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1 Institut für Mikrobiologie, Kurt-Mothes-Str. 3, Martin-Luther-Universität Halle-Wittenberg, D-06099 Halle, Germany
2 Biozentrum, Weinbergweg 22, Martin-Luther-Universität Halle-Wittenberg, D-06099 Halle, Germany
3 Umweltforschungszentrum Leipzig-Halle, Department Umweltmikrobiologie, Permoserstr. 15, D-04318 Leipzig, Germany
4 Institut für Mikrobiologie, Universität Hannover, Schneiderberg 50, D-30167 Hannover, Germany
5 Institute Français du Pétrole, 1-4, avenue de Bois-Préau, 92852 Rueil-Malmaison, France
Correspondence
Ute Lechner
ute.lechner{at}mikrobiologie.uni-halle.de
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ABSTRACT |
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-hydroxybutyrate (PHB) granules are formed. The DNA G+C content is 69–70.5 mol% and the main ubiquinone is Q-8. The major cellular fatty acids are 16 : 1 cis-9 and 16 : 0 and the only hydroxy fatty acid is 10 : 0 3-OH. The major phospholipids are phosphatidylethanolamine (PE) 16 : 1/16 : 1 and phosphatidylglycerol 16 : 0/16 : 1. A significant amount of PE 17 : 0/16 : 1 is present. The 16S rRNA gene sequences of these strains are almost identical and form a separate line of descent in the Rubrivivax–Roseateles–Leptothrix–Ideonella–Aquabacterium branch of the Betaproteobacteria with 97 % similarity to 16S rRNA genes of the type strains of Rubrivivax gelatinosus, Leptothrix mobilis and Ideonella dechloratans. However, physiological properties, DNA–DNA relatedness values and the phospholipid and cellular fatty acid profiles distinguish the novel isolates from the three closely related genera. Therefore, it is concluded that strains L10T, L108 and CIP I-2052 represent a new genus and novel species for which the name Aquincola tertiaricarbonis gen. nov., sp. nov., is proposed. The type strain is strain L10T (=DSM 18512T=CIP 109243T).
-hydroxybutyrate; PE, phosphatidylethanolamine; PG, phosphatidylglycerol; PL, phospholipids; TBA, tert-butanolThe GenBank/EMBL/DDBJ accession number for the partial 16S rRNA gene sequence of strain L10T is DQ656489.
Present address: Applera Europe B.V., LC-MS Support, Grundstrasse 10, 6343 Rotkreuz, Switzerland. 
Present address: Aquatische Biotechnologie, Biofilm-Zentrum, Universität Duisburg-Essen, Geibelstr. 41, D-47057 Duisburg, Germany.
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; Lopes Ferreira et al., 2006a). Their resistance to degradation is thought to be caused by both the presence of the ether bond and the tertiary carbon atom in these compounds. Aerobic degradation is proposed to proceed via tert-butanol (TBA) and 2-hydroxyisobutyric acid (2-HIBA), two intermediates in which the tertiary butyl moiety is retained (Fig. 1) and which also show resistance to bacterial attack. To achieve complete degradation, several enzymes have to react with the bulky tertiary butyl group, supposedly involving special monooxygenases, dehydrogenases, hydrolases and other enzymes. To date, only a few bacteria able to use MTBE as a sole carbon and energy source have been identified: Hydrogenophaga flava ENV735 (Hatzinger et al., 2001), two strains of Mycobacterium austroafricanum (François et al., 2002; Lopes Ferreira et al., 2006b) and Methylibium petroleiphilum PM1T (Nakatsu et al., 2006).
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). Based on the 16S rRNA gene sequences, the closest relative to these strains was another TBA-degrading strain, CIP I-2052, isolated from a wastewater treatment plant near Paris, France (Piveteau et al., 2001). This latter strain was consequently included in the current study. Here we present the results of phenotypic, chemotaxonomic and phylogenetic studies of the three TBA- or MTBE-degrading strains which support their placement in a new taxon within the Rubrivivax–Roseateles–Leptothrix–Ideonella–Aquabacterium branch of the class Betaproteobacteria.
