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Int J Syst Evol Microbiol 58 (2008), 97-102; DOI  10.1099/ijs.0.65039-0
© 2008 International Union of Microbiological Societies

Perlucidibaca piscinae gen. nov., sp. nov., a freshwater bacterium belonging to the family Moraxellaceae

Jaeho Song, Yoe-Jin Choo and Jang-Cheon Cho

Division of Biology and Ocean Sciences, Inha University, Incheon 402-751, Republic of Korea

Correspondence
Jang-Cheon Cho
chojc{at}inha.ac.kr


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A freshwater bacterium, designated IMCC1704T, was isolated from a eutrophic pond. The strain was Gram-negative, oxidase-positive, catalase-negative, chemoheterotrophic and facultatively aerobic with cells that were motile rods with a single polar flagellum. Based on 16S rRNA gene sequence similarity analyses, the novel strain was most closely related to the genera Alkanindiges (91.7 %), Acinetobacter (89.0–91.2 %), Moraxella (87.9–90.1 %), Psychrobacter (87.2–89.5 %) and Enhydrobacter (87.8 %). Phylogenetic trees generated using 16S rRNA gene sequences showed that the novel isolate belonged to the family Moraxellaceae of the class Gammaproteobacteria and formed a distinct phyletic lineage within the family. The DNA G+C content of the strain was 63.1 mol% and the predominant constituents of the cellular fatty acids were C16 : 1{omega}7c and/or iso-C15 : 0 2-OH (21.2 %), C18 : 1{omega}7c (12.8 %) and C12 : 0 3-OH (12.3 %). These chemotaxonomic properties, together with several phenotypic characteristics, differentiated the novel strain from other members of the family Moraxellaceae. From the taxonomic data, which revealed the distant relationship of the new strain to the related genera, the strain should be classified as a novel genus and species in the family Moraxellaceae, for which the name Perlucidibaca piscinae gen. nov., sp. nov. is proposed. The type strain of Perlucidibaca piscinae sp. nov. is IMCC1704T (=KCCM 42363T=NBRC 102354T).

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain IMCC1704T is DQ664237.

An electron micrograph of a cell of strain IMCC1704T is available with the online version of this paper.


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The family Moraxellaceae of the order Pseudomonadales in the class Gammaproteobacteria was proposed by Rossau et al. (1991)Go based on comprehensive DNA–rRNA hybridization results. The family currently comprises five recognized genera: Moraxella (Lwoff, 1939Go), Acinetobacter (Brisou & Prévot, 1954Go), Psychrobacter (Juni & Heym, 1986Go), Enhydrobacter (Staley et al., 1987Go) and Alkanindiges (Bogan et al., 2003Go). Because the members of the family Moraxellaceae are widely distributed in diverse environments and are of clinical importance, many novel species, especially within the genera Acinetobacter and Psychrobacter, have been isolated and classified recently (Bakermans et al., 2006Go; Bozal et al., 2003Go; Carr et al., 2003Go; Jung et al., 2005Go; Nemec et al., 2001Go, 2003Go; Yoon et al., 2005bGo). The present study focuses on the description of strain IMCC1704T that was isolated from a freshwater pond (Song et al., 2007Go). Based on the taxonomic data collected in this study, we propose the inclusion of the strain in a new genus and novel species within the family Moraxellaceae.

Strain IMCC1704T was isolated from an artificial freshwater pond located inside Inha University, Korea, by a standard dilution plating method on R2A agar (Reasoner & Geldreich, 1985Go; Difco) plates. After incubating the agar plates aerobically at 20 °C for 5 days, strain IMCC1704T was purified as single colonies and subsequently stored at –80 °C as 10 % (v/v) glycerol suspensions. After the optimum growth temperature of the strain was determined, cultures were routinely maintained on R2A agar at 30 °C.

DNA extraction, PCR and sequencing of the 16S rRNA gene were performed as described previously (Cho & Giovannoni, 2003Go) and almost complete 16S rRNA gene sequences (1467 bp) of strain IMCC1704T were obtained. Preliminary sequence comparisons with 16S rRNA gene sequences held in the GenBank database showed that the novel strain belonged to the family Moraxellaceae in the class Gammaproteobacteria. The 16S rRNA gene sequences of the novel strain were aligned using the ARB software package (Ludwig et al., 2004Go) and 1269 unambiguously aligned nucleotide positions were used for phylogenetic analyses in PAUP 4.0 beta 10 (Swofford, 2002Go). Phylogenetic trees were generated by the neighbour-joining (Saitou & Nei, 1987Go) method with Jukes–Cantor distance (Jukes & Cantor, 1969Go), maximum-parsimony (Fitch, 1971Go) and maximum-likelihood (Felsenstein, 1981Go) algorithms. The resultant neighbour-joining and maximum-parsimony trees were evaluated by bootstrap analysis based on 1000 resamplings.

