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Int J Syst Evol Microbiol 56 (2006), 1875-1881; DOI  10.1099/ijs.0.64224-0
© 2006 International Union of Microbiological Societies

Pseudomonas peli sp. nov. and Pseudomonas borbori sp. nov., isolated from a nitrifying inoculum

Bram Vanparys, Kim Heylen, Liesbeth Lebbe and Paul De Vos

Laboratory of Microbiology, Department of Biochemistry, Physiology and Microbiology, Ghent University, K. L. Ledeganckstraat 35, B-9000 Gent, Belgium

Correspondence
Bram Vanparys
bram.vanparys{at}ugent.be


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Sixteen Gram-negative, rod-shaped, non-spore-forming isolates were obtained from a nitrifying inoculum. Analysis of repetitive sequence-based PCR and SDS-PAGE banding patterns, 16S rRNA gene sequence analysis and DNA–DNA hybridizations showed that the isolates belonged to various groups within the genus Pseudomonas. One group of isolates could be assigned to Pseudomonas migulae and a second to Pseudomonas veronii. Two groups could be differentiated genotypically from each other and from all other currently known Pseudomonas species. Analysis of the fatty acid composition and physiological and biochemical tests allowed differentiation of these groups from their closest phylogenetic neighbours and they therefore represent two novel species within the genus Pseudomonas, for which the names Pseudomonas peli sp. nov. and Pseudomonas borbori sp. nov. are proposed, with strains LMG 23201T (=DSM 17833T=R-20805T) and LMG 23199T (=DSM 17834T=R-20821T), respectively, as the type strains.

The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of Pseudomonas peli LMG 23201T and Pseudomonas borbori LMG 23199T are AM114534 and AM114527.


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In aquaria and aquaculture ponds with high fish densities, ammonia excreted by fish can reach toxic levels. To accelerate the start-up of biofilters, inocula with highly active nitrifying communities are commercially available. An isolation campaign of one of these inocula, developed by enrichment of the autotrophic nitrifying community from activated sludge by adding a daily load of nitrogen (Grommen et al., 2002Go), revealed a large diversity of heterotrophic bacteria. Sixteen isolates (Table 1Go), identified as members of the genus Pseudomonas by the Microbial Identification software (MIDI) with the TSBA database version 5.0 (Microbial ID) after quantitative analysis of the cellular fatty acid composition, were analysed further in a polyphasic study.


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  		Table 1. Strains used in this study with their origin (reference strains) or isolation conditions (this study)

Abbreviations: NA, nutrient agar (Oxoid); TSA, tryptone soya agar (Oxoid); R2A, R2A agar (Difco); MMO, mineral salts medium (Stanier et al., 1966Go) with 1.69 mM succinate and 1.5 % agar. All new isolates were obtained after aerobic incubation for 3 weeks.

 
The nearly complete 16S rRNA gene sequences of the isolates were determined as described previously (Vanparys et al., 2005Go). FASTA analysis at the EMBL database (Pearson, 1990Go) confirmed that all isolates belonged to the genus Pseudomonas. The phylogenetic positions of the isolates were analysed by comparing their 16S rRNA gene sequences with all publicly available complete 16S rRNA gene sequences of the type strains of currently described Pseudomonas species. Similarity matrices were constructed after pairwise alignment. Phylogenetic trees constructed using the neighbour-joining algorithms without corrections for evolutionary distance (Fig. 1a, bGo) were in agreement with trees constructed using the maximum-parsimony, maximum-likelihood and neighbour-joining algorithms (data not shown) with corrections as described by Jukes & Cantor (1969)Go and Kimura (1980)Go. Phylogenetic trees were constructed after multiple alignment using BIONUMERICS version 3.5 software (Applied-Maths). The 16 isolates were scattered over five groups (A–E; Fig. 1a, bGo). Group A (three isolates with 100 % 16S rRNA gene sequence similarity) showed the highest sequence similarity (99.5 %) to Pseudomonas migulae CIP 105470T. Group B (LMG 23196) showed the highest sequence similarity (99.8 %) to Pseudomonas veronii CIP 104663T. Group C (two isolates with 100 % 16S rRNA gene sequence similarity) clustered most closely with Pseudomonas anguilliseptica NCIMB 1949T with a 16S rRNA gene sequence similarity of 98.2 %. Sequence similarities versus other type strains were below 97.0 %. The isolates of group D (six isolates) and E (four isolates) fell within one rather homogeneous 16S rRNA gene cluster, with Pseudomonas straminea IAM 1598T, Pseudomonas argentinensis CH01T, Pseudomonas flavescens ATCC 51555T and P. anguilliseptica NCIMB 1949T as closest phylogenetic neighbours.


