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J. Gen. Appl. Microbiol., 52, 223–234 (2006)

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J. Gen. Appl. Microbiol., 52, 223–234 (2006) J. Gen. Appl. Microbiol., 52, 223–234 (2006) Full Paper Geobacillus toebii subsp. decanicus subsp. nov., a hydrocarbon-degrading, heavy metal resistant bacterium from hot compost Annarita Poli,1 Ida Romano,1 Gaetano Caliendo,4 Giancarlo Nicolaus,3 Pierangelo Orlando,2 Antonio de Falco,4 Licia Lama,1 Agata Gambacorta,1 and Barbara Nicolaus1,* 1 Istituto di Chimica Biomolecolare (ICB), CNR, Via Campi Flegrei 34, 80078 Pozzuoli, Napoli, Italy 2 Istituto di Biochimica delle Proteine (IBP), CNR, Napoli, Italy 3 Istituto di Ricerche di Biologia Molecolare “P. Angeletti” IRBM, Pomezia, Rome, Italy 4 Pomigliano Ambiente s.p.a., Napoli, Italy (Received December 14, 2005; Accepted August 4, 2006) A thermophilic, spore-forming bacterial strain L1T was isolated from hot compost “Pomigliano Environment” s.p.a., Pomigliano, Naples, Italy. The strain was identified by using a polyphasic taxonomic approach. L1T resulted in an aerobic, gram-positive, rod-shaped, thermophilic with an optimum growth temperature of 68°C chemorganotrophic bacterium which grew on hydrocar- bons as unique carbon and energy sources and was resistant to heavy metals. The G؉C DNA content was 43.5 mol%. Phylogenetic analysis of 16S rRNA gene sequence and Random Ampli- fied Polymorphic DNA-PCR (RAPD-PCR) analysis of L1T and related strains showed that it forms within Geobacillus toebii, a separate cluster in the Geobacillus genus. The composition of cellu- lar fatty acids analyses by Gas-Mass Spectroscopy differed from that typical for the genus Geobacillus in that it is lacking in iso-C15 fatty acid, while iso-C16 and iso-C17 were predomi- nant. Isolates grew on a rich complex medium at temperatures between 55–75°C and presented a doubling time (td) of 2 h and 6 h using complex media and hydrocarbon media, respectively. Among hydrocarbons tested, n-decane (2%) was the more effective to support the growth (1 g/L of wet cells). The microorganism showed resistance to heavy metal tested during the growth. Furthermore, intracellular a-galactosidase and a-glucosidase enzymatic activities were de- tectable in the L1T strain. Based on phenotypic, phylogenetic, fatty acid analysis and results from DNA-DNA hybridization, we propose assigning a novel subspecies of Geobacillus toebii, to DSM؍) be named Geobacillus toebii subsp. decanicus subsp. nov., with the type strain L1T .(ATCC BAA 1004؍17041 Key Words——alkanes; DNA-DNA hybridization; fatty acid; Geobacillus; heavy metals; hot compost; lipid; PCR finger print; thermozymes Introduction * Address reprint requests to: Dr. Barbara Nicolaus, Istituto di Industrial composting is a microbial, aerobic, self- Chimica Biomolecolare (ICB), CNR, Via Campi Flegrei 34, 80078 Pozzuoli, Napoli, Italy. heating and solid-phase biodegradation process of Tel: ϩ39–081–8675245 Fax: ϩ39–081–8041770 organic-waste materials (Miller, 1996). During the ther- E-mail: [email protected] mogenic phase of the composting process, a large 224 POLI et al. Vol. 52 central zone remains at temperatures higher than caldoproteolyticus (Chen et al., 2004), G. gargensis 70°C for many weeks (Fugio and Kume, 1991; Strom, (Nazina et al., 2004), and G. jurassicus (Nazina et al., 1985a, b). In this “hot-zone” a high number of ther- 2005) were assigned to the Geobacillus group. mophilic bacteria, forming a different microbial commu- This paper describes the isolation of a new ther- nity, belonging to Thermus, Bacillus and Hy- mophilic Geobacillus strain, designated L1T, from ther- drogenobacter species were identified (Beffa et al., mogenic compost made from 12-week-old organic 1996; Blanc et al., 1999; Lyon et al., 2000; Strom, waste samples, able to grow at temperatures up to 1985a). 