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1 Department of Biological Sciences, University of Missouri-Rolla, Rolla, MO 65401, USA
2 Marshfield Clinic Research Foundation, 1000 N. Oak Avenue, Marshfield, WI 54449, USA
3 Department of Microbiology and Parasitology, University of Sevilla, 41012 Sevilla, Spain
4 Department of Chemical Engineering, Washington State University, Pullman, WA 99164, USA
5 Department of Biological Sciences, Central Washington University, Ellensburg, WA 98926, USA
Correspondence
Melanie R. Mormile
mmormile{at}umr.edu
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in the presence of acetate. Strain 4CAT was oxidase- and catalase-positive; it degraded Tween 60, but not DNA, urea, gelatin or starch. It grew at pH values from 7·5 to 11·0, with optimum growth occurring at pH 9·0, and growth was observed in NaCl concentrations of 0·2–1·3 M, with optimum growth at 0·8 M NaCl. The optimum temperature for growth was 37 °C. Strain 4CAT was resistant to erythromycin, bacitracin, novobiocin, polymyxin B, neomycin, gentamicin, streptomycin, carbenicillin, rifampicin and tetracycline, and was susceptible to nalidixic acid, chloramphenicol, ampicillin and penicillin. The isolate's 16S rRNA gene sequence indicated that it belonged to the 
-Proteobacteria, showing 90–94 % similarity to its closest relatives. Maximum-likelihood phylogenetic inferences placed strain 4CAT within a novel lineage related to the marine bacterial genera Neptunomonas and Marinobacterium. The DNA G+C content of the isolate was 47·4 mol%. On the basis of genotypic and phenotypic characterization, it was concluded that strain 4CAT should be placed in a separate taxon as a novel genus and species, with the proposed name Nitrincola lacisaponensis gen. nov., sp. nov. The type strain is 4CAT (=ATCC BAA-920T=DSM 16316T).
Published online ahead of print on 3 June 2005 as DOI 10.1099/ijs.0.63647-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Nitrincola lacisaponensis 4CAT is AY567473.
Present address: Department of Forest Sciences, University of British Columbia, Vancouver, BC, Canada V6T 1Z4. 
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). In particular, the majority of Gram-negative isolates and culture-independent bacterial clones retrieved from soda lakes belong to the -Proteobacteria (Jones et al., 1994, 1998; Ma et al., 2004), including strains related closely to typical aquatic bacteria such as Aeromonas and Pseudomonas (Duckworth et al., 1996), moderate halophiles from the Halomonas/Deleya group, and marine bacteria, e.g. Marinobacter (Rees et al., 2004).
Of the phylogenetically diverse Gram-negative, marine and/or halophilic aerobes and facultative anaerobes, the genus Oceanospirillum is the most widely studied and has traditionally consisted of various types of bacteria that occur in marine ecosystems (Hylemon et al., 1973). DNA–rRNA hybridization experiments (Pot et al., 1989, 1992) and fatty acid analysis (Sakane & Yokota, 1994) have revealed much intrageneric diversity within this group. Recently, analyses based on 16S rRNA and gyrB genes helped to clarify the taxonomic affiliation of the oceanospirilla and related bacteria (Satomi et al., 2002), leading to the redefinition of this genus to include four species. Other, less-studied genera affiliated with Oceanospirillum include Marinobacterium and Neptunomonas. These marine bacteria display the capability to grow on a wide range of substrates, including some polycyclic aromatic hydrocarbons in the case of Neptunomonas, and are frequently isolated from creosote-contaminated marine environments (González et al., 1997; Hedlund et al., 1999; González & Whitman, 2002).
In this study, we report the isolation and characterization of a new bacterium, designated strain 4CAT, obtained from Soap Lake, a meromictic lake with high alkalinity. Through the analysis of molecular and physiological properties, isolate 4CAT was found to bear resemblance to the Marinobacterium–Neptunomonas–Oceanospirillum cluster, although it was distinct enough to be separated into a novel genus.