Sequence comparisons based on the multiple alignment in the ARB database, Ribosomal Database Project (RDP-II) and BLASTN search results showed that the most closely related cultured species with respect to strain IMCC1704T was ‘Alkanindiges hongkongensis’ HKU9 (92.5 % gene sequence similarity), which was described by Woo et al. (2005)Go but the name has not yet been validly published. Strain IMCC1704T showed the highest 16S rRNA gene sequence similarity with the recognized species Alkanindiges illinoisensis DSM 15370T (91.7 %), followed by Acinetobacter calcoaceticus ATCC 23055T (91.2 %) and Acinetobacter parvus LMG 21765T (91.0 %). Strain IMCC1704T was moderately related to the genera of the family Moraxellaceae with relatively low 16S rRNA gene sequence similarities: Alkanindiges, 91.7 %; Acinetobacter, 89.0–91.2 %; Moraxella, 87.9–90.1 %; Psychrobacter, 87.2–89.5 % and Enhydrobacter, 87.8 %. No other recognized species exceeded 92.0 % 16S rRNA gene sequence similarity to strain IMCC1704T. In all of the phylogenetic trees generated in this study, strain IMCC1704T, the uncultured freshwater bacteria 156ds20 (GenBank accession no. AY212607; Simpson et al., 2004Go) and 216ds20 (AY212663; Simpson et al., 2004Go) formed an independent monophyletic lineage with 96–100 % bootstrap support for a position within the family Moraxellaceae (Fig. 1Go). This lineage formed a larger clade with the genera Acinetobacter and Alkanindiges in all of the phylogenetic trees; however, the phylogenetic relationship between strain IMCC1704T and the genera Acinetobacter and Alkanindiges was distinct. The results of phylogenetic analyses revealed that strain IMCC1704T could not be associated with any of the known genera in the family. Therefore, strain IMCC1704T was considered to represent a new genus in the family Moraxellaceae.


Figure 1
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  		Fig. 1. Neighbour-joining phylogenetic tree, based on 16S rRNA gene sequences, showing relationships between strain IMCC1704T and representatives of the family Moraxellaceae. Bootstrap percentages (above 50 %) from both neighbour-joining (above nodes) and maximum-parsimony (below nodes) are shown. The closed and open circles at each node indicate nodes recovered reproducibly by all treeing methods or by two treeing methods, respectively. Bar, 0.01 substitutions per nucleotide position.

