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1 Environmental Engineering Research Centre, School of Civil and Environmental Engineering, Nanyang Technological University, Singapore 639798
2 DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Inhoffenstr. 7b, D-38124 Braunschweig, Germany
Correspondence
Abdul Majid Maszenan
cmaszenan{at}ntu.edu.sg
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peptidoglycan (LL-A2pm
Gly with alanine at position 1 of the peptide subunit). The G+C content of the DNA is 69 mol%. Menaquinone MK-9(H4) was the major isoprenoid quinone. The polar lipids included diphosphatidylglycerol and phosphatidylglycerol, while 13-methyltetradecanoic acid (i-C15 : 0) and 1,1-dimethoxy-iso-pentadecane (i-C15 : 0 DMA) were the major components in whole-cell methanolysates. PG-02T stained positively for intracellular polyphosphate granules but not poly-
-hydroxyalkanoates. It produces capsular material and possesses an autoaggregation capability. Phenotypic and 16S rRNA gene sequence analyses showed that PG-02T differed from its closest phylogenetic relatives, namely members of the suborder Propionibacterineae, which includes the genera Tessaracoccus, Microlunatus, Luteococcus, Micropruina, Propionibacterium, Propioniferax, Nocardioides, Friedmanniella and Aeromicrobium, and that it should be placed in a new genus and species as Granulicoccus phenolivorans gen. nov., sp. nov. The type strain of Granulicoccus phenolivorans is PG-02T (=ATCC BAA-1292T=DSM 17626T).
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain PG-02T is AY566575.
Details of signature nucleotides within the 16S rRNA gene sequences of strain PG-02T and related taxa are available as supplementary material in IJSEM Online.
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) and xenobiotic compounds (van Schie & Young, 1998). Due to their wide usage in agricultural and industrial processes, phenol and its derivatives are pollutants of environmental concern (Jensen, 1996). Phenol pollution is often associated with pulp mills, coal mines, cooking plants, oil refineries, industrial resin manufacturing and wood preservation processes and their wastewater (Semple & Cain, 1995; Selvaratnam et al., 1997; Whiteley & Bailey, 2000). In the absence of proper treatment, industrial and agricultural effluents can be an important source of anthropogenic phenol. This, together with the acute toxicity of phenols, has led them to be included as priority pollutants for both the World Health Organization and the US Environmental Protection Agency (Davì & Gnudi, 1999).
The influx of phenol and its derivatives into waste-treatment systems may inhibit microbial activity and result in deterioration of treatment performance and, in extreme cases, complete breakdown of wastewater treatment (Soda et al., 1998; Watanabe et al., 1999). Biodegradation of phenol and phenolics in waste and wastewater is known to be carried out by bacteria of diverse phylogeny, including members from both the Betaproteobacteria and Gammaproteobacteria (Dapaah & Hill, 1992; Arai et al., 1998; Whiteley & Bailey, 2000). Some of these have been isolated and characterized (Hino et al., 1998; Watanabe et al., 1996, 1998; Whiteley & Bailey, 2000; Rehfuss & Urban, 2005). The ability of bacteria to aggregate is important in the bioremediation of toxic chemicals such as phenol in the activated sludge process, since those capable of aggregation will be retained in the system through biomass recycling and be protected from predatory protozoa (van Limbergen et al., 1998; Farrell & Quilty, 2002). Several factors such as substrate gradients, slow growth rates, stress and predation have been suggested to trigger aggregation, although the precise mechanism is not known (Bossier & Verstraete, 1996).
Aerobic granulation, which represents a novel form of cell immobilization without a carrier matrix, was recently used successfully to treat phenolic wastewater at a load that would lead to failure in conventional activated sludge systems (Jiang et al., 2004). It was thought that aggregation of microbial cells into compact granules protected the organisms from possible phenol toxicity (Jiang et al., 2004). In this study, the description of strain PG-02T, one of several phenol degraders that were isolated from these granules, is presented.
Phenol-degrading aerobic granules were cultivated in a laboratory-scale sequencing batch reactor from activated sludge seed, fed with synthetic wastewater containing phenol as the sole carbon source (Jiang et al., 2004). Granules were harvested 8 weeks after steady-state reactor operation. Granules (2.5 g) were added to 15 ml MP medium, which contained (l–1) 1.0 g (NH4)2SO4, 0.2 g MgCl2.6H2O, 0.1 g NaCl, 0.02 g FeCl3.6H2O, 0.01 g CaCl2 and phosphate buffer (1.35 g KH2PO4 and 1.65 g K2HPO4), with trace elements and vitamins as described by Cote & Gherna (1994). The supernatant was serially diluted with medium from 10–1 to 10–7 dilutions and 150 µl aliquots of each dilution was spread onto agar plates containing MP medium solidified with 1.2 % Bacto agar (Difco). Plates were incubated at 25 °C and monitored for 4 weeks for colony growth by examination on a colony counter. Visible colonies were observed after 1 week of incubation. Strain PG-02T takes 10 days to produce visible colonies on MP agar plates. Culture purity was confirmed by microscopic examination of cells taken from single colonies. An axenic culture of strain PG-02T was preserved at –80 °C in MP medium containing 20 % glycerol.