Strains L10T, L108 and CIP I-2052 were routinely cultivated aerobically in mineral salt medium consisting of 0.11 mM NH4Cl, 2.5 mM KH2PO4, 2.5 mM K2HPO4, 0.025 mM CaCl2, 0.29 mM MgSO4, 1.5 µM ZnSO4, 3.6 µM MnSO4, 3.1 µM CuSO4, 1 µM Na2MoO4, 18 µM FeSO4 and the following vitamins (in µg l–1): biotin, 20; folic acid, 20; pyridoxine-HCl, 100; thiamine-HCl, 50; riboflavin, 50; nicotinic acid, 50; Ca-pantothenate, 50; p-aminobenzoic acid, 50 and lipoic acid, 50. Cobalt ions were usually added to the mineral salt medium at 50 µg cobalt l–1 or cobalt was replaced by cyanocobalamin at 50–100 µg l–1. MTBE, TBA or 2-HIBA were usually added at a concentration of 2, 5 and 10 mM, respectively. Cultivation with MTBE was carried out in serum bottles closed with a Teflon-sealed cap to prevent loss of MTBE by volatilization and containing sufficient headspace to provide enough oxygen for the complete oxidation of MTBE. The strains grew well on low-nutrient complex medium R2A (Reasoner & Geldreich, 1985) and formed white, circular colonies on solid medium, but failed to grow on rich media such as trypticase soy agar (Difco). Strain L108 easily lost the ability to degrade MTBE during subcultivation on R2A (Rohwerder et al., 2006), but degradation of TBA and of the intermediate 2-HIBA was a stable property in this and the other two strains.
Gram-staining was performed according to standard procedures (Gerhardt et al., 1994). Cell motility and morphology were investigated by phase-contrast microscopy and transmission electron microscopy using cells from the late exponential growth phase grown in mineral medium with 5 mM glucose or in R2A liquid medium. Cells were Gram-negative rods (0.8–1.1x1.2–2.3 µm) and motile by means of a single polar flagellum (Fig. 2a). Two types of pili were attached to the cells: thin pili (diameter 6 nm) forming an extended network around the cells (Fig. 2b) and thick, probably conjugation pili (diameter 55 nm, not shown). The cells accumulated large amounts of poly -hydroxybutyrate (PHB) granules (Fig. 2c). The accumulation of PHB was confirmed by staining whole cells with Nile red and by observation under a fluorescence microscope (excitation and emission wavelengths 488 and 600 nm, respectively) (Müller et al., 1999) and by GC analysis after extraction and acid propanolysis (Breuer et al., 1995).
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) of L10T (GenBank accession no. DQ656489) and L108 (DQ436455; Rohwerder et al., 2006), amplified using primers fD1 and rP2 (Weisburg et al., 1991), were identical, whereas the sequence of strain CIP I-2052 (AF244133; Piveteau et al., 2001) differed in two bases. The next closest sequences of cultivated bacteria in the EMBL database showed 97–98 % sequence similarity. Among these were the sequences of four species with validly published names which exhibited 97 % similarity and belonged to three different genera: Rubrivivax gelatinosus DSM 1709T, Ideonella dechloratans CCUG 30977T, Leptothrix mobilis DSM 10617T and Leptothrix cholodnii [strains LMG 7171 (=CCM 1827) and LMG 8142; Spring et al., 1996]. A more distant relationship (96 % sequence similarity) was suggested for Rubrivivax benzoatilyticus ATCC BAA-35T (Ramana et al., 2006), Roseateles depolymerans DSM 11813T (Suyama et al., 1999), Mitsuaria chitosanitabida IAM 14711T (Amakata et al., 2005), Leptothrix discophora LMG 8141T and Azohydromonas lata IAM 12599T (basonym: Alcaligenes latus; Xie & Yokota, 2005). The other related MTBE-degrading betaproteobacterium, Methylibium petroleiphilum PM1T (Nakatsu et al., 2006), exhibited 95.6 % 16S rRNA gene sequence similarity to strains L10T and L108 and showed a distinctly deeper branching in the phylogenetic tree (Fig. 3). The tree demonstrates the placement of the isolates in the Rubrivivax–Roseateles–Leptothrix–Ideonella–Aquabacterium branch (Manaia et al., 2003), which diverges from the phylogenetic lineage of the family Comamonadaceae (Wen et al., 1999).