Isolate 4CAT was obtained from decayed, red-coloured wood collected on the shore of Soap Lake, a meromictic, alkaline, saline lake located in Grant County, WA, USA. Soap Lake is a closed, evaporative system with neither a significant surface inlet nor outlet. This results in the concentration of salts, mainly sodium carbonate and sodium sulfate (Anderson, 1958). The current pH of the lake is about 9·8 and its NaCl concentration can exceed 10 % (w/v) (Walker, 1974). Two sections of wood (approx. 1 cm2) were removed aseptically from the sample and added to Soap Lake basal medium (SLBM), an enrichment medium for putative moderately halophilic, alkaliphilic bacteria. SLBM contained the following (l–1): CaSO4, 4·0 mg; FeSO4, 1·0 mg; NaCl, 17·5 g; SiO2, 5·0 mg; MgCl2, 4·0 mg; MnSO4, 4·0 mg; NH4NO3, 50·0 mg; Na2SO4, 13·5 g; KH2PO4, 3·0 g; K2HPO4, 3·0 g; Na2CO3, 1·0 g; and 1 ml trace element stock solution [g l–1: sodium nitriloacetate, 1·5; MgSO4.7H2O, 3·0; MnSO4.H2O, 0·5; NaCl, 1·0; FeSO4.7H2O, 0·1; CaCl2.2H2O, 0·1; CoCl2.6H2O, 0·1; ZnCl2, 0·13; CuSO4.5H2O, 0·01; AlK(SO4)2.12H2O, 0·01; H3BO3, 0·01; Na2MoO4.2H2O, 0·025; NiCl2.6H2O, 0·024; Na2WO4.2H2O, 0·025]. To enrich for bacteria capable of utilizing lignin-hydrolysis compounds, coumaric acid (CA) was added to a final concentration of 0·05 % (w/v). The final pH of the medium was adjusted to 9·8 with 1 M NaOH. Cultures were placed in a shaking incubator (200 r.p.m.) at 37 °C. To obtain pure cultures, the enriched cells were streaked onto solid SLBM containing 0·05 % (w/v) CA (pH 9·8). The strain selected for further study was maintained on solid SLBM or nutrient agar (Difco) slants.
The carbon-source utilization pattern was ascertained with a salt basal medium (SBM) described previously (Mormile et al., 1999), except that the NaCl, yeast extract and NaNO3 concentrations were lowered to 17·5, 0·1 and 0 g l–1, respectively, and the pH was adjusted to 9·0. Each carbon source tested was added separately from sterile stocks to give a 1 % final concentration, except for vanillic acid and CA, which were added at a concentration of 0·05 %. A growth test was considered positive when the OD600 reached or exceeded a value of 0·3 after 72 h at 37 °C. SBM containing acetate was used to determine growth responses to pH by adjusting, for each test, the pH at values ranging from 6·0 to 13·0 by using a finely adjusted KH2PO4/K2HPO4 or Na2CO3/NaHCO3 buffer system. The growth response to NaCl was measured by varying the NaCl concentration from 0 to 3·5 M. To determine whether the isolate required Na+ or Cl–, medium was prepared separately with KCl, Na2SO4, NaNO3 or Na2CO3 to substitute for these ions. Tolerance to salt and pH values was determined by measuring OD600 after 48 h incubation at 37 °C. Tolerance to temperature was determined after growth in SBM with acetate for 48 h. Potential electron acceptors other than oxygen were tested on SBM/acetate containing 0·001 g resazurin l–1 and included NaNO3, NaNO2, Na2SO4, Na2SO3 and Na2SeO4, each supplied at a concentration of 10 mM. Anaerobic conditions were achieved as described by Cutter et al. (1998).
Gram reaction was determined with a Gram-stain kit (Difco). Catalase and oxidase activities, as well as endospore production, were determined as described by Smibert & Krieg (1994). Analyses for hydrolysis of starch and DNA were performed with starch agar (Difco) and DNase (Difco) media, respectively. The ability to reduce nitrate under aerobic conditions was assessed on nitrate broth (Difco) by following the manufacturer's recommendations. King's media A and B were used to determine the production of pigments (King et al., 1954). Additional enzymic activities were assayed by using API 20E strips (bioMérieux). Antibiotic susceptibilities were determined by using antibiotic discs (Becton Dickinson) on SBM at pH 9·0.
For transmission electron microscopy (TEM), a bacterial cell pellet obtained from an overnight culture was fixed with 2 % glutaraldehyde/2 % paraformaldehyde in 0·1 M cacodylate buffer. After the samples were washed several times, 2 % liquid agar was added and, upon solidification, 1 mm3 portions were post-fixed in 1 % OsO4. En bloc staining was done in 1 % aqueous uranyl acetate. Samples were dehydrated in an ethanol series and infiltrated with Epon-Araldite epoxy resin. The material was then placed into fresh resin in BEEM embedding capsules and polymerized at 60 °C. After polymerization, blocks were sectioned on a Leica UCT ultramicrotome and ultrathin sections (70 nm thick) were stained with 1 % uranyl acetate and lead citrate. Samples were viewed and photographed in a JEOL 1200EX transmission electron microscope and imaged on Kodak 4489 TEM film. To visualize flagella, a 5 µl aliquot of strain 4CAT culture was placed on a Ni sample disc and evaporated to dryness. The sample was placed in a 27 % solution of phosphotungstic acid for 30 s and rinsed with ultrapure water before TEM.