75°C. The characteristics of this isolate were com- Thermophiles isolated from compost in recent years pared with its nearest neighbor. Data on L1T strain have become extremely interesting from a technologi- ability to grow using hydrocarbons as unique carbon cal point of view (Lyon et al., 2000; Strom 1985b). sources and its resistance to heavy metals, were also Many are the studies undertaken for defining the prin- reported. cipal metabolic pathways and the peculiar properties of their molecules. Hot compost is considered to offer Materials and Methods a favorable habitat for thermophilic bacilli. Strom (1985b) isolated more than 750 heterotrophic spore- Compost characteristics. Compost samples were forming strains from compost. Most of these microor- from “Pomigliano Environment” s.p.a., Pomigliano ganisms grew under 60°C, and only Bacillus coagu- d’Arco (Campania Region, southern Italy). The first lans, Geobacillus stearothermophilus and Geobacillus step, in the bio-fermentation process, is essentially toebii were isolated at 65°C (Strom, 1985a; Sung et based on a static heap covered by a sandwich consti- al., 2002). Thermophilic bacteria related to the genus tuted of two supports of polyester with interposed a foil Geobacillus has been widely isolated from geothermal of Gore-Tex® and on a forced airing cycle-treatment of and man-made environments throughout the world 30 days. The process is monitored by a computerized (Maugeri et al., 2002; Nazina et al., 2001, 2005; Rhee system (BIOE® s.r.l, Milan, Italy) that checks the oxy- et al., 2002; Sung et al., 2002). gen, the temperature and the humidity levels. The tem- Thermophilic Bacillus species of the group 5 rRNA perature of the inner core of the heap is above 60°C. are a phenotypically and phylogenetic coherent group At 30 days from pretreatment, the pile is moved to the displaying very high similarity among their 16S rRNA threshing floor of maturation where, for a further 60 sequences (98.5–99.2%) (Ash et al., 1991; Rainey et days, it is turned weekly to favor the oxygenation and al., 1994; Sunna et al., 1997); this group was trans- consequently, the degradation of the more slowly ferred to a new genus Geobacillus that comprised biodegradable matrixes (lignin). The material is refined at that time 12 validated species G. stearother- through a phase of drum sifting by obtaining the “com- mophilus, G. thermocatenulatus, G. thermoleovorans, post.” The presence of heavy metals was determined G. kaustophilus, G. thermoglucosidasius, G. thermo- by atomic spectrometry (Shimadzu AA6200) (Poli et denitrificans, G. subterraneus, G. uzenensis, G. cal- al., 2005). Bacterial tests were performed by the meth- doxylosilyticus and G. toebii (Ahmad et al., 2000; ods of Koneman (Koneman, 1984). Claus and Berkeley, 1986; Fortina et al., 2001a, b; Sampling and isolation. Thirty grams of compost Golovacheva et al., 1975; Logan and Berkeley, 1984; (fresh wt) were placed in 200 ml of sterile water, ho- Manichini et al., 2000; Nazina et al., 2001; Priest et al., mogenized at room temperature on a shaker (150 rpm) 