consistent with the corresponding rRNA gene sequence-based phylogenies (Eisen, 1995; Young, 1998).
A recA gene fragment was amplified by PCR from isolate SJTT using published recA primers (Gaunt et al., 2001) [recA 6 (forward; CGKCTSGTAGAGGAYAAATCGGTGGA) and recA 555 (reverse; CGRATCTGGTTGATGAAGATCACCAT), where mixtures of bases used at certain positions are as follows: K, T or G; S, G or C; Y, C or T; R, A or G]. The recA gene sequence-based phylogenetic affinities of strain SJTT were reconstructed using the neighbour-joining method (Saitou & Nei, 1987) with distances estimated using Jukes–Cantor as well as Kimura's two-parameter models with 100 bootstrap replications.
Phylogenetic analysis based on the recA gene sequence also placed SJTT in the same evolutionary branch as Mesorhizobium species (Fig. 2). The partial recA gene sequence of strain SJTT had maximum similarity (88 %) to strains of M. loti, whereas other rhizobial isolates awaiting specific designation and tentatively described as Mesorhizobium species (Weir et al., 2004) also exhibited 88 % nucleotide sequence similarity to the recA gene of SJTT. The translated amino acid sequences of the recA genes of these organisms had 97 % identity to that of SJTT. The partial recA gene sequences of strains of M. plurifarium, Mesorhizobium huakuii, Mesorhizobium tianshanense, Mesorhizobium ciceri, Mesorhizobium mediterraneum, M. amorphae and M. chacoense had 85–87 % similarity to that of strain SJTT. The translated amino acid sequences of the recA genes of all these Mesorhizobium species had 96–97 % identity to that of SJTT. recA gene sequence similarities of the novel sulfur-oxidizing chemolithotroph with species of other genera like Rhizobium, Sinorhizobium, Agrobacterium, Azorhizobium, Bradyrhizobium, Rhodopseudomonas, Mycoplana and Brucella were much lower, between 80 and 84 % (Fig. 2), whereas the translated amino acid sequences of the recA genes of these organisms had obviously lower identities (<96 %) to that of strain SJTT.
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with minor modifications. Dot-blot hybridization experiments were carried out with the DIG DNA Labelling and Detection system as described previously (Labrenz et al., 2000) to determine DNA–DNA binding values. The taxonomic uniqueness of SJTT was supported by its low DNA–DNA binding values with the four phylogenetically closest species: M. plurifarium LMG 11892T (28 %); M. loti LMG 17826 t2 (24 %); M. amorphae LMG 18932 (18 %); and M. chacoense LMG 19008T (22 %). The phylogenetically related sulfur-oxidizing chemolithotrophic Pseudaminobacter salicylatoxidans KCT001 (Deb et al., 2004) exhibited an even lower DNA–DNA binding value (10 %) with SJTT.
In this connection, it is noteworthy that homologues of the sulfur oxidation (Sox) genes discovered by virtue of genetic studies with alphaproteobacteria like Paracoccus pantotrophus, Pseudaminobacter salicylatoxidans strain KCT001 and Rhodovulum sulfidophilum (Friedrich et al., 2000; Mukhopadhyaya et al., 2000; Rother et al., 2001; Appia-Ayme et al., 2001; C. Lahiri, S. Mandal, W. Ghosh, B. Dam and P. Roy, unpublished observations) have also been revealed from whole genome sequence analyses of several species of the order Rhizobiales (Kaneko et al., 2002; see NCBI Microbial Genomes Annotation Project, accession no. NZ_AAAF01000001 for Rhodopseudomonas palustris). However, despite the close phylogenetic relationship of the two organisms, no hybridization was detected, even under low stringency conditions, when the genomic DNA of SJTT was probed by Southern hybridization with DIG-labelled soxT, soxYZ or soxBC gene fragments from Pseudaminobacter salicylatoxidans KCT001 (Mukhopadhyaya et al., 2000; GenBank/EMBL accession number AJ404005) (data not shown). A distinct DNA G+C content of 59·6 mol%, determined using HPLC as described by Mesbah et al. (1989), was observed for SJTT, which differs from the G+C contents of most of the closely related species of Mesorhizobium, thus reiterating the distinction of the isolate as a unique member of the mesorhizobia.