PG-02T is a facultative anaerobe, as growth occurred down the line of inoculation in stab cultures. It grew at 15–37 °C, with optimum growth at 30 °C, and at pH 5.0–8.5, with optimum growth at pH 7.0. Cells stained Gram-positively with the modified Gram-stain method of Hucker (Smibert & Krieg, 1994) and this was confirmed by the absence of stringiness with 3 % KOH treatment (Buck, 1982). No flagella were detected and the motility test confirmed that strain PG-02T was non-motile (Smibert & Krieg, 1994). Polyphosphate granules were observed by the staining method of Rees et al. (1992) in cells grown aerobically with either glucose, acetate or propionate as the sole carbon source, but polyhydroxyalkanoate granules were not detected when cells were incubated anaerobically. Capsular material was observed with the Indian ink stain.
Physiological and biochemical characteristics of strain PG-02T are presented in the descriptions of the genus and species. Enzyme profiles and biochemical characteristics of strain PG-02T were determined using the API ZYM and API 20E systems according to the manufacturer's instructions (bioMérieux). Carbon substrate utilization tests were performed with Biolog GN and GP systems. Cultures were catalase- and urease-positive but oxidase-negative as determined by method of Smibert & Krieg (1994). The genomic G+C content as determined by reversed-phase HPLC (Schumann et al., 1997) was 69 mol%.
Peptidoglycan, menaquinone and polar lipid compositions were analysed as described by Schumann et al. (1997). Fatty acids were extracted and analysed following the instructions of the Microbial Identification System operating manual (MIDI, 1999) and as described by Kämpfer & Kroppenstedt (1996). Strain PG-02T possessed a type A3 peptidoglycan (LL-A2pmGly with alanine at position 1 of the peptide subunit; type A41.1 according to http://www.dsmz.de/species/murein.htm). The peptidoglycan amino acids were alanine/glycine/glutamic acid/LL-diaminopimelic acid (LL-A2pm) in a molar ratio of 1.5 : 0.8 : 1.0 : 1.0, as determined by gas chromatography (MacKenzie, 1987). Cells contained two isoprenoid quinones, MK-9(H4) and MK-8(H4), with a composition ratio of 42 : 1. Polar lipids included diphosphatidylglycerol, phosphatidylglycerol, two unknown glycolipids and three minor phospholipids, and 13-methyltetradecanoic acid (i-C15 : 0) and 1,1-dimethoxy-iso-pentadecane (i-C15 : 0 DMA) were the two major components of whole-cell methanolysates, respectively contributing 50.5 and 37.4 % to the total. Traces of 12-methyltetradecanoic acid (ai-C15 : 0), C12 : 0 DMA and 9,10-cyclo C19 : 0 DMA were also detected (Table 1). 1,1-Dimethoxy-iso-pentadecane (i-C15 : 0 DMA) was identified on the basis of its relative retention times on polar (Varian VF-23ms; 0.25 mmx30 m) and non-polar (5 % phenyl methyl silicone, 0.2 mmx25 m) gas chromatography columns, and its presence was confirmed by GC-MS using a non-polar OV-1 column (0.15 mmx25 m), which revealed fragment ions at m/z 75 and 241. When these were compared with the mass spectrum of i-C16 : 0 DMA, which generated a fragment at m/z 255 (Männistö et al., 2000), the expected mass difference of –14 was observed.
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). A 16S rRNA gene sequence of 1320 nucleotides was obtained in both directions, corresponding to positions 20–1471 of the Escherichia coli sequence according to the nomenclature of Winker & Woese (1991). This sequence was aligned manually against sequences of its close relatives using the alignment editor in BioEdit (Hall, 1997). Sequence analysis was performed with BLAST (Altschul et al., 1997) and CLUSTAL W (Thompson et al., 1994) and SIMILARITY_RANK and SUGGEST_TREE in the Ribosomal Database Project, version 8.0 (Maidak et al., 1997). Distance analysis was performed on a final dataset of an unambiguous alignment of 1162 bases of strain PG-02T and its closest relatives. A phylogenetic tree was constructed from evolutionary distances using the FITCH program in PHYLIP (Felsenstein, 1985). Bootstrap confidence values were obtained with 1000 resamplings.