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and the species description. Tests for cytochrome oxidase and catalase were performed according to standard procedures (Gerhardt et al., 1994). Substrate utilization was studied in mineral medium supplemented with the carbon sources at concentrations between 2 and 10 mM and monitored by the increase in optical density (600 nm). API 20NE biochemical tests were performed according to the manufacturer's (bioMérieux) instructions. Use of Biolog GN microplates was not suitable for the characterization of the isolates, as has also been found for I. dechloratans CCUG 30977T (Malmqvist et al., 1994). Photoheterotrophic growth was studied in anaerobic medium 27 (DSMZ). Bacteriochlorophyll a was monitored at 870 nm in intact and ultrasonicated cells as previously described (Suyama et al., 1999) using Rubrivivax gelatinosus DSM 1709T grown anaerobically in the light as a positive control. Oxidation of Mn2+ to Mn4+ was followed by the formation of dark brown colony pigmentation during growth on MnSO4-containing medium 803 (DSMZ). The capability to grow at the expense of chlorate reduction was tested in anaerobic mineral medium containing 25 mM acetate and 10 mM potassium chlorate.
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). The prominent common feature of strains L10T, L108 and CIP I-2052 is the capability to grow with compounds containing a tertiary alkyl moiety such as TBA, 2-HIBA or tert-amylalcohol. Strain L108 was also able to grow with ETBE and methyl tert-amylether. Utilization of 2-HIBA was not observed for Rubrivivax gelatinosus DSM 1709T, I. dechloratans CCUG 30977T or L. mobilis DSM 10617T (Table 1
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All strains investigated in this study were compared by using the API 20NE test. All strains investigated were oxidase-positive and gave negative results in tests for arginine dihydrolase, urease, -galactosidase, aesculin hydrolysis, utilization of L-arabinose, capricate, phenylacetate, citrate and adipate, fermentation of glucose and nitrate reduction. Strains L10T, L108 and CIP I-2052 can be easily differentiated from members of the genera Rubrivivax, Leptothrix and Ideonella by their ability to utilize a broader range of carbohydrates such as mannose, mannitol and N-acetylglucosamine (Table 1). Furthermore, three physiological features essential for the description of the genera Rubrivivax, Leptothrix or Ideonella, photoheterotrophic growth, oxidation of manganese and reduction of chlorate, were absent in strain L10T (Table 1). Unlike species of the genus Rubrivivax (Willems et al., 1991), strain L10T did not grow photoheterotrophically. It did not produce bacteriochlorophyll a under aerobic conditions, as has been described for Roseateles depolymerans (Suyama et al., 1999), another related species (Fig. 3). Strains L10T, L108 and CIP I-2052, as well as Rubrivivax gelatinosus DSM 1709T and I. dechloratans CCUG 30977T, lacked the typical ability of members of the genus Leptothrix to oxidize Mn2+ (Siering & Ghiorse, 1996; Spring et al., 1996). Strain L10T did not grow with chlorate and acetate as the electron acceptor and donor, respectively, when compared with I. dechloratans CCUG 30977T as a positive control (Malmqvist et al., 1994). Strain L10T was also unable to grow anaerobically with nitrate (10 mM) as the electron acceptor as described for I. dechloratans (Malmqvist et al., 1994) using glucose, 2-HIBA or 3-hydroxybutyrate as carbon sources.
DNA–DNA hybridization experiments were carried out on isolated DNA and renaturation rates were measured using the spectrophotometric method (De Ley et al., 1970) as previously described (Auling et al., 1986). DNA from cells of strain L10T showed the highest degree of binding (D) (100 %) to DNA of strains L108 and CIP I-2052. The same D value was obtained during DNA–DNA hybridization of strains L108 and CIP I-2052. DNA–DNA relatedness values of greater than 70 % indicate a relationship at the species level, therefore, strains L10T, L108 and CIP I-2052 must be members of the same species. The D values for DNA–DNA hybridization of strain L10T and Rubrivivax gelatinosus DSM 1709T, L. mobilis DSM 10617T and I. dechloratans CCUG 30977T were 43 %, 49.4 % and 57.6 %, respectively, reflecting a low but distinct phylogenetic distance of strain L10T from all three of the reference organisms. It is probable that the genera of this phylogenetic radiation are shallow phylogenetic taxa that evolved over a relatively short period, as has been suggested for some other aerobic Proteobacteria (Stackebrandt 2006). For Mitsuaria chitosanitabida, another bacterium of the Rubrivivax–Roseateles–Leptothrix–Ideonella–Aquabacterium branch, high D values with related genera have been reported, albeit derived from a different method of solution DNA–DNA hybridization (Amakata et al., 2005).
