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Geobacillus Subterraneus Subsp. Aromaticivorans Subsp. Nov., a Novel Thermophilic and Alkaliphilic Bacterium Isolated from a Hot Spring in Sırnak, Turkey

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Geobacillus Subterraneus Subsp. Aromaticivorans Subsp. Nov., a Novel Thermophilic and Alkaliphilic Bacterium Isolated from a Hot Spring in Sırnak, Turkey J. Gen. Appl. Microbiol., 58, 437‒446 (2012) Full Paper Geobacillus subterraneus subsp. aromaticivorans subsp. nov., a novel thermophilic and alkaliphilic bacterium isolated from a hot spring in Sırnak, Turkey Annarita Poli,1,* Kemal Guven,2 Ida Romano,1 Hamsi Pirinccioglu,2 Reyhan Gul Guven,3 Jean Paul Marie Euzeby,4 Fatma Matpan,2 Omer Acer,2 Pierangelo Orlando,5 and Barbara Nicolaus1 1 Consiglio Nazionale delle Ricerche (C.N.R.), Istituto di Chimica Biomolecolare (I.C.B.), Via Campi Flegrei 34, 80078, Pozzuoli, Napoli, Italy 2 Department of Biology, Faculty of Science, Dicle University, 21280, Diyarbakir, Turkey 3 Department of Science Teaching, Faculty of Ziya Gokalp Education, Dicle University, 21280, Diyarbakir, Turkey 4 Société de Bactériologie Systématique et Vétérinaire, France 5 Consiglio Nazionale delle Ricerche (C.N.R.), Istituto di Biochimica delle Proteine (I.B.P.), Via P. Castellino 111, 80131 Napoli, Italy (Received April 2, 2012; Accepted September 20, 2012) A new thermophilic spore-forming strain Ge1T was isolated from the Guclukonak hot spring in Sırnak, Turkey. The strain was identifi ed by using a polyphasic taxonomic approach. Strain Ge1T was Gram-positive, spore-forming, alkaliphilic rod-shaped, motile, occurring in pairs or fi lamen- tous. Growth was observed between 30 and 65°C (optimum 60°C) and at pH 5.5‒10.0 (optimum pH 9.0). It was capable of utilizing starch, growth was observed at 0‒3% NaCl (w/v) and was positive for catalase and urease. The major cellular fatty acids were iso-C15:0 and iso-C17:0, and the predominant lipoquinone found was menaquinone MK7 type. The DNA G+C content of the genomic DNA of strain Ge1T was 52.0%. Comparative 16S rRNA gene sequence studies showed that the isolate belonged to the genus Geobacillus. The DNA-DNA hybridization mean values between the representative strain Ge1T and the closely related species G. subterraneus, G. ther- modenitrifi cans, G. thermocatenulatus, G. vulcani and G. thermoleovorans were 69.3%, 57%, 37%, 27% and 26%, respectively. The results of DNA-DNA hybridization, physiological and bio- chemical tests allowed genotypic and phenotypic differentiation of strain Ge1T. Based on these results, we propose assigning a novel subspecies of Geobacillus subterraneus, to be named as Geobacillus subterraneus subsp. aromaticivorans subsp. nov. with the type strain Ge1T (DSM 23066 T= CIP 110341T). Key Words—DNA-DNA hybridization analysis; Geobacillus subterraneus subsp. aromaticivorans subsp. nov.; lipids; taxonomy; thermophile Introduction * Corresponding author: Dr. Annarita Poli, Consiglio Nazion- On the basis of physiological characteristics, the re- ale delle Ricerche (C.N.R.), Istituto di Chimica Biomolecolare sults of fatty acid analysis, DNA-DNA hybridization (I.C.B.), Via Campi Flegrei 34, 80078, Pozzuoli, Napoli, Italy. studies and 16S rRNA gene sequence analysis, Nazi- Tel: +390818675311 Fax: +390818041770 E-mail: apoli＠icb.cnr.it na et al. (2001) proposed a new genus, Geobacillus The GenBank/EMBL/DDBJ accession number for the 16S gen. nov., containing subsurface isolates as two new rRNA gene sequence of strain Ge1T is HE613733. species, Geobacillus subterraneus sp. nov. and Geoba- 438 POLI et al. Vol. 58 cillus uzenensis sp. nov. They also proposed the trans- pared with its near neighbor and on the basis of fer of the validly described species of group 5, Bacillus DNA-DNA hybridization values and biochemical prop- stearothermophilus, Bacillus thermocatenulatus, Bacil- erties, we propose that it represents a novel subspe- lus thermoleovorans, Bacillus kaustophilus, Bacillus cies of Geobacillus subterraneus. thermoglucosidasius and Bacillus thermodenitrifi cans to Geobacillus as the new combinations G. stearother- Materials and Methods mophilus, G. thermocatenulatus, G. thermoleovorans, G. kaustophilus, G. thermoglucosidasius and G. ther- Location of sampling. Bacteria were isolated from modenitrifi cans, respectively. The Geobacillus species the mud of Guclukonak hot spring in Sırnak which is a are a phenotypically and phylogenetically coherent city in the southeast of Turkey. The temperature and group of thermophilic bacilli. The 16S rRNA gene se- pH of the muddy water were 60°C and 6.9, respec- quence heterogeneity within the genus is 92.6% (Na- tively. The hot spring water contained Ca, Mg, SO4, Cl zina et al., 2001). At present, this genus includes the and hydrogen sulphide. following species: Geobacillus stearothermophilus Culture medium and growth condition. All samples (Nazina et al., 2001), G. thermocatenulatus (Golavache- were immediately incubated in the temperature range va et al., 1975), G. thermoleovorans (Zarilla and Perry, 25‒ 70°C in Nutrient Broth (NB medium, Oxoid). Cul- 1987), G. kaustophilus, G. thermoglucosidans (nom. tures were purifi ed from the samples grown in the solid corrig., formerly ‘thermoglucosidasius’) (Coorevits et NB medium, containing 2% agar (Oxoid), at 60°C. Af- al., 2011; Nazina et al., 2001), G. thermodenitrifi cans ter 1 week of incubation a number of cream colonies (Manachini et al., 2000), G. subterraneus and G. uzen- had developed. They were purifi ed using the repeated ensis (Nazina et al., 2001), G. toebii (Sung et al., 2002), serial dilution technique followed by re-streaking on G. lituanicus (Kuisiene et al., 2004), G. vulcani and G. the solid NB medium and the purity of the isolates was gargensis (Nazina et al., 2004), G. debilis (Banat et al., examined based on cell shape under a microscope 2004), G. tepidamans (Schäffer et al., 2004), G. cal- and colony homogeneity on the plates. Several iso- doxylosilyticus (Ahmad et al., 2000; Fortina et al., 2001) lates were selected and the taxonomic properties of and G. jurassicus (Nazina et al., 2005), which have strain Ge1T will be presented in this paper. Subcultur- growth temperatures ranging from 35 to 78°C. G. pal- ing was performed on the same medium for 24 h at lidus (Banat et al., 2004) has recently been transferred 60°C and isolates were maintained as glycerol stock at to the genus Aeribacillus (Miñana-Galbis et al., 2010). -70°C for further studies. Moreover, a recent study (Dinsdale et al., 2011) de- Geobacillus subterraneus DSM 13552T, G. thermod- scribed the emendation of G. thermoleovorans and G. enitrifi cans DSM 466T, G. thermocatenulatus DSM thermocatenulatus with the merger of G. kaustophilus, 730T, G. vulcani DSM 13174T, G. thermoleovorans DSM G. lituanicus, G. thermoleovorans subsp. strombolien- 5366T, G. stearothermophilus DSM22T, G. uzenensis sis and G. vulcani to G. thermoleovorans, and the DSM13551T, G. jurassicus DSM 15726T, G. gargensis merger of G. thermocatenulatus and G. gargensis to G. DSM 15378T, G. kaustophilus DSM 7263T and G. li- thermocatenulatus. In addition, Bacillus thermantarcti- tuanicus DSM 15325T were obtained from the Deutsche cus, proposed at fi rst with the name of the genus “Ba- Sammlung von Mikroorganismen und Zellkulturen, cillus” by Nicolaus et al. (1996), was recently trans- Brunschweig, Germany (DSMZ) and were grown ac- ferred to genus Geobacillus as G. thermantarcticus; cording to the DSMZ catalogue. moreover, the same authors transferred G. tepidamans Morphological and physiological tests. The tem- to Anoxybacillus as A. tepidamans (Coorevits et al., perature range for growth was determined by incubat- 2011). ing the isolate from 25 to 75°C. For the spore formation . With the ultimate goal of studying the microbial com- test, enrichment medium plus 0.001% (w/v) MnCl2 4H2O munity present in the Guclukonak hot spring in Sırnak, was used. The pH tolerance of strains was tested at located in the southeast of Turkey, some thermophilic 60°C at different pH values by using buffered NB me- bacilli from the mud were isolated. dium (50 mM MES, HEPES, TAPS and CAPSO) over In this paper, a novel member of the genus Geoba- these pH values: 5.0, 5.5, 6.0, 6.5, 7.5, 8.0, 8.5, 9.0, cillus is reported on the basis of a polyphasic ap- and 10.0. In order to study the utilization of single car- proach. The characteristics of this isolate are com- bon sources, the isolates were grown statically using 2012 Geobacillus subterraneus subsp. aromaticivorans 439 M162 minimal medium (Poli et al., 2006). The organic (Poli et al., 2012). compounds tested (1%, w/v) were D-glucose, D-lac- Lipid and fatty acid compositions. Polar lipids were tose, D-maltose, D-fructose, D-galactose, D-xylose, D- obtained from 3.0 g of freeze-dried cells grown in aer- mannose, D-trehalose, glycerol, D-cellobiose, sodium obic conditions on NB medium at 60°C and harvested acetate and sucrose. In order to test the capability to use at the stationary growth phase. Polar lipids were ex- hydrocarbons, the NB medium was diluted (15 times) tracted with CHCl3/MeOH/H2O (65：25：4, by vol.). and 1% (v/v) hydrocarbons were added and incubated The lipid extract was analyzed by thin layer chroma- for 72 h. All growth tests were done at 60°C and the tography (TLC) on silica gel (0.25 mm, F254, Merck) growth was scored positive if the A540nm was greater eluted with CHCl3/MeOH/H2O (65：25：4, by vol.). All than 0.300 after 3 days. Cellular morphology and mo- polar lipids were detected by spraying the plates with tility were determined by phase-contrast microscopy 0.1% (w/v) Ce(SO4)2 in 2 N H2SO4 followed by heating (Zeiss) and colony morphology was determined with a at 100°C for 5 min. Phospholipids and aminolipids Leica M8 stereomicroscope using cultures grown on were detected on the plates upon spraying with the media NB agar plates for 24 h at the optimal tempera- Dittmer-Lester and the ninhydrin reagents, respective- ture. Gram staining and KOH test were performed as ly, and glycolipids were visualized with α-naphtol (Ni- previously reported (Poli et al., 2009). colaus et al., 2001). Polar lipids were also identifi ed by Unless otherwise stated the strain was character- 1H-NMR spectra.
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