International Journal of Systematic and Evolutionary Microbiology (2005), 55, 1827–1832
    
    DOI 10.1099/ijs.0.63716-0
    
    Aminobacter ciceronei sp. nov. and Aminobacter lissarensis sp. nov., isolated from various terrestrial environments
    Ian R. McDonald,13 Peter Kampfer,2 Ed Topp,3 Karen L. Warner,1 ¨ 1 Michael J. Cox, Tracy L. Connell Hancock,4 Laurence G. Miller,4 Michael J. Larkin,5 Veronique Ducrocq,5 Catherine Coulter,6 David B. Harper,6 J. Colin Murrell1 and Ronald S. Oremland4
    Correspondence Ian R. McDonald i.mcdonald@waikato.ac.nz
    1 2
    
    Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UK
    
    Institut fur Angewandte Mikrobiologie, Justus-Liebig-Universitat Giessen, D-35390 Giessen, ¨ ¨ Germany Agriculture and Agri-Food Canada, London, Ontario, Canada N5V 4T3 US Geological Survey, 345 Middlefield Rd, MS 480, Menlo Park, CA 94025, USA Questor Centre, Queen’s University Belfast, Belfast BT9 5AG, UK School of Agriculture and Food Science, Queen’s University Belfast, Newforge Lane, Belfast BT9 5PX, UK
    
    3 4 5 6
    
    The bacterial strains IMB-1T and CC495T, which are capable of growth on methyl chloride (CH3Cl, chloromethane) and methyl bromide (CH3Br, bromomethane), were isolated from agricultural soil in California fumigated with CH3Br, and woodland soil in Northern Ireland, respectively. Two pesticide-/herbicide-degrading bacteria, strains ER2 and C147, were isolated from agricultural soil in Canada. Strain ER2 degrades N-methyl carbamate insecticides, and strain C147 degrades triazine herbicides widely used in agriculture. On the basis of their morphological, physiological and genotypic characteristics, these four strains are considered to represent two novel species of the genus Aminobacter, for which the names Aminobacter ciceronei sp. nov. (type strain IMB-1T=ATCC 202197T=CIP 108660T=CCUG 50580T; strains ER2 and C147) and Aminobacter lissarensis sp. nov. (type strain CC495T=NCIMB 13798T=CIP 108661T= CCUG 50579T) are proposed.
    
    The genus Aminobacter was proposed following the transfer of Pseudomonas aminovorans den Dooren de Jong 1926 to Aminobacter aminovorans (Urakami et al., 1992). At the same time, two novel species were described, Aminobacter aganoensis and Aminobacter niigataensis (Urakami et al., 1992). More recently, the closely related species Chelatobacter heintzii (Auling et al., 1993) was also shown to be a member of the genus Aminobacter, as a later heterotypic (formerly subjective) synonym of Aminobacter aminovorans ¨ (Kampfer et al., 2002). The facultatively methylotrophic strain IMB-1T was isolated
    Published online ahead of print on 22 April 2005 as DOI 10.1099/ ijs.0.63716-0. 3Present address: Department of Biological Sciences, University of Waikato, Private Bag 3105, Hamilton, New Zealand. The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains IMB-1T, ER2, C147 and CC495T are AF034798, L20802, AF246220 and AF107722, respectively.
    
    from CH3Br-fumigated soil collected in Irvine, CA, USA (Connell Hancock et al., 1998; Miller et al., 1997), and was initially phylogenetically characterized based on 16S rRNA gene sequence analysis as being closely related to members of the genus Rhizobium in the ‘Alphaproteobacteria’. Strain IMB-1T was able to grow on C1 compounds such as CH3Cl, CH3Br, CH3I and methylated amines as sole carbon and energy sources but was not able to grow on CH3F. Growth also occurred on glucose, acetate and pyruvate; some growth was observed with low levels of methanol (Connell Hancock et al., 1998). No growth or oxidation was observed with methane, formate, propyl iodide, dibromomethane, dichloromethane or difluoromethane (Connell Hancock et al., 1998; Miller et al., 1997; Schaefer & Oremland, 1999). Oxidation of CH3Br in soil was greatly enhanced by addition of CH3Br-grown cells of strain IMB-1T to the soil (Connell Hancock et al., 1998). The facultatively methylotrophic strain CC495T was isolated from the soil of a beech woodland at Lissara House, near
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    Printed in Great Britain
    