At the same time, the reference strains M. plurifarium LMG 11892T, M. loti LMG 17826 t2, M. amorphae LMG 18932 and M. chacoense LMG 19008T were tested for their ability to oxidize or chemolithotrophically utilize thiosulfate in autotrophic MST or mixotrophic MSTY media. However, these mesorhizobial strains phylogenetically closest to SJTT could neither oxidize nor grow in MST or MSTY medium under the experimental conditions used.
Nodulating ability of SJTT was tested on Clitoria ternatea, as well as two other economically important leguminous plants (Pisum sativum and Cicer arietinum). Seeds were surface-sterilized in concentrated H2SO4 for 20 min. After the acid was drained, seeds were washed thoroughly with 10 changes of sterile water and placed in moistened steam-sterilized sand to germinate at 28 °C for 3–5 days. Germinating seedlings, 3–4 cm long, were inoculated at the base of the stem or the radicle–plumule junction with 1 ml SJTT inoculum (heavy suspension of LB broth-grown exponential-phase culture in 10 ml nitrogen-free Jensen solution, pH 6·8) and placed in a steam-sterilized sand–vermiculite mixture in 12 cm diameter pots and left to establish in the greenhouse at 28 °C. The surface was covered with polyurethane beads to prevent evaporation and contamination. Plants were watered with a sterile nitrogen-free nutrient solution once in 3 days. Saplings were checked for the presence of nodules after 10 weeks of growth. None of the plant species (10–15 individual saplings were taken for each plant species) inoculated with SJTT were found to develop nodules. Positive controls of Cicer arietinum seedlings inoculated with M. ciceri ATCC 51585T developed nodules, whereas uninoculated plants did not. Since the negative observations found in these cases cannot be taken as attributes of the organism, it cannot be confirmed that SJTT does not have the potential to nodulate any plant host.
The inability to utilize maltose, raffinose, L-alanine, rhamnose, fructose, L-arabinose, sucrose or lactose as single carbon sources, fast growth rates, growth in LB medium and chemolithotrophic utilization of thiosulfate and sulfur are some of the phenotypic characters that discriminate strain SJTT from its phylogenetic relatives. Numerical analysis of all the available comparative phenotypic characteristics was performed using the simple matching coefficient (SSM) (Sneath & Sokal, 1973) followed by generation of phenograms using the unweighted pair group with mathematical averages (UPGMA) algorithm. These analyses largely corroborated the phylogenetic and genetic distinctiveness of strain SJTT. Table 2 shows the key phenotypic characters that distinguish SJTT from the most closely related Mesorhizobium species and Pseudaminobacter salicylatoxidans; the phenogram derived from UPGMA/SSM analysis of the phenetic characteristics of SJTT with respect to the nearest mesorhizobia is available as Supplementary Fig. S1 in IJSEM Online. Polyphasic evaluation that included almost 70 % phenotypic similarity to standard strains of M. plurifarium (Wang et al., 2003) and high 16S rRNA gene sequence similarity (98·75 %) to the type strain (LMG 11892T) of the species identified Ls29 as a strain of M. plurifarium. However, SJTT had several phenotypic dissimilarities from Ls29 (Table 2) and a lower SSM value (60 %).
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Cellular fatty acid profiles have also been shown to discern species of Mesorhizobium accurately and to distinguish between related genera (de Lajudie et al., 1998; Tighe et al., 2000). After an incubation period of 40 h at 30 °C on LB agar, a loopful of well-grown cells was harvested and the preparation, separation and identification of fatty acids were performed using the Sherlock Microbial Identification system (Microbial ID) at the DSMZ (Braunschweig, Germany). Strain SJTT synthesized 16 : 0, 17 : 0, 18 : 0, 17 : 0 iso, 17 : 1
8c, 18 : 17c and 19 : 0 cyclo 8c fatty acids, thus confirming its classification as a species of Mesorhizobium. On the other hand, SJTT was distinct from all related mesorhizobia by its unique possession of 14 : 0, 18 : 0 3-OH, 15 : 0 iso 3-OH, relatively large amounts (77·41 %) of 18 : 17c, and the absence of 13 : 0 iso 3-OH, 12 : 0 3-OH and 17 : 0 cyclo. The fatty acid profile also set SJTT apart from species of other phylogenetically related genera like Aminobacter, Pseudaminobacter and Sinorhizobium (Supplementary Table S1).