The sequence data reveal that PG-02T is a member of the Actinobacteria in the domain Bacteria (Stackebrandt et al., 1997). Pairwise comparison of the 16S rRNA gene sequence revealed that strain PG-02T was 95 % similar to Propioniferax innocua ATCC 49929T (Pitcher & Collins, 1991; Yokota et al., 1994) and strains of Microlunatus phosphovorus (Nakamura et al., 1995), less than 95 % similar to the type strains of Luteococcus japonicus and L. sanguinus (Tamura et al., 1994) and Friedmanniella antarctica, F. capsulata and F. spumicola (Schumann et al., 1997; Maszenan et al., 1999b), less than 93 % similar to the type strains of Tessaracoccus bendigoensis (Maszenan et al., 1999a), Propionibacterium propionicum, Propionibacterium avidum, Propionibacterium microaerophilum, Propionibacterium jensenii, Propionibacterium freudenreichii subsp. shermanii, Propionibacterium australiense and Propionibacterium lymphophilum (Charfreitag et al., 1988) and strains of Nocardiodes fulvus, N. luteus, N. albus, N. jensenii, N. dubius and N. kribbensis (Collins et al., 1994; Tamura & Yokota, 1994) and less than 92 % similar to Micropruina glycogenica Lg2T (Shintani et al., 2000), as shown in Fig. 1.
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, it is clear that strain PG-02T fits readily within the suborder Propionibacterineae. All of the closest related genera show complete concurrence with the 16S rRNA signature nucleotides of the taxonomic scheme of Stackebrandt et al. (1997) for members of the suborder Propionibacterineae with the exception of Micropruina glycogenica, which has A–T instead of G–C at nucleotide positions 987 : 1218, and T. bendigoensis and Microlunatus sp. Y-73, which respectively have T–A and A–G instead of A–T at positions 671 : 735 (see Supplementary Table S1 available in IJSEM Online). Further analysis of the 16S rRNA structure of strain PG-02T also concurred with the signature scheme for the family Propionibacteriaceae. However, T. bendigoensis, F. antarctica, Friedmanniella sp. Ellin171 and F. spumicola have G–T instead of A–T at positions 602 : 636. At positions 658 : 748, instead of A–T, Micropruina glycogenica has A–A, members of the genus Friedmanniella have G–A and Microlunatus sp. Y-73 has G–T (Supplementary Table S2). On the basis of these signature nucleotides, strain PG-02T may belong to a novel genus in the family Propionibacteriaceae. However, the scheme of Stackebrandt et al. (1997) will need modification when more actinobacterial isolates within the suborder Propionibacterineae and family Propionibacteriaceae are characterized.
Strain PG-02T differs morphologically from members of the genera Luteococcus, Friedmanniella and Tessaracoccus, which occur predominantly as cocci in pairs and tetrads. Even though members of Micropruina and Microlunatus share a similar morphology with strain PG-02T in that they all occur as single cocci or cocci in pairs, members of both genera are aerobic, while strain PG-02T is facultatively anaerobic based on growth observed down the stab culture. Furthermore, strain PG-02T differs from Micropruina glycogenica as it stores polyphosphate instead of intracellular glycogen and does not contain meso-A2pm in its peptidoglycan. Distinguishing characteristics of strain PG-02T are detailed in Table 2.
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). One unusual chemotaxonomic characteristic of strain PG-02T that differentiates it from members of the genera Luteococcus, Friedmanniella, Tessaracoccus, Propioniferax, Micropruina and Microlunatus is the presence of i-C15 : 0 DMA. 1,1-Dimethyl acetals have been detected in actinobacterial facultative anaerobes such as Propionibacterium freudenreichii and Propionibacterium jensenii within the family Propionibacteriaceae (Kämpfer et al., 2000) and also in the aerobic psychrophiles of the genera Frigoribacterium and Subtercola in the family Microbacteriaceae (Kämpfer et al., 2000; Männistö et al., 2000). However, in PG-02T, i-C15 : 0 DMA made up 37.4 % of the total cellular fatty acids, a much higher level than has been detected in other organisms. An increase in the i-C15 : 0 DMA concentration was noted in Subtercola boreus and Subtercola frigoramans when the growth temperature was lowered from 25 to 4 °C (Männistö et al., 2000). 1,1-Dimethyl acetals are derived from methanolysis of plasmalogens (alk-1'-enyl glyceryl ethers), which are found in the obligate anaerobes Eubacterium lentum and Megasphaera elsdenii and obligately anaerobic members of the Clostridia and the genera Fusobacterium, Propionibacterium, Subtercola and Frigoribacterium (Jantzen & Hofstad, 1981; Johnston & Goldfine, 1994; Kaufman et al., 1990; Verhulst et al., 1987; Kämpfer et al., 2000; Männistö et al., 2000). Kaufman et al. (1990) suggested that 1,1-dimethyl acetal composition may affect cell membrane fluidity in Megasphaera elsdenii. Based on the presence of i-C15 : 0 DMA in unusually large amounts, together with the other chemotaxonomic properties, phenotypic features and the 16S rRNA gene sequence data presented here, we propose that strain PG-02T should be classified in a novel genus and species as Granulicoccus phenolivorans gen. nov., sp. nov. within the family Propionibacteriaceae.