 
For phenotypic characterizations, strain IMCC1704T was routinely grown on R2A agar at 30 °C, unless otherwise specified. The type species of the most closely related genera Acinetobacter and Alkanindiges were also phenotypically characterized. Alkanindiges illinoisensis DSM 15370T and Acinetobacter calcoaceticus ATCC 23055T were purchased from the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ) collection and the Korean Culture and Type Collection (KCTC), respectively. Both type strains obtained from the culture collections were grown on R2A agar at 25 °C, unless otherwise indicated. Cell morphology and size were examined by transmission electron microscopy (CM200; Philips) and phase-contrast microscopy (80i; Nikon) using a 3 day culture. For electron microscopy, cells were washed twice with sodium cacodylate buffer and negatively stained with 2 % phosphotungstic acid (pH 7.0–7.2) on Formvar-coated copper grids. Colony morphology, size and colour were examined from cultures grown aerobically for 5 days. Motility based on flagella was tested from wet mounts using a 3 day culture. The growth temperature range and optimum were tested on R2A agar at 4, 10, 15, 20, 25, 30, 37 and 42 °C. The pH range and optimum were examined on R2A at pH values from pH 4.0 to 12.0 (at intervals of 1.0 pH units), adjusted with 0.1 M HCl and 0.1 M NaOH. The optimum NaCl concentration for growth was determined on R2A agar supplemented with 0–15 % NaCl (at intervals of 0.5 % from 0–5.0 %, 7.5 %, 10.0 %, 12.5 % and 15.0 %, w/v). The ranges and optima of temperature, pH and NaCl concentration for growth were monitored for 2 weeks. Anaerobic growth was tested using both the MGC anaerobic system (Mitsubishi Gas Chemical company, Inc.) and the Anaerocult C mini (EM Science). The catalase test was performed by the addition of 3.0 % hydrogen peroxide to fresh colonies and oxidase activity was determined using Kovacs' solution (Kovacs, 1956Go). Other biochemical tests were carried out with API 20NE and API ZYM (bioMérieux) kits following the manufacturer's instructions. Sole carbon source utilization tests were performed using custom-made 48-well microplates containing 47 different carbon compounds at a final concentration of 0.2 % (w/v or v/v), according to Choo et al. (2007)Go except that microplates were inoculated with bacterial suspensions in phosphate-buffered saline (pH 7.4). Cells at the exponential growth phase were harvested and cell densities were adjusted to approximately 2x103 cells ml–1 in phosphate-buffered saline (pH 7.4). A 1 ml sample of cell suspension was inoculated per well and the microplates were incubated at 30 °C for strain IMCC1704T and 25 °C for strains DSM 15370T and ATCC 23055T. After incubation of the microplates for 1 week, cellular growth and purity were checked by DAPI-stained epifluorescence microscopy. The DNA G+C content (Mesbah et al., 1989Go) was analysed by using HPLC with a Discovery C18 column (5 µm, 15 cmx4.6 mm; Supelco). Cellular fatty acid methyl esters of strains IMCC1704T, DSM 15370T and ATCC 23055T were prepared from the cultures grown on R2A agar at 30 °C for 3 days and were analysed according to the instructions of the Microbial Identification System (MIDI) by the Korean Culture Center of Microorganisms (KCCM). Respiratory quinones were analysed using a reverse-phase HPLC (Komagata & Suzuki, 1987Go).

Strain IMCC1704T was Gram-negative, chemoheterotrophic, facultatively aerobic, catalase-negative and oxidase-positive. Cells were motile short-rods that had a single polar flagellum (see Supplementary Figure S1 in IJSEM online). Detailed results of the phenotypic and biochemical tests are given in the species description and in Tables 1Go, 2Go and 3Go. Strain IMCC1704T could be differentiated from the other genera of the family Moraxellaceae by several phenotypic characteristics and the DNA G+C content (Table 1Go). The DNA G+C content of strain IMCC1704T was 63.1 mol%, which was 13–23 mol% higher than that of other members of the family Moraxellaceae, except for Enhydrobacter aerosaccus. The biochemical characteristics and carbon source utilization patterns also clearly differentiated strain IMCC1704T from the type strains of the type species of the genera Alkanindiges and Acinetobacter (Table 2Go). The major fatty acid constituents of strain IMCC1704T were C16 : 1{omega}7c and/or iso-C15 : 0 2-OH (21.2 %), C18 : 1{omega}7c (12.8 %), C12 : 0 3-OH (12.3 %), C12 : 0 (10.1 %) and C18 : 1{omega}9c (9.2%), and they were different from those of Alkanindiges illinoisensis DSM 15370T and Acinetobacter calcoaceticus ATCC 23055T.


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  		Table 1. Characteristics that differentiate strain IMC1704T from the genera of the family Moraxellaceae

Taxa: 1, strain IMCC1704T; 2, Acinetobacter (n=17, data taken collectively from this study and Bouvet & Grimont, 1986Go; Carr et al., 2003Go; Juni & Bøvre, 2005Go; Nemec et al., 2001Go, 2003Go; Nishmura et al., 1988Go); 3, Alkanindiges (n=1, data from this study and Bogan et al., 2003Go); 4, Psychrobacter (n=27, data taken collectively from Bakermans et al., 2006Go; Heuchert et al., 2004Go; Jung et al., 2005Go; Juni & Bøvre, 2005Go; Romanenko et al., 2004Go; Yoon et al., 2005aGo, bGo); 5, Enhydrobacter (n=1, Staley et al., 1987Go); 6, Moraxella (n=17, data taken collectively from Angelos et al., 2007Go; Juni & Bøvre, 2005Go; Kodjo et al., 1995Go; Vandamme et al., 1993Go; Xie & Yokota, 2005Go). +, Present in 90 % or more of the species; –, absent in 90 % or more of the species; V, present in 11–89 % of the species, ND, no data available; W, weakly positive.