To determine the DNA base composition, DNA was extracted and purified by the method of Marmur (1961) and its G+C content was determined from the mid-point value (Tm) of the thermal-denaturation profile (Marmur & Doty, 1962) by using the equation of Owen & Hill (1979). The 16S rRNA gene of strain 4CAT was PCR-amplified with the broad-range bacterial primers 27F (5'-AGAGTTTGATCCTGGCTCAG-3'), 806R (5'-GGACTACCAGGGTATCTAAT-3'), 13B (5'-AGGCCCGGGAACGTATTCAC-3') and 1527R (5'-AAGGAGGTGATCCAGCC-3') (Relman et al., 1992; Weisburg et al., 1991). PCR and sequencing reactions were performed by following the protocol described by Shukla et al. (2001). The sequencing reactions were resolved in an ABI 3100 gene analyser (Applied Biosystems). The assembled and edited 16S rRNA gene sequence of strain 4CAT was aligned with 16S rDNA sequences of closely related strains by conducting BLAST searches of genbank and performing multiple alignments using CLUSTAL W (Thompson et al., 1994) with additional manual alignment. The phylogenetic relationships of each taxon were inferred by maximum-likelihood, parsimony and evolutionary-distance methods of phylogenetic reconstruction, using PAUP* 4.0 b10 (Swofford, 2003). Maximum-likelihood trees were inferred by using the default starting parameters (neighbour-joining using a Jukes–Cantor model of evolution). Statistical support of the branch points was tested by performing 1000 maximum-likelihood bootstrap replications. Parsimony trees were inferred by conducting heuristic searches with the tree–bisection–reconnection branch-swapping algorithm, all positions were weighted equally and gaps were treated as missing. Pairwise distances were used to generate neighbour-joining/UPGMA trees using Hasegawa, Kishino and Yano (HGK85) distance.
When grown for 2 days at 37 °C on solid SBM containing acetate, colonies of strain 4CAT were typically white, circular and convex, with entire margins and a diameter of 1–2 mm. Colonies of the culture grown on nutrient agar (pH 9·8 and 1·75 % NaCl) exhibited similar morphology, but diameters were 3–4 mm. Liquid nutrient broth also supported growth of strain 4CAT, although the bacteria had a slight tendency to clump as cultures aged. Cells were motile, short rods that possessed a single polar flagellum and stained Gram-negative; they were typically 1·3–1·6 µm long and 0·5 µm wide. Electron microscopy analyses confirmed the Gram-negative structure (Fig. 1) and position and number of the flagella (Fig. 2). In most cases, strain 4CAT appeared as single cells. No endospore production was observed.
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; Ivey et al., 1998).
The new strain was oxidase- and catalase-positive and did not exhibit lysine decarboxylase, ornithine decarboxylase or arginine dihydrolase activities. Strain 4CAT was negative for the production of H2S, Voges–Proskauer reaction and indole production; urea, gelatin, DNA and starch were not hydrolysed. Cells did not produce visible or fluorescent pigments when incubated on solid King's media B or A, respectively, two characteristics widely used for preliminary determination of pseudomonad species (Stanier et al., 1966; Palleroni, 1984). Strain 4CAT grew with O2 or 
as electron acceptors in the presence of acetate, but not with 
, 
, 
or 
. Under aerobic conditions, it utilized DL-lactate, acetate, pyruvate, malate, fumarate, succinate and Tween 60. Additional characteristics are provided in the species description.
The G+C content of the DNA of strain 4CAT was 47·4 mol%, as determined by the thermal-denaturation method. The sequence of an approximately 1400 bp portion of the 16S rRNA gene was obtained for isolate 4CAT. No sequences available in the public databases exhibited >94 % similarity to the sequence of strain 4CAT. Phylogenetic analysis revealed that isolate 4CAT clustered within the -subclass of the Proteobacteria, encompassing the genera Neptunomonas, Marinobacterium and Oceanospirillum (Fig. 3). Some pseudomonads belonging to the Pseudomonas fluorescens intrageneric cluster, one of the two major clusters that comprise the genus Pseudomonas sensu stricto (Moore et al., 1996), formed a distinct subclade detached from strain 4CAT. Maximum-likelihood, parsimony and distance methods resulted in highly similar tree topologies. Strain 4CAT had a mean of 90–91·8 % sequence similarity to all taxa that fell into this cluster, and displayed 94, 92·5 and 93 % similarity to the marine bacteria Marinobacterium sp. strain DMS-S1 (Fuse et al., 2000), Neptunomonas naphthovorans (Hedlund et al., 1999) and Oceanospirillum beijerinckii (Hylemon et al., 1973), respectively.
