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Int J Syst Evol Microbiol 56 (2006), 867-871; DOI  10.1099/ijs.0.64089-0
© 2006 International Union of Microbiological Societies

Aquitalea magnusonii gen. nov., sp. nov., a novel Gram-negative bacterium isolated from a humic lake

Hoi-Ting Lau, John Faryna and Eric W. Triplett

Department of Microbiology and Cell Science, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL 32611-0700, USA

Correspondence
Eric W. Triplett
ewt{at}ufl.edu


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A Gram-negative, rod-shaped, non-spore-forming betaproteobacterium (TRO-001DR8T) was isolated from humic-lake samples collected from northern Wisconsin, USA. On the basis of 16S rRNA gene sequence analysis, strain TRO-001DR8T belonged to the family Neisseriaceae, and the phylogenetic distance from its closest relative, Chromobacterium violaceum, was 95 %. Strain TRO-001DR8T lacked the violet pigmentation of C. violaceum and shared only 26 % DNA–DNA relatedness with C. violaceum. The DNA G+C content of strain TRO-001DR8T was 59 mol%. The predominant fatty acids were C16 : 1{omega}7c + C16 : 1{omega}7c 2-OH iso (52·5 %), C16 : 0 (21·7 %), C18 : 1{omega}7c (8·0 %) and C12 : 0 (5·1 %). Strain TRO-001DR8T grew optimally at 35 °C and pH 6·0, did not utilize sucrose, but did use glucose, some organic acids and most protein amino acids. Biochemical, physiological, chemotaxonomic and phylogenetic analyses showed that strain TRO-001DR8T could not be assigned to any known genus of the Betaproteobacteria. Therefore, the isolate represents a novel genus and species, for which the name Aquitalea magnusonii gen. nov., sp. nov. is proposed. The type strain is TRO-001DR8T (=ATCC BAA-1216T=BCCM/LMG 23054T).

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain TRO-001DR8T is DQ018117.

A table showing some genotypic, phenotypic and nutritional characteristics that distinguish strain TRO-001DR8T from related betaproteobacteria is available as supplementary material in IJSEM Online.


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As part of an analysis of microbial diversity in lakes, we have been culturing novel organisms from humic and oligotrophic lakes. This work describes the isolation and characterization of a novel betaproteobacterium, strain TRO-001DR8T, from Trout Bog Lake in northern Wisconsin, USA (46·03° N 89·69° W). This facultatively anaerobic strain was isolated by dilution to extinction on dilute R2A medium (Difco). A sample (1 l) of surface water was collected in June 2004 and filtered through a 100 µm mesh filter and shipped to Gainesville, Florida, by express mail. Upon arrival in Gainesville, the sample was filtered through a sterile 0·2 µm filter 25 mm in diameter to concentrate bacterial cells. One-quarter of this filter was placed in 1 ml R2A medium diluted 1 : 10 with sterile distilled water. Cells on the filter piece were suspended in the test tube by vortexing. The resulting suspension of cells was serially diluted, with 100 µl each dilution spread on plates containing dilute (1 : 10) R2A medium solidified with 1·5 % agar.

Phylogenetic assignment of the 16S rRNA gene of strain TRO-001DR8T placed this organism among the Neisseriaceae. DNA isolation prior to 16S rRNA gene amplification was done as described previously (Borneman et al., 1996Go). Sequencing of the 16S rRNA gene was performed as described previously (Chelius & Triplett, 2000Go), except that the 8f primer (Escherichia coli numbering) was used for the amplification of the gene from strain TRO-001DR8T DNA. DNA sequencing was performed at the Interdisciplinary Center for Biotechnology Research at the University of Florida. Using BLASTN from NCBI, the closest cultured relative of strain TRO-001DR8T is Chromobacterium violaceum, with 95 % similarity over 1500 bases between the 16S rRNA gene sequences of these two organisms. C. violaceum inhabits soil and water and produces a characteristic violet pigment on agar media (Dessaux et al., 2004Go). Strain TRO-001DR8T does not utilize sucrose but will use glucose, some organic acids and most protein amino acids. It is not pigmented and differs metabolically from Chromobacterium.