1988; Sung et al., 2002; Suzuki et al., 1983; Tomita et for 20 min, and serially diluted (10Ϫ2 to 10Ϫ10) in the TH al., 2003; White et al., 1993; Zarrilla and Perry, 1987). medium (8 g/L peptone (Oxoid), 4 g/L yeast extract Other thermophilic established species belonged to (Oxoid), 2 g/L NaCl (Applichem) at pH 7.0). For opti- Geobacillus group such as Bacillus thermantarcticus mum temperature determination the cultures were in- (Nicolaus et al., 1996) validated in Int. J. Syst. Evol. cubated without agitation from 50°C to 80°C for 1 to 6 Microbiol. 2002 and G. vulcani (Caccamo et al., 2000; days. The pH dependence of growth was tested in the Gugliandolo et al., 2003; Maugeri et al., 2001; Nazina pH range 4.0 to 10.0. Pure strains were isolated at et al., 2004). The asporogenous Saccharococcus ther- 68°C at pH of 7.2 on the TH medium solidified with mophilus representing a separate line of descent (Naz- agar (2%, wt/v). The first pure culture obtained was ina et al., 2001; Nystrand, 1984) and more recently G. called L1T and studied in detail. 2006 Geobacillus toebii subsp. decanicus subsp. nov. 225 Reference strains and media. The reference (10 U), chloramphenicol (10, 50), kanamycin (5, 30), strains used were as follows: Geobacillus toebii DSM tylosin (10, 30), ampicillin (25), gentamicin (10, 30), 14590T (Sung et al., 2002), Geobacillus thermoleovo- novobiocin (30), nystatin (100), cycloheximide (30), rans ATCC 43513T (Zarrilla and Perry, 1987) and bacitracin (10 U), lincomycin (15), fusidic acid (10), Geobacillus caldoxylosilyticus ATCC 42125T. The vancomycin (30), streptomycin (25) and tetracycline media utilized were: TH medium; TH agar medium, (30, 50) (Nicolaus et al., 2000). containing (g/L) 20.0 agar (Oxoid); YN medium, con- Biochemical analysis. For the enzymatic assays, taining (g/L) 6.0 yeast extract, 6.0 NaCl at pH 6.5. cells grown in YN medium were collected during sta- Other media were prepared as follows: M162 min- tionary growth phase by centrifugation at 9,000ϫg for eral medium containing: (g/L) 4.0 NaCl (Applichem), 30 min. Wet cells (about 2.0 g) were suspended in 0.53 NH4Cl (J.T. Baker), Solution A 60 ml/L, Solution B 20 mM Tris-HCl at pH 8.0, lysed by ultrasonic treatment 20 ml/L, Solution C 100 ml/L; Solution A: (g/L) 35.58 (Heat System Instrument) for 4 min, and centrifuged at ϫ Na2HPO4 ·2H2O (Applichem); Solution B: (g/L) 27.19 15,000 g for 20 min. The supernatant (crude extract) KH2PO4 (Carlo Erba); Solution C: (g/L) 1.0 Nitrilotri- was assayed for a-galactosidase and a-glucosidase acetic acid (Applichem), 0.4 CaSO4 ·6H2O (Carlo enzymatic activities, by incubating for 10 min at 68°C a Erba), 2.0 MgCl2 ·6H2O (Applichem), 2.5 Ferric citrate reaction mixture containing in 1 ml final volume: 0.1 ml (Carlo Erba), Nitsch’s trace elements 5.0 ml/L. of the crude extract, 40 mM Tris-HCl pH 7.0 and 1 mM Minimal media were prepared using M162 medium of the following substrates: p-nitrophenyl-a-D-(glucopy- plus either 1% glycerol, glucose, lactose, Na-acetate, ranoside, galactopyranoside, maltoside, arabinoside); mannose, xylose, galactose, sucrose, cellobiose, ri- p-nitrophenyl-b -(glucopyranoside, xylopyranoside, bose, maltose, fructose, ethanol, EDTA, sorbose, raffi- galactopyranoside, lactopyranoside, maltoside); p-ni- nose, malic acid, citric acid or trehalose as sole carbon trophenyl N-acetyl-b-D-glucosamide and 2-nitrophenyl- sources, at pH 7.2 (Maugeri et al., 2002).
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