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. The strain could be distinguished from members of the genus Oceanospirillum by its shape and its ability to grow in the absence of NaCl. Some phenotypic properties delineating strain 4CAT were also in marked disagreement with those that characterize members of the genus Marinobacterium: the type species, Marinobacterium georgiense, can utilize sugars and amino acids, requires a salt-based medium for growth and grows best at pH 7·0 (González et al., 1997; González & Whitman, 2002). A similar physiological profile is observed for members of the genus Neptunomonas (Hedlund et al., 1999). None of the related genera can use 
as an electron acceptor, nor do they exhibit an alkaliphilic phenotype.
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) evidence that warrants the affiliation of strain 4CAT to a separate, novel lineage, excluding it from any of the previously described genera of the -Proteobacteria to which it is phylogenetically related. Thus, we conclude that isolate 4CAT represents a novel genus and species, for which the name Nitrincola lacisaponensis gen. nov., sp. nov. is proposed.
Description of Nitrincola gen. nov.
Nitrincola (Nit.rin'co.la. L. neut. n. nitrum soda; L. masc. n. incola inhabitant, dweller; N.L. masc. n. Nitrincola an inhabitant of a soda environment).
Alkaliphilic, halotolerant and heterotrophic. Cells are non-pigmented, asporogenous, motile, Gram-negative rods. 
and O2 can be used as electron acceptors. Fermentable carbon sources do not support growth. Chemo-organotrophic. Requires sodium for growth. Oxidase- and catalase-positive. Optimal pH for growth is 9·0. The genus is a member of the -subclass of the Proteobacteria. Isolated from a saline, alkaline lake. The DNA G+C content is 47·4 mol% (Tm). The type species is Nitrincola lacisaponensis.
Description of Nitrincola lacisaponensis sp. nov.
Nitrincola lacisaponensis (la.ci.sa.po.nen'sis. L. n. lacus lake; L. n. sapo -onis soap; N.L. masc. adj. lacisaponensis pertaining to Soap Lake).
Cells are short, motile rods, occurring singly or in pairs (1·3–1·5 µm in length and 0·5 µm in width). When grown on alkaline nutrient agar, colonies are 3–4 mm in diameter, whitish-beige-coloured, entire, smooth and convex. Obligate alkaliphile. Oxidase and catalase are produced. Lysine decarboxylase, ornithine decarboxylase and arginine dihydrolase are not produced; nor are H2S, acetoin or indole. Urea, gelatin, DNA and starch are not hydrolysed. No visible or fluorescent pigments are formed during incubation on solid King's media B or A, respectively. Strain 4CAT can grow with O2 or 
as electron acceptors in the presence of acetate, but not with 
, 
, 
or 
. Carbon-source utilization is restricted to a limited range of organic acids, including DL-lactate, acetate, pyruvate, malate, fumarate and succinate. Glycine, L-alanine, L-arginine, L-asparagine, L-aspartic acid, L-glutamic acid, L-glutamine, L-isoleucine, L-leucine, L-ornithine, L-phenylalanine, sarcosine, L-threonine, L-serine, L-tryptophan, L-methionine, mannitol, D-mannose, D-arabinose, sucrose, D-xylose, glucose, D-galactose, cellobiose, D-fructose, D-ribose, ethanol, adonitol, glycerol, dulcitol, sorbitol, propanol, lactose, glucuronate, saccharate, hippurate, vanillate, coumarate and benzoate are not utilized. Cells are resistant to erythromycin, bacitracin, novobiocin, polymyxin B, neomycin, gentamicin, streptomycin, carbenicillin, rifampicin and tetracycline, and are susceptible to nalidixic acid, chloramphenicol, ampicillin and penicillin. In minimal medium (SBM) containing acetate, the conditions for growth are pH 7·5–11·0 and up to 1·3 M NaCl. Optimum growth occurs at pH 9·0 and at 0·8 M NaCl. The DNA G+C content is 47·4 mol% (Tm).
Isolated from decayed wood collected at Soap Lake, a saline, alkaline environment. The type strain is 4CAT (=ATCC BAA-920T=DSM 16316T).
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ACKNOWLEDGEMENTS |
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