The 16S rRNA gene sequences of two uncultured relatives present in the databases showed 95–98 % similarity with the 16S rRNA gene from strain TRO-001DR8T. One of the uncultured relatives (AB089102) was discovered in DNA isolated from the gut of the termite Reticulitremes speratus (Hongoh et al., 2003Go). The other clone (AB076875) was discovered following PCR amplification of DNA from an activated sludge (Khan et al., 2002Go).

The 16S rRNA gene sequences from 11 genera within the Neisseriaceae were compared to determine the mean distance between the most closely related pairs of genera: this was found to be 94 %, with a range of 90–98 %. The distance between Chromobacterium and the proposed Aquitalea genus is similar to the mean distance between any two genera in this family.

The 16S rRNA gene sequences were aligned using the web-based CLUSTAL W program at the Biology Work Bench (http://workbench.sdsc.edu/). The 16S rRNA gene of strain TRO-001DR8T (GenBank accession no. DQ018117) was aligned against 19 reference strains (Fig. 1Go). The 16S rRNA genes of the two most closely related uncultured organisms were also included in this analysis (Fig. 1Go). A Bayesian estimate of phylogeny was determined using MrBayes 3, which infers a posterior probability distribution of trees using Markov chain Monte Carlo searches (Ronquist & Huelsenbeck, 2003Go). These searches were run with four chains for 1 000 000 generations with trees sampled every 100 generations. A consensus tree was developed on the basis of the 10 000 trees developed using the Markov chain Monte Carlo method. The consensus tree was generated using TREEVIEW (Page, 1996Go).


Figure 1
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  		Fig. 1. Phylogenetic tree, based on the alignment of 16S rRNA genes, comparing strain TRO-001DR8T (Aquitalea magnusonii) with other selected betaproteobacteria within the Neisseriaceae. A Bayesian estimate of phylogeny was used to infer a posterior probability distribution of trees using Markov chain Monte Carlo searches (Ronquist & Huelsenbeck, 2003Go). A consensus tree was developed on the basis of the 10 000 trees developed by using the Markov chain Monte Carlo method. The consensus tree was generated using TREEVIEW (Page, 1996Go).

 
Strain TRO-001DR8T could not be assigned to any known genus on the basis of the fatty acid databases in the MIDI Sherlock Microbial Identification System. Two of the fatty acids present in strain TRO-001DR8T are absent in its closest relative, and two other fatty acids are present in C. violaceum ATCC 12472T but absent in strain TRO-001DR8T (Table 1Go). Four other fatty acids were found in both strains. However, their concentrations differed significantly between the two strains (Table 1Go). Fatty acid content was determined by GC and compared to the fatty acid database in the Microbial Identification System, Sherlock version 4.5 (MIDI).


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  		Table 1. Fatty acid content (%) of strain TRO-001DR8T and C. violaceum ATCC 12472T

All of the major unsaturated fatty acids found in this analysis were cis isomers (indicated by the suffix ‘c’). The summed fatty acids below cannot be separated by the GLC of the MIDI system. The position of the double bond in the unsaturated fatty acids is obtained by counting from the methyl ({omega}) end of the molecule.

 
Cells of strain TRO-001DR8T are rod-shaped with one polar flagellum and are 1–7 µm in length (mean length ~4 µm). The larger cells are often slightly curved. In stationary phase, cells can form long filaments. Colonies are a tan colour and produce a moderate amount of slime on R2A agar. Unlike C. violaceum, strain TRO-001DR8T does not produce a pigment on peptone agar. No resting stages were observed.

For light microscopy, strain TRO-001DR8T was visualized under phase-contrast microscopy and differential interference contrast optics on a Zeiss LSM-5 Pascal laser scanning microscope after 24 and 48 h growth (see Fig. 2aGo). For electron microscopy, exponential-phase Luria broth-cultured cells were gently deposited on a 300-mesh Formvar-coated grid, washed once with deionized water, briefly stained with 1 % aqueous uranyl acetate and then viewed at 100 kV on a Zeiss Em-10CA transmission electron microscope. The remainder of the culture was pelleted, resuspended in 1 % glutaraldehyde/0·1 M cacodylate (pH 7·2) and then fixed overnight at 4 °C. Cells were secondarily fixed in 1 % osmium tetroxide/0·1 M cacodylate buffer for 1 h and then subjected to 1 % aqueous uranyl acetate treatment for 1 h. After dehydration through an ethanol series and acetone, cells were embedded, thin-sectioned, post-stained with 5 % uranyl acetate and lead citrate and then viewed by transmission electron microscopy as above (Fig. 2b–dGo).