Description of Granulicoccus gen. nov.
Granulicoccus [Gra.nu.li.coc'cus. L. neut. n. granulum a small grain; L. masc. n. coccus a berry; N.L. masc. n. Granulicoccus a coccus from (sludge) granules].
Gram-positive, non-spore-forming cocci, 0.3–1.4 µm in diameter (Fig. 2). Contain type A3 peptidoglycan (LL-A2pmGly with alanine at position 1 of the peptide subunit). Menaquinone MK-9(H4) is the major isoprenoid quinone. Polar lipids include diphosphatidylglycerol and phosphatidylglycerol. 13-Methyltetradecanoic acid and 1,1-dimethoxy-iso-pentadecane are the major components in whole-cell methanolysates. The genus is a member of the family Propionibacteriaceae. The type species is Granulicoccus phenolivorans.
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In addition to the characteristics described for the genus, results obtained with the Biolog GN and GP systems and API 20E system show that the type strain can utilize the following components: Tweens 40 and 80, L-arabinose, 
-D-glucose, -D-lactose, lactulose, maltose, maltotriose, D-mannose, D-melezitose, D-melibiose, methyl -D-galactoside, methyl -D-galactoside, 3-methyl glucose, methyl -D-glucoside, methyl -D-glucoside, psicose, D-raffinose, L-rhamnose, D-ribose, salicin, sedoheptulosan, stachyose, sucrose, D-tagatose, D-trehalose, turanose, D-xylose, myo-inositol, D-mannitol, D-sorbitol, xylitol, 2,3-butanediol, glycerol, DL--glycerol phosphate, glucose 1-phosphate, glucose 6-phosphate, adenosine, AMP, TMP, UMP and fructose 6-phosphate. Acids and their derivatives utilized by the type strain include methyl pyruvate, monomethyl succinate, acetic acid, citric acid, D-galactonic acid lactone, D-gluconic acid, D-glucuronic acid, -, - and -hydroxybutyric acids, p-hydroxyphenylacetic acid, itaconic acid, -ketobutyric acid, -ketoglutaric acid, -ketovaleric acid, lactamide, D-lactic acid methyl ester, L- and DL-lactic acid, D- and L-malic acid, propionic acid, pyruvic acid, quinic acid, D-saccharic acid, sebacic acid, succinic acid, bromosuccinic acid, succinamic acid, N-acetylglutamic acid, L-glutamic acid, glycyl L-glutamic acid and L-pyroglutamic acid. The type strain can consume amino compounds including glucuronamide, alaninamide, D-alanine, L-alanine, L-alanyl glycine, L-asparagine, L-phenylalanine, L-proline, L-serine, inosine, uridine, thymidine and putrescine. Gentiobiose is utilized weakly. -Cyclodextrin, -cyclodextrin, dextrin, glycogen, inulin, mannan, amygdalin, adonitol, D-arabitol, arbutin, cellobiose, i-erythritol, D-fructose, L-fucose, D-galactose, 2-aminoethanol, N-acetyl-D-galactosamine, N-acetyl-D-glucosamine, N-acetylmannosamine, phenyl ethylamine, deoxyadenosine, L-histidine, hydroxy-L-proline, L-leucine, L-ornithine, D-serine, L-threonine, DL-carnitine, D-galacturonic acid, formic acid, D-glucosaminic acid, malonic acid, L-aspartic acid, -aminobutyric acid and urocanic acid are not utilized. Enzyme activities detected by both the API ZYM and API 20E systems are alkaline phosphatase, esterase, lipase, leucine arylamidase, valine arylamidase, naphthol-AS-BI-phosphohydrolase, -galactosidase, -galactosidase, -glucuronidase, -glucosidase and -glucosidase. Activities of the following enzymes are not detected with API ZYM: acid phosphatase, esterase lipase, cystine arylamidase, trypsin, chymotrypsin, N-acetyl--glucosaminidase, -mannosidase and -fucosidase. Activities of -galactosidase, urease and gelatinase are detected with API 20E. Arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase and tryptophan deaminase activities are not detected. H2S and indole are not produced. Voges–Proskauer-negative and does not produce acetoin or reduce nitrate to nitrite. Catalase-positive and oxidase-negative. The genomic G+C content of the type strain is 69 mol%.
The type strain, PG-02T (=ATCC BAA-1292T=DSM 17626T), was isolated from phenol-degrading aerobic granules.
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ACKNOWLEDGEMENTS |
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