From the above findings, it is evident that the novel mesophilic, neutrophilic and facultatively sulfur-oxidizing chemolithoautotrophic isolate constitutes a unique taxonomic entity that belongs to the genus Mesorhizobium, but is distinct from all known species of the genus. Strain SJTT is thus classified as the type strain of a novel species, Mesorhizobium thiogangeticum sp. nov. However, in the absence of an adequate number of strains required to describe a bacterial species in general and a rhizobial species in particular, the complete description and delimitation of the novel species can only be finalized when more isolates are discovered or become available.
Description of Mesorhizobium thiogangeticum sp. nov.
Mesorhizobium thiogangeticum (thi.o.gan.ge'ti.cum. Gr. neut. n. thion sulfur; L. neut. adj. gangeticum from Ganga; N.L. neut. adj. thiogangeticum because the bacterium is so far the only sulfur-lithotrophic member of Mesorhizobium and is a native of the Gangetic plains of India).
Gram-negative, aerobic, non-spore-forming, irregularly elongated or rod-shaped bacterium (cells 1·2–1·5x0·2–0·4 µm). Colonies on LB or MSTY media are shining white, convex, opaque and reach 1–3 mm in diameter within 4–5 days at 30 °C. Maximum temperature for growth is 37 °C and range of pH tolerance is 5·5–8·5. Catalase-positive, but oxidase-negative. Strain SJTT cannot liquefy gelatin, produce indole or solubilize phosphate. It can grow heterotrophically in complex media like LB, NB, YMA and MS-peptone casein hydrolysate. In synthetic media supplemented with 50 mg yeast extract l–1 or vitamin mixture, the isolate utilizes only a few carbon compounds, D-glucose, L-arabinose, D-galactose, D-mannitol, L-histidine, L-leucine, L-isoleucine, L-glutamine, succinate and sodium benzoate, as the sole source of energy for chemo-organoheterotrophic growth. No growth is observed with citrate, oxalate, malate, acetate, maltose, sucrose, glycerol, myo-inositol, mandelate, DL-lactate, D-fructose, D-raffinose, D-xylose, D-lactose, L-aspartic acid, L-lysine, L-cysteine, L-cystine, L-tyrosine, L-threonine, L-alanine, L-serine, D-mannose, L-arginine or tryptophan. No growth is observed in nitrogen-free Burk medium under aerobic conditions. Chemolithoautotrophic growth is observed with thiosulfate and elemental sulfur, but not tetrathionate, thiocyanate, soluble sulfides, sulfite or arsenite. Synthesizes the following fatty acids: 14 : 0 (0·88 %), 15 : 0 iso (8·23 %), summed feature 3 (16 : 17c/15 : 0 iso 2-OH) (1·82 %), 16 : 0 (2·46 %), 15 : 0 iso 3-OH (0·41 %), 17 : 0 iso (0·85 %), 17 : 18c (0·51 %), 17 : 0 (0·81 %), 18 : 17c (77·41 %), 18 : 0 (1·28 %), 11-methyl 18 : 17c (4·23 %), 19 : 0 cyclo 8c (0·64 %) and 18 : 0 3-OH (0·47 %). The DNA G+C content of the type strain is 59·6 mol%, as determined by HPLC.
The type strain, strain SJTT (=LMG 22697T=MTCC 7001T), is the only known strain of the species, isolated from soil adjacent to the roots of the leguminous plant Clitoria ternatea, a native of the lower Gangetic plains of India.
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ACKNOWLEDGEMENTS |
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