Figure 2
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  		Fig. 2. (a) Differential interference contrast image of strain TRO-001DR8T (note the variability in length from approximately 3 to 9 µm). Bar, 5 µm. (b) Electron micrograph of a cell negatively stained with 1 % aqueous uranyl acetate, showing the single polar flagellum. Bar, 1 µm. (c) Electron micrograph of thin-sectioned cells; most cells contain lipid-like inclusions. Bar, 1 µm. (d) Higher-magnification electron micrograph of cell cross-section, showing typical Gram-negative cell-wall structure. Bar, 0·1 µm.

 
The DNA–DNA relatedness between strain TRO-001DR8T and C. violaceum ATCC 12472T was 26 %. The DNA G+C content of strain TRO-001DR8T is 59·2 mol%. Genome sequencing of C. violaceum ATCC 12472T has revealed that it has a DNA G+C content of 64·83 mol% (Brazilian National Genome Project Consortium, 2003Go). For DNA–DNA hybridization, cells were disrupted using a French pressure cell and the DNA was purified by hydroxyapatite chromatography (Cashion et al., 1977Go). DNA–DNA hybridization was done as described by De Ley et al. (1970)Go, with the modifications of Huß et al. (1983)Go. The G+C content of strain TRO-001DR8T was determined by using HPLC (Mesbah et al., 1989Go) after isolation and purification of the DNA (Cashion et al., 1977Go).

As C. violaceum was the closest cultured relative of strain TRO-001DR8T, C. violaceum ATCC 12472T was used as the reference strain (Table 2Go). Selected strains from closely related genera in the Neisseriaceace are also included in Supplementary Table S1 in IJSEM Online. Strain TRO-001DR8T cannot utilize the following substrates utilized by C. violaceum: D-mannose, D-trehalose, L-alaninamide, L-phenylalanine, D-serine, L-threonine, inosine, uridine, thymidine, 2-aminoethanol, 2,3-butanediol, DL-{alpha}-glycerol phosphate, {alpha}-D-glucose 1-phosphate and D-glucose 6-phosphate. Strain TRO-001DR8T does utilize the following substrates not utilized by C. violaceum: cis-aconitic acid, citric acid, p-hydroxyphenylacetic acid, {alpha}-ketoglutaric acid, L-leucine and {gamma}-aminobutyric acid. Unlike Chromobacterium, strain TRO-001DR8T ferments (but does not oxidize) glucose and does not hydrolyse gelatin. Strain TRO-001DR8T is also more sensitive to salt as it cannot grow on 1·5 % NaCl whereas C. violaceum can tolerate concentrations up to 6 % NaCl. The carbon-assimilation tests were done using API 20NE (bioMérieux) according to the manufacturer's instructions. Additional carbon-assimilation tests were done using the Biolog GN2 MicroPlate according to the manufacturer's instructions. Cultures were inoculated on Biolog Universal Growth agar with 5 % sheep blood or chocolate agar and then incubated at 30 °C for 4–6 and 16–24 h prior to testing with the Biolog system. On the basis of the results of the Biolog GN carbon-utilization tests and other API 20NE metabolic tests, strain TRO-001DR8T could not be assigned to any known genus.


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  		Table 2. Some genotypic, phenotypic and nutritional characteristics that distinguish strain TRO-001DR8T from the closest genus type strain C. violaceum ATCC 12472T

 
OF medium (Hugh & Leifson, 1953Go) was used for the oxidation/fermentation test. Phenol red broth with a Durham tube inserted was used to identify acid/gas production. Tests for catalase and cytochrome c oxidase activity were completed using cells scraped from Luria agar and subsequently treated with 3 % (w/v) hydrogen peroxide or tetramethyl-p-phenylenediamine (Difco), respectively. Tests for nitrate reduction, indole production, arginine dihydolase, urease, aesculin ferric citrate and protease activity were done with an API 20NE kit. Cells grown in Luria broth (for 24 h at 28 °C) were wet-mounted and viewed under a light microscope to test for motility. To test for amylase activity, colonies were grown on starch agar for 14 days at 37 °C (Difco) and then flooded with iodine. Growth over a range of temperatures (4–45 °C) was tested with strains inoculated on Luria agar. Optimal growth was observed at 35 °C and pH 6·0.