 

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  		Table 2. Biochemical characteristics and carbon source utilization patterns that differentiate strains IMCC1704T, Acinetobacter calcoaceticus ATCC 23055T and Alkanindiges illinoisensis DSM 15370T

Strains: 1, IMCC1704T; 2, Acinetobacter calcoaceticus ATCC 23055T; 3, Alkanindiges illinoisensis DSM 15370T. +, Positive; –, negative; W, weakly positive. All data were obtained in the present study. All the strains were negative for acid production from glucose, for activities of arginine dihydrolase, trypsin, {alpha}-chymotrypsin, acid phosphatase, {alpha}-galactosidase, β-galactosidase, β-glucuronidase, {alpha}-glucosidase, β-glucosidase, N-acetyl-β-glucosaminidase, {alpha}-mannosidase and {alpha}-fucosidase and for utilization of methanol, ethanol, DL-glyceraldehyde, D-cellobiose, D-lactose, melibiose, D-melezitose, adonitol, succinic acid, L-glutamic acid and L-leucine. All the strains were positive for esterase (C4) and esterase lipase (C8) activities and for utilization of L-proline and were weakly positive for aesculin hydrolysis.

 

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  		Table 3. Cellular fatty acid content (%) of strain IMCC1704T, Acinetobacter calcoaceticus ATCC 23055T and Alkanindiges illinoisensis DSM 15370T

Strains: 1, IMCC1704T; 2, Acinetobacter calcoaceticus ATCC 23055T; 3, Alkanindiges illinoisensis DSM 15370T. –, Not detected. All the strains were grown on R2A agar at 30 °C for 3 days. Only fatty acids representing at least 1 % of the total cellular fatty acids of at least one of the strains are shown.

 
It is evident from the low 16S rRNA gene sequence similarity (<92 %), the formation of an independent phyletic line in the phylogenetic analyses (Fig. 1Go) and the differential phenotypic characteristics (Tables 1Go, 2Go and 3Go) that strain IMCC1704T cannot be assigned to any of the known genera in the family Moraxellaceae. Conclusively, based on the taxonomic results in this study, strain IMCC1704T should be classified as a novel species within a new genus, for which the name Perlucidibaca piscinae gen. nov., sp. nov. is proposed.

Description of Perlucidibaca gen. nov.
Perlucidibaca (Per.lu.ci.di.ba'ca. L. adj. perlucidus transparent, pellucid; L. fem. n. baca a small round fruit, a berry; N.L. fem. n. Perlucidibaca a transparent berry).

Gram-negative. Oxidase-positive and catalase-negative. Chemoheterotrophic and facultatively aerobic. Anaerobic growth is similar to aerobic growth. Cells are short rods that are motile by a polar flagellum. Indole is produced. Nitrate reduction is weakly positive. Acid is not produced from glucose fermentation. Predominant cellular fatty acids are C16 : 1{omega}7c and/or iso-C15 : 0 2-OH, C18 : 1{omega}7c, C12 : 0 3-OH and C12 : 0. The DNA G+C content is 63.1 mol%. The major respiratory quinone is Q-8. Phylogenetically, the genus belongs to the family Moraxellaceae. The type species is Perlucidibaca piscinae.

Description of Perlucidibaca piscinae sp. nov.
Perlucidibaca piscinae (pis.ci'nae. L. gen. n. piscinae of a fish-pond).

The description is the same as that for the genus, with the following additional properties. Cells in the exponential phase are short rods, 0.7–1.2 µm long and 0.5–0.7 µm wide. Colonies on R2A agar are circular, convex, smooth, butyrous and transparent with an entire margin. Colony size is 0.5–1.0 mm after incubation on R2A at 30 °C for 5 days. Grows at 8–37 °C (optimally at 30 °C), but not at 4 and 42 °C. Growth occurs at pH 6–10 and with 0–1 % NaCl; optimum at pH 7.0 and without NaCl. Biochemical characteristics and carbon source utilization patterns are shown in Table 2Go. The cellular fatty acid content is listed in Table 3Go.

The type strain, IMCC1704T (=KCCM 42363T=NBRC 102354T), was isolated from an artificial freshwater pond located inside Inha University, Korea.


   ACKNOWLEDGEMENTS
 
We are grateful to Dr Jean Euzéby for his recommendations about etymology. This study was supported by Inha University Research Grant.


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