The G+C content of DNA was determined by HPLC after digestion to the nucleoside level as described previously (Breitenstein et al., 2002). The DNA G+C contents of strains L10T, L108 and CIP I-2052 were 70.5, 69.8 and 69 mol%, respectively.
Chemotaxonomic properties of strains L10T, L108 and CIP I-2052 were compared with those of the reference strains. The isoprenoid quinones were extracted and analysed by HPLC as previously described (Lechner et al., 1995). All strains contained an ubiquinone with eight isoprene units (UQ-8). As no menaquinone was detected in strains L10T, L108 and CIP I-2052, they differed from Rubrivivax gelatinosus DSM 1709T, which contained a menaquinone in addition to UQ-8. Cellular fatty acids were extracted from R2A-grown cells and analysed as previously described (Härtig et al., 2005). The fatty acids of strain L10T were, in order of amount detected (mean values of triplicate analysis): 16 : 1 cis-9 (39 %), 16 : 0 (37 %), 18 : 1 (6 %), 12 : 0 (4 %), 15 : 0 (3 %), 10 : 0 3-OH (2 %), 14 : 0 (2 %), 15 : 1 (2 %), 17 : 0 (2 %), 17 : 0 cyclo (2 %) and 18 : 0 (1 %). The fatty acid contents of strains L108 and CIP I-2052 were essentially the same. A comparison of the fatty acids of Rubrivivax gelatinosus DSM 1709T, L. mobilis DSM 10617T and I. dechloratans CCUG 30977T grown under the same conditions revealed a very similar profile with 16 : 1 cis-9, 16 : 0 and 18 : 1 as predominant components. This finding was in accordance with previously published data (Hiraishi et al., 1991; Spring et al., 1996). However, fatty acids 17 : 0, 17 : 0 cyclo and 15 : 1 present in strains L10T, L108 and CIP I-2052 were absent in Rubrivivax gelatinosus DSM 1709T and L. mobilis DSM 10617T or only detectable in minor amounts (0.5 %) in I. dechloratans CCUG 30977T. The latter clearly differed from strains L10T, L108, CIP I-2052 and also from Rubrivivax gelatinosus DSM 1709T and L. mobilis DSM 10617T in possessing considerable amounts of the (diagnostic) hydroxy fatty acids 12 : 0 2-OH (2 %), 12 : 0 3-OH (4 %) and 14 : 0 2-OH (2 %).
Phospholipids (PL) were extracted from cells grown in liquid R2A medium by a single phase chloroform/methanol/buffer solvent and purified as previously described (White & Ringelberg, 1998). The polar lipid fraction containing glycerophospholipids was analysed by LC electrospray-ionization tandem mass spectrometry (LC-ESI-MS-MS) as previously described (Curtis et al., 2006; Lytle et al., 2000) on a mass spectrometer (4000 QTRAP; Applied Biosystems/MDS Sciex) coupled to an LC system (1100 series; Agilent). The profiles of the major PL of strains L10T, L108, CIP I-2052 and the reference strains are shown in Table 2. Molecular species of phosphatidylglycerol (PG) and phosphatidylethanolamine (PE) with fatty acids 16 : 0 and/or 16 : 1 amounted to 22–29 and 43–58 %, respectively. The high percentage of PG and PE lipids is in accordance with PL patterns of other members of the Rubrivivax–Roseateles–Leptothrix–Ideonella–Aquabacterium branch (Manaia et al., 2003) and the family Comamonadaceae (Jeon et al., 2004; Blümel et al., 2001). Headgroups of about 23–34 % of total PL of the novel isolates and the reference organisms could not be assigned specifically because neither the molecular ion nor the diagnostic fragments were in accordance with published data (Lytle et al., 2000) or with the calculated molecular masses of common phospholipids. An unknown PL has also been reported for Xenophilus azovorans (Blümel et al., 2001). Strains L10T, L108 and CIP I-2052 contained significant amounts of PE with 17 : 0 and/or 17 : 0 cyclo fatty acids (not distinguishable by LC-MS) in conjunction with 16 : 1 (m/z 702.5, Table 2). Interestingly, this phospholipid was absent in Rubrivivax gelatinosus DSM 1709T, I. dechloratans CCUG 30977T and L. mobilis DSM 10617T. On the other hand, the reference strains contained PE with 16 : 0 or 16 : 1 combined with 14 : 0 and 14 : 1 (m/z 662.5 and 672.5, Table 2), respectively, which were not detected in the novel isolates. Finally, a principal component analysis (PCA) was performed based on the occurrence and relative amounts of phospholipids and this indicated that strains L10T, L108 and CIP I-2052 formed a cluster that was different from the other genera in question (Fig. 4).