Figure 1
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  		Fig. 1. Phylogenetic positions based on neighbour-joining clustering after multiple alignment (1450 bp) of the 16S rRNA gene sequences of the isolates of groups A and B among related members of the Pseudomonas fluorescens group (Anzai etal., 2000Go) (a) and multiple alignment (1370 bp) of the 16S rRNA gene sequences the isolates of groups C, D and E among related members of the Pseudomonas aeruginosa group (Anzai et al., 2000Go) (b). Bootstrap values higher than 70 % (expressed as percentages of 1000 replications) are shown at branch points.

 
For SDS-PAGE of whole-cell proteins, isolates were grown on phosphate-buffered nutrient agar (pH 6.8) and incubated aerobically at 28 °C for 48 h. An SDS-PAGE banding pattern for all isolates was generated using a previously described protocol (Pot et al., 1994Go). Visual comparison of the banding profiles and UPGMA clustering of Pearson's correlation similarity coefficients using BIONUMERICS version 3.5 (Fig. 2Go) revealed a similar grouping to that obtained by 16S rRNA gene sequence analysis, with the exception that groups D and E did not cluster together.


Figure 2
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  		Fig. 2. Grouping of normalized digitized SDS-PAGE patterns of the 16 Pseudomonas isolates in a dendrogram based on UPGMA clustering of Pearson's correlation similarity coefficients.

 
Repetitive sequence-based PCR profiles of the isolates were determined using a method described previously (Heyrman et al., 2005Go) with REP and (GTG)5 primers. UPGMA clustering of Pearson's correlation similarity coefficients of the combined normalized REP and (GTG)5 banding patterns is shown in Fig. 3Go. Delineation at 90 % again revealed the same groups as those shown by 16S rRNA gene sequence analysis and by analysis of the SDS-PAGE banding patterns. The high similarity of the PCR banding patterns within each group, combined with the 16S rRNA gene sequence and SDS-PAGE data, suggested that the isolates within each group are of clonal origin.


Figure 3
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  		Fig. 3. Grouping of combined normalized REP-PCR and (GTG)5 patterns of the 16 Pseudomonas isolates in a dendrogram based on UPGMA clustering of Pearson's correlation similarity coefficients.

 
To analyse whether the different groups represented novel genotypic species, DNA–DNA hybridization experiments were performed using a modification of the microplate method of Ezaki et al. (1989)Go, as described by Willems et al. (2001)Go. A hybridization temperature of 45 °C was used. For each group, a representative strain was hybridized with its closest phylogenetic neighbour(s). The representative of group A (LMG 23195) showed a DNA–DNA relatedness value of 83.2 % (±0.4 % spread on the reciprocal values) to P. migulae LMG 21608T and the isolates of group A were hence allocated to this species. LMG 23196 (group B) showed a DNA–DNA relatedness value of 89.5 % (±7.2 %) to P. veronii LMG 17761T and was hence allocated to this species. As it was shown by 16S rRNA gene sequence analysis that groups C, D and E are highly related, representatives of each group were first hybridized internally. LMG 23198 (group D) showed a DNA–DNA relatedness value of 80.9 % (±5.4 %) to LMG 23199T (group E), whilst LMG 23201T (group C) showed DNA–DNA relatedness values of 35.3 % (±0.5 %) and 40.4 % (±7.0 %) to LMG 23198 and LMG 23199T, respectively. It could thus be concluded that the strains of groups D and E belonged to a single species, which was different from group C. A representative of group D/E (LMG 23199T) showed DNA–DNA relatedness values of 27.0 % (±10.0 %) to P. straminea LMG 21615T, 27.4 % (±2.3 %) to P. flavescens LMG 18387T, 33.6 % (±11.5 %) to P. anguilliseptica LMG 21629T and 29.5 % (±1.2 %) to P. argentinensis LMG 22563T. LMG 23201T (group C) showed a DNA–DNA relatedness value of 52.5 % (±1.6 %) to P. anguilliseptica LMG 21629T. Group C and group D/E thus represent two novel genotypic species. The DNA G+C contents of LMG 23201T, LMG 23199T and LMG 23200, as determined by HPLC (Mesbah et al., 1989Go), were 60.7, 60.0 and 60.5 mol%, respectively.

