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Ciceribacter Lividus Gen. Nov., Sp. Nov., Isolated from Rhizosphere Soil of Chick Pea (Cicer Arietinum L.)

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Ciceribacter Lividus Gen. Nov., Sp. Nov., Isolated from Rhizosphere Soil of Chick Pea (Cicer Arietinum L.) International Journal of Systematic and Evolutionary Microbiology (2013), 63, 4484–4488 DOI 10.1099/ijs.0.049726-0 Ciceribacter lividus gen. nov., sp. nov., isolated from rhizosphere soil of chick pea (Cicer arietinum L.) R. Kathiravan,1 S. Jegan,1 V. Ganga,1 V. R. Prabavathy,1 L. Tushar,2 Ch. Sasikala3 and Ch. V. Ramana2 Correspondence 1Microbiology Department, M. S. Swaminathan Research Foundation, 3rd Cross street, V. R. Prabavathy Taramani institutional area, Chennai 600113, India [email protected] or 2Department of Plant Sciences, School of Life Sciences, University of Hyderabad, [email protected] PO Central University, Gachibowli, Hyderabad 500046, India 3Bacterial Discovery laboratory, Centre for Environment, Institute of Science and Technology, JNT University Hyderabad, Kukatpally, Hyderabad 500085, India The taxonomic position of strain MSSRFBL1T, isolated from chickpea rhizosphere soil from Kannivadi, India, was determined. Strain MSSRFBL1T formed bluish black colonies, stained Gram-negative and was motile, aerobic, capable of fixing dinitrogen, oxidase-negative and catalase-positive. Q-10 was the major respiratory quinone. Major fatty acids of strain T MSSRFBL1 were C18 : 1v7c and C19 : 0cyclov8c. Minor amounts of C18 : 0,C12 : 0,C14 : 0 3-OH, C18 : 0 3-OH, C16 : 0,C16 : 1v6c/C16 : 1v7c,C17 : 0 3-OH and C20 : 1v7c were also present. Polar lipids included diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylmethylethanolamine, phosphatidylcholine and two unidentified glycolipids. Bacteriohopane derivatives (BHD1 and 2), diplopterol, diploptene, bishomohopanediol, adenosylhopane and 2b-methyl bacteriohopanetetrol were the major hopanoids of strain MSSRFBL1T. The genomic DNA G+C content was 71 mol%. EzTaxon-e-based BLAST analysis of the 16S rRNA gene indicated the highest similarity of strain MSSRFBL1T to Ensifer adhaerens LMG 20216T (97.3 %) and other members of the genus Ensifer (,96.9 %) in the family Rhizobiaceae of the class Alphaproteobacteria. However, phylogenetic analysis based on 16S rRNA, recA, thrC and dnaK gene sequences showed distinct out-grouping from the recognized genera of the family Rhizobiaceae. Based on phenotypic, genotypic and chemotaxonomic characters, strain MSSRFBL1T represents a novel species in a new genus in the family Rhizobiaceae for which the name Ciceribacter lividus gen. nov., sp. nov. is proposed. The type strain of Ciceribacter lividus is MSSRFBL1T (5DSM 25528T5KCTC 32403T). While understanding the rhizosphere bacterial diversity of family Rhizobiaceae for strain MSSRFBL1T isolated from chick pea (Cicer arietinum L.) we came across bluish black the rhizosphere soil of C. arietium L. colonies which happened to be a close relative of the genus Rhizosphere soils of C. arietium L. collected from Ensifer based on 16S rRNA gene sequence analysis. The Kannivadi (GPS position of the sample collection site is family Rhizobiaceae comprises the genera Ensifer, Shinella, 10u 229 44.400 N77u 499 48.00 E), Tamil Nadu, India, were Kaistia and Rhizobium. Except for the members of the serially diluted and plated on yeast malt agar (no. M424; genus Kaistia, all other members of the family Rhizobiaceae HiMedia) and incubated at 28 uC for 7 days. Bluish black are dinitrogen fixers and are associated with plants. colonies appeared along with other white colonies and Through this study, we propose a novel genus in the these were of particular interest because of the unique colony colour; they were purified and maintained on yeast malt agar. The purified isolate was designated MSSRFBL1T The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA, and preserved at 280 uC in 20 % (v/v) glycerol. recA, dnaK, thrC and nifH gene sequences of strain MSSRFBL1T are JQ230000, KC189949, KC189950, KC189951 and KC189952, Genomic DNA was extracted and purified from strain T respectively. MSSRFBL1 according to the method of Marmur (1961). + Five supplementary figures are available with the online version of this G C content of the DNA as determined by reversed-phase paper. HPLC (Mesbah et al., 1989) was 71±0.5 mol% for strain 4484 049726 G 2013 IUMS Printed in Great Britain Ciceribacter lividus gen. nov., sp. nov. MSSRFBL1T. PCR amplification of the 16S rRNA gene was E. adhaerens LMG 20216T (5AT; representing the type done by using the primer set 27f and 1492r (Lane, 1991). species of the genus Ensifer and also phylogenetically Amplification and sequencing were done as described by closely related to strain MSSRFBL1T), Ensifer kostiensis Rameshkumar & Nair (2009) using fluorescent terminators DSM 13372T (5TTR 15T; an additional strain represent- (Big Dye; Applied