Strain TRO-001DR8T will grow on Luria agar supplemented with ampicillin, rifampicin and streptomycin but not with chloramphenicol, kanamycin, spectinomycin, tetracycline and trimethoprim. In contrast, C. violaceum ATCC 12472T expresses resistance to a wider array of antibiotics, being insensitive to kanamycin, tetracycline and trimethoprim. Antibiotic sensitivity was tested using Luria agar supplemented with the following: spectinomycin, streptomycin or tetracycline, each at 10 µg ml–1; ampicillin, chloramphenicol or trimethoprim, each at 25 µg ml–1; kanamycin at 50 µg ml–1.

Description of Aquitalea gen. nov.
Aquitalea (A.qui.ta'le.a. L. fem. n. aqua -ae, water; L. fem. n. talea -ae a slender staff, rod, stick; N.L. fem. n. Aquitalea a rod of water).

Cells are Gram-negative, non-spore-forming, short rods. Rods are straight or slightly curved and 1–7 µm in length. Strain is aerobic, facultatively anaerobic, chemoheterotrophic and sensitive to NaCl. Cells are motile with one polar flagellum and are catalase- and oxidase-positive. DNA G+C content is 59·2 mol% (HPLC). Predominant fatty acids are C16 : 1{omega}7c (53 %) and C16 : 0 (22 %), C18 : 1{omega}7c (8 %) and C12 : 0 (5 %). Phylogenetically belongs to the family Neisseriaceae.

The type species is Aquitalea magnusonii.

Description of Aquitalea magnusonii gen. nov., sp. nov.
Aquitalea magnusonii (mag'nu.son'i.i. N.L. gen. n. magnusonii of Magnuson, in honour of Professor Emeritus John J. Magnuson, an ecologist at the University of Wisconsin-Madison who has contributed greatly to the study of the biodiversity, biogeography and climate-change analysis of lake ecosystems.

In addition to possessing the characteristics of the genus, described above, this species can grow on glycogen, pyruvic acid methyl ester, succinic acid monomethyl ester, acetic acid, cis-aconitic acid, citric acid, beta-hydroxybutyric acid, p-hydroxyphenylacetic acid, {alpha}-ketoglutaric acid, DL-lactic acid, propionic acid, succinic acid, bromosuccinic acid, L-asparagine, L-aspartic acid, L-glutamic acid, L-histidine, L-proline, L-serine and {gamma}-aminobutyric acid. Reduces nitrate and produces indole from L-tryptophan. Produces catalase, arginine dihydrolase and cytochrome oxidase. Resistant to ampicillin (25 µg ml–1), rifampicin (25 µg ml–1) and streptomycin (10 µg ml–1), but sensitive to chloramphenicol (25 µg ml–1), kanamycin (50 µg ml–1), spectinomycin (10 µg ml–1), tetracycline (10 µg ml–1) and trimethoprim (25 µg ml–1). Growth occurs between pH 5 and 8. Growth occurs between 28 and 40 °C but not at 4 or 45 °C. Strain TRO-001DR8T ferments, but does not oxidize, glucose.

The type strain, TRO-001DR8T (=ATCC BAA-1216T=BCCM/LMG 23054T), was isolated from a humic lake in northern Wisconsin, USA.


   ACKNOWLEDGEMENTS
 
This work was supported by funds from the National Science Foundation (MCB 9977903, MCB 0401987 and DEB 0217533) and the Florida Agricultural Experiment Station. We thank Donna Williams of the Microbiology and Cell Science Department at the University of Florida for the microscopy done in this study. We thank Stuart Jones of the University of Wisconsin-Madison for collecting lake samples for us.


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