After an incubation period of 48 h at 28 °C on tryptone soya agar (TSA; Oxoid), a loopful of well-grown cells was harvested and fatty acid methyl esters were prepared as described previously (Vandamme et al., 1992Go), separated and identified using MIDI with the TSBA database version 5.0. The mean fatty acid composition of the strains of the two novel genotypic species, together with that of the type strain of their closest phylogenetic neighbours, is shown in Table 2Go. The strains of group C differed from P. anguilliseptica LMG 21629T in containing smaller amounts of C16 : 0. The strains of the combined group D–E differed from P. flavescens LMG 18387T, P. straminea LMG 21615T, P. argentinensis LMG 22563T, P. anguilliseptica LMG 21629T and group C in containing smaller amounts of C18 : 1{omega}7c and larger amounts of C16 : 1{omega}7c and/or iso-C15 : 02-OH (summed feature 3).


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  		Table 2. Cellular fatty acid composition of the novel species characterized in this study and their closest phylogenetic neighbours

Values are percentages of the total fatty acid content; results for groups of strains are expressed as means with standard deviations in parentheses.Strains: 1, strains LMG 23198, LMG 23199T, LMG 23200, R-20806, R-20807, R-20954, R-20955, R-22829, R-23040 and R-23174 (group D/E; P. borbori); 2, P. straminea LMG 21615T; 3, P. flavescens LMG 18387T; 4, P. argentinensis LMG 22563T; 5, P. anguilliseptica LMG 21629T; 6, LMG 23201T and R-20815 (group C; P. peli). Summed feature 3 contains C16 : 1{omega}7c and/or iso-C15 : 0 2-OH. tr, Trace (<1.0 %); –, not detected.

 
Cell morphology was investigated by light microscopy at a magnification of x1000 for cells grown on TSA for 24 h at 28 °C. Cells were Gram stained and examined for catalase and oxidase activity. The presence of fluorescent pigments was tested under UV light after growth for 48 h on King's B medium (King et al., 1954Go). Utilization of carbon sources and enzyme production (Table 3Go) was tested using API 20 NE, API 50 CH and API ZYM strips (bioMérieux) according to the manufacturer's instructions. The temperature range for growth was tested at 4, 20, 28, 37, 45 and 52 °C after incubation for 48 h on TSA.


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  		Table 3. Physiological characteristics of the novel species and their closest phylogenetic neighbours

Species/strains: 1, P. borbori sp. nov. LMG 23198, LMG 23199T and LMG 23200; 2, P. straminea LMG 21615T; 3, P. straminea strains (data from Uchino et al., 2000Go); 4, P. flavescens LMG 18387T; 5, P. flavescens strains (Uchino et al., 2000Go); 6, P. flavescens strains (Hildebrand etal., 1994Go); 7, P. argentinensis LMG 22563T; 8, P. argentinensis strains (Peix et al., 2005Go); 9, P. anguilliseptica LMG 21629T; 10, P. peli sp.nov. LMG 23201T. Data are from this study unless indicated. +, Positive; W, weakly positive; –, negative; d, strain-dependent, with reaction for type strain in parentheses. All strains characterized in this study were positive for oxidase, catalase and leucine arylamidase. Allstrains were negative for cystine arylamidase, {alpha}-galactosidase, beta-galactosidase, beta-glucuronidase, {alpha}-glucosidase, beta-glucosidase, N-acetyl-beta-glucosaminidase, {alpha}-mannosidase, {alpha}-fucosidase, indole production, acidification of glucose, arginine dihydrolase, urease, aesculin hydrolysis, gelatin hydrolysis and the assimilation of adipate, phenylacetate, erythritol, D-arabinose, L-xylose, D-adonitol, methyl beta-D-xyloside, L-sorbose, L-rhamnose, dulcitol, inositol, D-sorbitol, methyl {alpha}-D-mannoside, methyl {alpha}-D-glucoside, amygdalin, arbutin, aesculin, salicin, D-cellobiose, D-lactose, D-melibiose, inulin, D-melezitose, D-raffinose, starch, glycogen, xylitol, gentiobiose, D-turanose, D-lyxose, D-tagatose, D- and L-fucose, L-arabitol and 2- and 5-ketogluconate.