Biosystems) and run in a 3130xl ing the genus Ensifer) and Sinorhizobium americanum Applied Biosystems ABI prism automated DNA sequencer. DSM 15007T (5CFNEI 156T; a representative of the Identification of phylogenetic neighbours and calculation genus Ensifer) were used for comparative taxonomic of pairwise 16S rRNA gene sequence similarity were studies along with strain MSSRFBL1T. Colonies of strain achieved using the EzTaxon-e server (http://eztaxon-e. MSSRFBL1T were bluish black, while those of both ezbiocloud.net/). members of the genus Ensifer were white. Morphological properties (cell shape, size and cell division) were observed Based on the 1392 bp 16S rRNA gene sequence BLAST T under an Olympus model BH-2 phase-contrast light search analysis, Ensifer adhaerens LMG 20216 was the T T microscope. Cells of strain MSSRFBL1 were rod-shaped, nearest phylogenetic neighbour of strain MSSRFBL1 with 1–2 mm long and 0.3–0.5 mm wide, motile (confirmed 97.3 % sequence similarity. The CLUSTAL W algorithm of through hanging drop method) and multiplied by binary MEGA 4.0 software (Tamura et al., 2007) was used for fission. The colour of the cell suspension was bluish black. sequence alignments and for phylogenetic analysis of the In vivo absorption spectra as measured with a Spectronic individual sequences. Distances were calculated by using Genesys 2 spectrophotometer in sucrose solution (Tru¨per the Kimura correction in a pairwise deletion manner & Pfennig, 1981) exhibited maxima at 286 nm; however, (Kimura, 1980). Neighbour-joining (NJ), maximum-par- the lmax indicated that the pigment was not indigoidine, simony (MP) and minimum-evolution (ME) methods in which has absorption maxima at 300, 350 and 395 nm, the MEGA 4.0 software were used to reconstruct phylogen- found in Vogesella indigofera (Kuhn et al., 1965) and etic trees. Percentage support values were obtained using a Vogesella alkaliphila (Subhash et al., 2013). While indigoi- bootstrap procedure. Phylogenetic trees showed that the dine is easily extractable in methanol, the pigment of strain novel isolate (MSSRFBL1T) branched separately from other MSSRFBL1T was not extractable with most of the common members of the genus Ensifer (Fig. 1). The highest sequence organic solvents and hence could not be characterized in similarities for strain MSSRFBL1T were found with the type this study. T strain of E. adhaerens LMG 20216 (97.3 %) and a few T Strain MSSRFBL1 grew within a pH range of 6.0–8.5 other members of the genera Ensifer, Rhizobium, Shinella (optimum pH 7). The temperature range for growth was and Kaistia (,96.9 %); Fig. 1 shows the NJ tree, while determined using yeast malt broth under optimum pH. the ME and MP trees show similar tree topology (data The broth was incubated at different temperatures ranging not shown). Such phylogenetic distinction of strain u T from 20 to 45 C for 3 days and the growth was measured MSSRFBL1 from the rest of the genera in the family turbidometrically at 660 nm. Strain MSSRFBL1T was able Rhizobiaceae was also observed when all the type species to grow well from 25 to 37 uC. A test for utilization of were considered for tree reconstruction (Fig. S1, available electron acceptors in the presence of yeast extract (0.03 %, in IJSEM Online). For a more reliable classification of w/v) was carried out. Propionate, methanol and ethanol T strain MSSRFBL1 , we have considered three housekeeping were used as electron donors at concentrations of genes, recA, dnaK and thrC, which were amplified as 0.1 % (v/v) in the presence of NaHCO3 (0.1 %, w/v) described by Martens et al. (2007). The NJ dendrograms of and media without electron donor served as control. recA (Fig. S2), dnaK (Fig. S3) and thrC (Fig. S4) support Strain MSSRFBL1T was able to utilize propionate but the 16S rRNA gene sequence-based distinction of strain not methanol or ethanol. Chemolithoautotrophy using T MSSRFBL1 from the rest of the taxa in the family Na2S2O3 (1 mM) or Na2S (0.5 mM) as electron donor and Rhizobiaceae. NaHCO3 (0.1 %, w/v) as carbon source could not be 93 Ensifer adhaerens AT (AM181733) 0.01 55 Ciceribacter lividus MSSRFBL1T (JQ230000) 53 Rhizobium leguminosarum 3Hoq18T (U29386) 98 Shinella granuli Ch06T (AB187585) Mycoplana dimorpha TK0055T (D12786) Kaistia adipata Chj404T (AY039817) Rhodobacter capsulatus ATCC 11166T (D16428) Fig. 1. Phylogenetic tree based on 16S rRNA sequences available from the EMBL database (accession numbers in parentheses), reconstructed after multiple alignment of data by CLUSTAL W (Thompson et al., 1994) as described. Bootstrap values based on 1000 replications are given as percentages at branching points. Bar, 0.01 substitutions per nucleotide position by using the neighbour-joining method. http://ijs.sgmjournals.org 4485 R. Kathiravan and others demonstrated as no growth was observed. Utilization of amplified 360 bp stretch was sequenced and showed
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