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Description of Aquincola gen. nov.
Aquincola (A.quin'co.la. L. n. aqua water; L. masc. n. incola inhabitant; N.L. masc. n. Aquincola inhabitant, dweller of water).
Cells are 0.8–1.1 µm wide and 1.2–2.3 µm long. Cells are motile by means of a polar flagellum. Endospores are not formed. Gram-negative. Obligately aerobic. Oxidase-positive. Catalase activity is weakly positive. Tests for phototrophic growth, manganese oxidation and chlorate reduction are negative. The major respiratory quinone is UQ-8. The major cellular fatty acids are 16 : 1 cis-9 and 16 : 0; the only hydroxy fatty acid is 10 : 0 3-OH. The major phospholipids are PE 16 : 0/16 : 0 and PG 16 : 0/16 : 1. A significant amount of PE 17 : 0 and/or 17 : 0 cyclo/16 : 1 is present. The DNA G+C content is 69–70.5 mol% (as determined by HPLC). Phylogenetically, the genus belongs to the class Betaproteobacteria and can be recognized by the 16S rRNA gene sequence. The type species is Aquincola tertiaricarbonis.
Description of Aquincola tertiaricarbonis sp. nov.
Aquincola tertiaricarbonis [ter.ti.a.ri.car'bo.nis. N.L. adj. (numeral) tertiarius tertiary (the third of the kind); L. gen. n. carbonis of carbon; N.L. gen. n. tertiaricarbonis from tertiary carbon, the characteristic utilized substrate].
Displays the following properties in addition to those given in the genus description. Colonies are white, smooth and circular and about 2 mm in diameter. In all stages of cultures grown on R2A or mineral medium, subpopulations of smaller (0.8x1.2 µm) and larger (1x2 µm) cells occur. Thin and thick pili are formed. Large amounts of PHB granules accumulate in the late exponential phase. The temperature range for growth is between 4 and 40 °C, with optimum growth at 30 °C. No growth occurs below 4 °C and above 40 °C. The optimum pH for growth is between 6 and 7. No growth occurs at pH 5 and pH 9. Nitrate is not reduced. No production of urease, arginine dihydrolase, gelatinase, -galactosidase or indole. Aesculin is not hydrolysed. Acetate, butyrate, DL-3-hydroxybutyrate, lactate, pyruvate, fumarate, glutarate, D-glucose, D-mannose, D-mannitol, D-maltose, N-acetylglucosamine, DL-leucine, L-alanine, L-isoleucine, L-asparagine and L-valine are assimilated, but ethanol, L-arabinose, formate, capricate, adipate, citrate, phenylacetate, phenol, 3,4-dihydroxybenzoate and benzoate are not utilized for growth. Compounds containing a tertiary alkyl moiety such as TBA, tert-amylalcohol and 2-HIBA are used as substrates for growth. Tert-butyl formate is also utilized. The DNA G+C content of the type strain is 70.5 mol% as determined by HPLC.
The type strain, strain L10T (=DSM 18512T=CIP 109243T), was isolated from an MTBE-contaminated aquifer in Leuna, Germany.
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ACKNOWLEDGEMENTS |
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