 
Based on the polyphasic data presented, the strains of group C and of the combined group D/E represent two novel species in the genus Pseudomonas, for which the names Pseudomonas peli sp. nov. and Pseudomonas borbori sp. nov. are proposed.

Description of Pseudomonas peli sp. nov.
Pseudomonas peli (pe'li. Gr. n. pelos sludge; N.L. gen. n. peli of sludge).

After 24 h incubation at 28 °C on TSA, colonies are 1–2 mm, smooth, round with irregular edges and beige to yellow. Cells are rod-shaped (1 µm wide and 2–3 µm long) with rounded ends, Gram-negative, non-spore-forming and non-fluorescent. Cells are motile and oxidase- and catalase-positive. After 24 h, good growth is observed at 28–37 °C, but not below 20 °C or above 45 °C. No anaerobic growth is observed. Enzyme activities and carbon source utilization are given in Table 3Go. Can be differentiated from the type strain of its closest phylogenetic neighbour, P. anguilliseptica LMG 21629T, by the presence of esterase lipase, the absence of acid phosphatase and the inability to reduce nitrate and to assimilate D-galactose, caprate and citrate.

The type strain is LMG 23201T (=DSM 17833T=R-20805T), which has a DNA G+C content of 60.7 mol%. The type strain and strain R-20815 were isolated from a nitrifying inoculum in Gent, Belgium.

Description of Pseudomonas borbori sp. nov.
Pseudomonas borbori (bor'bo.ri. Gr. n. borboros sludge; N.L. gen. n. borbori of sludge).

After 24 h incubation at 28 °C on TSA, colonies are 1–2 mm, smooth, round with irregular edges and beige. Cells are rod-shaped (1 µm wide and 2–3 µm long) with rounded ends, Gram-negative, non-spore-forming and non-fluorescent. Cells are motile and oxidase- and catalase-positive. After 24 h, good growth is observed at 22–28 °C, but not at 4 °C or above 37 °C. No anaerobic growth is observed. Enzyme activities and carbon source utilization are given in Table 3Go. Can be differentiated from all P. straminea strains characterized by Uchino et al. (2000)Go by the ability to assimilate D-maltose and the inability to assimilate L-arabinose, D-galactose, D-mannose and D-mannitol. Can be differentiated from all P. flavescens strains characterized by Uchino et al. (2000)Go and Hildebrand et al. (1994)Go by the ability to assimilate D-maltose and the inability to assimilate D-galactose, D-mannose, D-mannitol and D-trehalose. Can be differentiated from all P. argentinensis strains characterized by Peix et al. (2005)Go by the ability to assimilate D-maltose and the inability to assimilate L-arabinose, D-galactose, D-mannose, D-mannitol and D-trehalose. Can be differentiated from P. anguilliseptica LMG 21629T by the ability to assimilate D-glucose, D-maltose and gluconate, the inability to assimilate D-galactose and the absence of acid phosphatase. Can be differentiated from P. peli by the ability to reduce nitrate and to assimilate D-glucose, D-maltose and gluconate.

The type strain is LMG 23199T (=DSM 17834T=R-20821T), which has a DNA G+C content of 60.7 mol%. The type strain and eight other strains were isolated from a nitrifying inoculum in Gent, Belgium (Table 1Go).


   ACKNOWLEDGEMENTS
 
This work was supported by project grant G.O.A. 1205073 (2003–2008) of the ‘Ministerie van de Vlaamse Gemeenschap, Bestuur Wetenschappelijk Onderzoek’ (Belgium) and the FWO project G20156.02.


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