    I. R. McDonald and others
    
    Crossgar, County Down, Northern Ireland. Phylogenetic analysis of its 16S rRNA gene sequence indicated that, as with strain IMB-1T, it was closely associated with the genus Rhizobium (Coulter et al., 1999). Strain CC495T, in the presence of cyanocobalamin, was able to grow on CH3Cl and CH3Br as sole carbon and energy sources but was not able to utilize either CH3I or CH3F. However, oxidation of CH3I by CH3Cl-grown cell suspensions was observed. Growth also occurred on methylamine, for which no supplementation of the medium by cyanocobalamin was required (Coulter et al., 1999). The C1 compounds methanol, methane, formaldehyde, formate, methane thiol and dichloromethane did not act as growth substrates, although formate, formaldehyde and methane thiol were oxidized by CH3Cl-grown cell suspensions. Strain CC495T was able to utilize glucose, pyruvate and glycerol as sole carbon and energy sources, but not veratrate or syringate (Coulter et al., 1999). Under microaerophilic or anaerobic conditions, suspensions of CH3Cl-grown cells of strain CC495T catalysed the transhalogenation of the halomethanes CH3Cl, CH3Br and CH3I, i.e. the exchange of various halide ions with the halomethanes (Harper et al., 2000). Several other bacteria have also been isolated that utilize methyl halides as sole sources of carbon (Doronina et al., 1996; Goodwin et al., 1997). These strains have been designated Hyphomicrobium chloromethanicum CM2T (McDonald et al., 2001), Methylobacterium chloromethanicum CM4T (McDonald et al., 2001) and Leisingera methylohalidivorans MB2T (Schaefer et al., 2002). The facultatively methylotrophic strain ER2 was isolated from an agricultural soil in Canada. This strain rapidly degraded the aryl N-methyl carbamate insecticide carbofuran (Topp et al., 1993) and was initially characterized phylogenetically as being closely related to members of the methylotrophic bacteria. Strain ER2 is able to utilize several N-methyl carbamate insecticides as sole sources of carbon and nitrogen. The atrazine-degrading bacterial strain C147 was isolated from farm soil in Canada. It rapidly degraded the herbicide atrazine (Topp et al., 2000). Strain C147 is able to utilize atrazine and other S-triazine herbicides as sole sources of carbon and nitrogen. Here we report the physiological characteristics, fatty acid composition and phylogenetic characterization (based on 16S rRNA gene sequence analysis and DNA–DNA hybridization) for strains IMB-1T, CC495T, ER2 and C147. The complete 16S rRNA gene sequences (McDonald et al., 1997) from strains IMB-1T, CC495T, ER2 and C147 were aligned, using the ARB program (Ludwig et al., 2004), to representative organisms from Aminobacter and related genera, and their phylogenetic positions were determined using the DNADIST, DNAML, DNAPARS and SEQBOOT programs of the PHYLIP package (Felsenstein, 1993). Phylogenetic dendrograms were constructed from the distance data using the Fitch–Margoliash method and the dendrograms were drawn using TreeView version 1.5 (Page, 1996). DNA–DNA hybridization was carried out using the two
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    ¨ methods of Huß et al. (1983) and Kampfer et al. (2002). The two methods gave comparable results, with the exception of hybridization of A. aminovorans and strain CC495T, for which repeat hybridizations gave widely differing values (20?8–72?0 %) in reciprocal hybridizations. These differences in reciprocal hybridization had already been detected ¨ in previous studies (Urakami et al., 1992; Kampfer et al., 2002). This may be due to the presence of plasmids in CC495T; however, no plasmids have been detected in this strain to date. Phenotypic characterization and fatty acid analysis were ¨ carried out as described by Kampfer et al. (1999, 2002), and indicated that IMB-1T, ER2 and C147 were very similar at this level of characterization (Tables 1 and 2). Phylogenetic analysis of the 16S rRNA gene sequences of strains IMB-1T, CC495T, ER2 and C147 (Fig. 1) showed them to be located within the genus Aminobacter (Urakami et al., 1992), as supported by bootstrap values. The 16S rRNA gene of strain IMB-1T had high sequence similarity with A. aminovorans DSM 7048T (99?6 %), A. aganoensis DSM 7051T (99?6 %), A. niigataensis DSM 7050T (99?6 %), C147 (99?6 %) and ER2 (97?8 %). Analysis of the 16S rRNA gene sequence of strain CC495T showed it to be most closely related to A. aminovorans (99?3 %), A. aganoensis (99?2 %) and A. niigataensis (99?2 %). The 16S rRNA gene of strain ER2 had high sequence similarity with A. aganoensis DSM 7051T (97?9 %), A. niigataensis DSM 7050T (97?9 %), IMB-1T (97?8 %), CC495T (97?8 %), C147 (97?8 %) and A. aminovorans DSM 7048T (97?7 %). Analysis of the 16S rRNA gene sequence of strain C147 showed it to be most closely related to A. aganoensis DSM 7051T (99?6 %), A. niigataensis DSM 7050T (99?6 %), IMB-1T (99?6 %), A. aminovorans DSM 7048T (99?5 %) and CC495T (98?9 %). The previously characterized strains of Aminobacter (A. aminovorans DSM 7048T, A. niigataensis DSM 7050T and A. aganoensis DSM 7051T) and strains ER2 (Topp et al., 1993) and C147 (Topp et al., 2000) were tested for their ability to grow on CH3Cl or CH3Br, and then screened by Southern probing and PCR for the presence of genes that code for enzymes involved in degradation of methyl halides (McDonald et al., 2002). However, all strains tested negative, indicating that strains IMB-1T and CC495T are distinct from the other Aminobacter species, representing the only species able to grow on CH3Cl or CH3Br. The previously characterized Aminobacter species (A. aminovorans, A. niigataensis, A. aganoensis) and IMB-1T and CC495T were tested for the ability to degrade atrazine or carbofuran by HPLC analysis of cell suspensions incubated in mineral salts medium. Degradation was tested with the substrate as sole carbon and nitrogen sources in the absence of glucose, or as a sole nitrogen source in the presence of glucose, which supports growth as determined by turbidity. No degradation was detected for any of the strains tested. PCR amplification of genomic DNA using gene-specific primers also indicated that none of the strains possessed the genes atzA (atrazine chlorohydrolase) (de Souza et al., 1996) or mcd
    International Journal of Systematic and Evolutionary Microbiology 55
    
    Two novel Aminobacter species from soils
    
    Table 1. Physiological characteristics of the type strains of Aminobacter species
    +, Positive; 2, negative; (+) weakly positive; pNP, para-nitrophenyl; pNA, para-nitroanilide. Test results given in the table were read after 72 h of incubation at 30 uC. All seven strains were positive for the following: utilization of N-acetyl-D-glucosamine, L-arabinose, D-cellobiose, D-fructose, D-galactose, D-glucose, D-mannose, D-maltose, D-ribose, D-xylose, i-inositol, D-mannitol, D-sorbitol, acetate, 4-aminobutyrate, DL-3-hydroxybutyrate, DL-lactate, oxoglutarate, L-alanine, L-aspartate, L-histidine, L-leucine, L-ornithine, L-proline and L-serine, and hydrolysis of bis-pNP-phosphate, pNP-phenyl phosphonate, L-alanine-pNA and L-proline-pNA. All seven strains were negative for the following: utilization of p-arbutin, a-D-melibiose, salicin, adonitol, maltitol, putrescine, cis-aconitate, trans-aconitate, adipate, azelate, citrate, fumarate, itaconate, mesaconate, suberate, L-phenylalanine, 3-hydroxybenzoate and phenylacetate, hydrolysis of aesculin, pNP b-D-galactopyranoside, pNP b-D-glucuronide, 2-deoxythymidine-59-pNP phosphate and L-glutamate c-3-carboxy-pNA and acid production from lactose, adonitol, rhamnose, methyl D-glucoside, erythritol and melibiose. Test Utilization of: Gluconate
    L-Rhamnose
    
    IMB-1T
    
    ER2
    
    C147
    
    CC495T
    
    A. aminovorans DSM 7048T
    
    A. niigataensis DSM 7050T
    
    A. aganoensis DSM 7051T
    
    Sucrose
    D-Trehalose
    
    Propionate Glutarate
    L-Malate
    
    Pyruvate
    b-Alanine
    L-Tryptophan
    
    4-Hydroxybenzoate Hydrolysis of: pNP a-D-glucopyranoside pNP b-D-glucopyranoside pNP phosphorylcholine Acid produced from:D Glucose Sucrose
    D-Mannitol
    
    (+) + + + + + 2 + + + 2 (+) 2 (+) (+) 2 (+) 2 2 2 2 (+) 2 (+) (+) 2 2 2 (+)
    
    2 + 2 2 + + 2 + (+) 2 2 (+) 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2
    
    2 + 2 2 + + 2 + (+) 2 2 (+) 2 2 2 2 2 2 2 2 2 2 2 2 (+) 2 2 2 2
    
    2 + + + + + 2 + + + 2 2 2 2 (+) (+) (+) 2 2 2 (+) (+) 2 2 (+) 2 2 (+) (+)
    
    2 + +* 2 + + 2 2 2 2 2 + (+) + (+)* (+)* (+)* (+) (+) 2 2 (+)* (+) (+) (+)* (+)* (+) (+) (+)
    
    2 + +* +* 2 2 2 + + 2 + + (+) 2 (+)* (+)* (+)* (+) (+) (+)* (+)* (+) 2 (+)* (+)* (+)* 2 (+)* (+)
    
    2 2 +* +* + + + + + 2 + + (+) (+) (+)* (+)* (+)* 2 2 (+)* (+)* 2* 2 (+)* (+)* 2* 2 (+)* (+)
    
    Dulcitol Salicin Inositol Sorbitol
    L-Arabinose
    
    Raffinose Maltose
    D-Xylose
    
    Trehalose Cellobiose
    D-Arabitol D-Mannose
    
    *Data are in line with those published by Urakami et al. (1992). DAcid formation from carbohydrates in most cases was very weak (even after prolonged incubation). These tests cannot be recommended for differentiation.
    
    (methylcarbamate hydrolase) (Tomasek & Karns, 1989). These genes were found in strains ER2 and C147, respectively, and are widely found in other Gram-negative bacteria that degrade atrazine or carbofuran. Therefore, there is no evidence for the degradation of atrazine or carbofuran by any of the other characterized Aminobacter species. This
    http://ijs.sgmjournals.org
    
    ability of strains ER2 and C147 to degrade atrazine or carbofuran is therefore unique among the Aminobacter species. The result of genotypic and phenotypic investigations justify the proposal of two novel Aminobacter species.
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    I. R. McDonald and others
    
    Table 2. Major fatty acid compositions of type strains of species of the genus Aminobacter
    Values are percentages of total fatty acids. All strains were grown on trypticase soy broth agar at 28 uC for 48 h prior to fatty acid analysis. For unsaturated fatty acids, the position of the double bond is located by counting from the methyl (v) end of the carbon chain; cis and trans isomers are indicated by the suffixes c and t, respectively. Summed features are groups of two or three fatty acids that cannot be separated by GLC with the MIDI system. Summed feature 4 contains 16 : 1v7c and/or 15 : 0 iso 2-OH; summed feature 7 contains 18 : 1v7c, 18 : 1v9t and/or 18 : 1v12t. Unknown fatty acids have no name listed in the peak library file of the MIDI system and therefore cannot be identified. Compound Saturated fatty acids: 9:0 16 : 0 17 : 0 18 : 0 20 : 0 Unsaturated fatty acids: 15 : 1v8c 17 : 1v8c 17 : 1v6c 11-Methyl 18 : 1v7t 19 : 1v12t 20 : 0v6,9c 20 : 1v9t Branched fatty acids: 15 : 0i 17 : 0i 19 : 0i Hydroxy fatty acids: 12 : 0 3-OH 15 : 0i 3-OH Summed features: Summed feature 4 Summed feature 7 Cyclopropane acids: 17 : 0 cyclo 19 : 0 cyclo v8c Unknown 14?966 Unknown 18?081 Unknown 18?597 Unknown 18?804 IMB-1T ER2 C147 CC495T A. aminovorans DSM 7058T 1?0 4?9 0?7 1?5 A. niigataensis DSM 7050T A. aganoensis DSM 7051T
    
    1?1 5?7 1?0 2?9 0?3
    
    6?8 5?0 0?7
    
    6?5 0?7 4?4 0?5
    
    8?9 3?3
    
    6?0 2?0
    
    6?2 2?0
    
    1?3 0?6 18?9 0?6 0?6 14?3 13?4 10?5 1?3 1?0 0?9 0?8 0?7 3?1 3?0 2?9 4?8 0?7
    
    2?4
    
    2?9
    
    2?4 0?5 0?3
    
    2?4
    
    1?0
    
    0?4
    
    0?4
    
    0?3
    
    0?3
    
    0?4
    
    0?4
    
    0?5 59?1
    
    52?7
    
    54?7
    
    69?8
    
    0?5 46?4 0?5 13?7 0?7 24?8 0?5 0?4
    
    1?0 48?6
    
    1?1 64?8
    
    5?6 1?0
    
    15?3 0?8
    
    14?3 0?9
    
    5?0
    
    10?3 21?0 1?8 0?7
    
    4?7 10?9 0?8
    
    Description of Aminobacter ciceronei sp. nov. Aminobacter ciceronei (cic.er.one9i. N.L. gen. n. ciceronei of Cicerone, named after Professor Ralph Cicerone, an American atmospheric chemist who has made many seminal contributions to our understanding of the chemistry of atmospheric trace gases, with particular reference to his work on the biogeochemistry of methyl halides). Gram-negative, rod-shaped cells. Cells are 0?6 mm in diameter and 1?3 mm long. Cells are motile and nonpigmented. Growth is aerobic. Grows on CH3Br, CH3Cl, CH3I and methylamine as sole carbon and energy sources. Further physiological features are given in Table 1. The main fatty acids are C16 : 0 and C18 : 1 (see Table 2). Optimum
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    temperature for growth is 28–30 uC. Optimum pH for growth is 6?5–7?5. G+C content of the DNA is 62?0– 63?7 mol%. Levels of DNA–DNA relatedness to representatives of the genus Aminobacter are indicated in Table 3. The type strain, IMB-1T (=ATCC 202197T=CIP 108660T =CCUG 50580T), was isolated from CH3Br-fumigated agricultural soil at Irvine, CA, USA. Strain ER2 was isolated from soil from Prince Edward Island (Canada) that was enriched with carbofuran-degrading micro-organisms by perfusing it continuously for 4 months with distilled water containing 100 mg carbofuran l21; strain C147 was isolated from a loam soil from a site near Ottawa, Ontario, Canada.
    International Journal of Systematic and Evolutionary Microbiology 55
    
    Two novel Aminobacter species from soils
    
    Fig. 1. Phylogenetic analysis of the 16S rRNA gene sequences of Aminobacter ciceronei sp. nov. strains IMB-1T, ER2 and C147, Aminobacter lissarensis sp. nov. CC495T, other Aminobacter strains and related genera. The dendrogram shows the results of an analysis in which DNADIST was used. Bootstrap values greater than 50 % derived from 100 replicates are also shown. Bar, 1 % sequence divergence, as determined by measuring the lengths of the horizontal lines connecting any two species.
    
    Description of Aminobacter lissarensis sp. nov. Aminobacter lissarensis (liss.ar.en9sis. N.L. masc. adj. lissarensis pertaining to Lissara House in Northern Ireland, where the type strain was isolated). Gram-negative, rod-shaped cells, 0?5–0?6 mm in diameter and 1?3–1?5 mm long. Cells are motile and faintly pinkpigmented. Growth is aerobic. Grows on CH3Cl and CH3Br as sole carbon and energy sources in the presence of cyanocobalamin (1 mg l21). Methyl amine, glucose, pyruvate and glycerol also act as growth substrates without a requirement for supplementation of the medium with cyanocobalamin. C1-compound assimilation is via the serine pathway. Further physiological features are given in Table 1. The main fatty acid is C18 : 1. Optimum temperature for growth is 25 uC. Optimum pH for growth is 6?7–7?2. G+C content of the DNA is 62?5 mol%. Levels of DNA– DNA hybridization of the type strain to representatives of the genus Aminobacter are indicated in Table 3. The type strain, CC495T (=NCIMB 13798T=CIP 108661T
    
    =CCUG 50579T), was isolated from an unpolluted beech woodland soil in County Down, Northern Ireland.
    
    Acknowledgements
    We acknowledge financial support provided by the Natural Environment Research Council (UK) for PhD studentships to K. L. W. and M. J. C., and for an advanced research fellowship to ´ I. R. M. Thanks to Jean Euzeby for advice on naming of the bacterial strains.
    
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