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1 Escola Superior de Biotecnologia, Universidade Católica Portuguesa, 4200-072 Porto, Portugal
2 LEPAE-Departamento de Engenharia Química, Faculdade de Engenharia, Universidade do Porto, 4200-465 Porto, Portugal
3 Area de Microbiologia, Universitat de les Illes Balears, 07071 Palma de Mallorca, Spain
Correspondence
Célia M. Manaia
celman{at}esb.ucp.pt
| ABSTRACT |
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-hydroxybutyrate and had an optimal growth temperature of about 47 °C. Strain N2-680T was unable to reduce nitrate and could use organic acids, amino acids and carbohydrates as single carbon sources. Chemotaxonomic analysis revealed that ubiquinone 8 was the major respiratory quinone of this organism and that phosphatidylethanolamine and phosphatidylglycerol were the major polar lipids. At 50 °C, the major components in fatty acid methyl ester analysis were C16 : 0 and cyclo-C17 : 0. The highest 16S rDNA sequence identity of isolate N2-680T was to Leptothrix mobilis and Ideonella dechloratans (95·7 %) and to Rubrivivax gelatinosus and Aquabacterium commune (95·6 %). 16S rDNA sequence similarities to species of two related thermophilic genera, Caldimonas manganoxidans and Tepidimonas ignava, were lower (93·6 and 94·7 %). On the basis of phylogenetic analyses and physiological and chemotaxonomic characteristics, it is proposed that isolate N2-680T represents a new genus and species, for which the name Caenibacterium thermophilum gen. nov., sp. nov. is proposed.
-hydroxybutyratePublished online ahead of print on 7 February 2003 as DOI 10.1099/ijs.0.02622-0.
The GenBank/EMBL/DDBJ accession number for the 16S rDNA sequence of isolate N2-680T is AJ512945.
| INTRODUCTION |
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-subclass of Proteobacteria that includes the genera Rubrivivax, Roseateles, Leptothrix, Ideonella, Aquabacterium and Caldimonas constitutes a heterogeneous group from physiological and ecological perspectives. Bacteriochlorophyll-containing members of this group are represented by the species Rubrivivax gelatinosus (Willems et al., 1991
The genus Leptothrix includes sheath-forming bacteria capable of manganese oxidation, occurring in natural iron- and manganese-containing systems (Mulder, 1989
; Siering & Ghiorse, 1996
). Members of the genus Leptothrix have been found in both unpolluted natural waters and man-made habitats such as activated sludge (Mulder, 1989
; Mulder & Deinema, 1992
). Ideonella dechloratans was isolated from activated sludge and is characterized by its ability to use chlorate as an electron acceptor (Malmqvist et al., 1994
). The genus Aquabacterium was defined to accommodate three bacterial strains isolated from biofilm occurring in the Berlin drinking-water distribution system (Kalmbach et al., 1999
). These organisms are strict heterotrophs capable of growth on nutrient-rich medium but unable to metabolize carbohydrates.
Among the phylogenetic lineage RubrivivaxRoseatelesLeptothrixIdeonellaAquabacterium, thermophily is represented by the genus Caldimonas (Takeda et al., 2002
). Caldimonas manganoxidans, the single species within this genus with a validly published name, comprises chemo-organotrophic organisms capable of manganese oxidation and able to grow on poly(3-hydroxybutyrate) (Takeda et al., 1998
, 2002
). The type strain of Caldimonas manganoxidans has an optimal temperature for growth around 50 °C and was isolated from a hot spring in Japan, exposed to sun and extensively colonized with cyanobacteria, potential producers of large amounts of poly(3-hydroxybutyrate) (Takeda et al., 1998
). More phylogenetically distantly related to this lineage is the thermophile Tepidimonas ignava (Moreira et al., 2000
), with an optimal temperature for growth around 55 °C. Tepidimonas ignava, isolated from a Portuguese hot spring, represents a chemolithoheterotrophic organism, capable of using sulphur compounds as an energy source.
This paper reports the isolation and characterization of a thermophilic bacterium enriched on a poly-
-caprolactone thermoplastic from a thermophilic aerobic digester of activated sludge. Based on phenotypic, chemotaxonomic and 16S rDNA-based phylogenetic analysis, the definition of a new genus and species is proposed within the
-subclass of Proteobacteria with the name Caenibacterium thermophilum gen. nov., sp. nov., and the type strain is N2-680T.
| METHODS |
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-caprolactone thermoplastic (oxepanone homopolymer, with a molecular mass of 80 000; Solvay). Cultures were transferred weekly to fresh medium for 2 months. Isolate N2-680T was purified from the mixed culture obtained in this enrichment by subculturing on LB broth containing 20 g agar l-1 (Carlton & Brown, 1981
Determination of morphological, growth and biochemical characteristics.
Colony and cell morphology of strain N2-680T were examined using standard protocols (Doetsch, 1981
). Cell morphology, Gram-staining reaction, production of spores and the accumulation of poly-
-hydroxybutyrate (PHB) granules were determined by microscopic examination, following procedures described previously (Doetsch, 1981
; Smibert & Krieg, 1981
). The number and position of flagella were determined by light microscopy, after staining the cells with Ryu stain (Heimbrook et al., 1989
).
The growth temperature range was examined by measuring turbidity (at 610 nm) of cultures in 250 ml screw-capped Erlenmeyer flasks containing 50 ml LB medium incubated in an orbital water-bath shaker.
Phenotypic tests on isolate N2-680T were carried out as described by Smibert & Krieg (1981)
, using 2-day cultures on LB agar. Unless otherwise stated, all incubations were performed at 50 °C. The pH range for growth was examined in LB medium, using 10 mM MES (Sigma) to adjust the pH between 5·0 and 6·0 or 10 mM CAPS (Sigma) to adjust the pH between 9·0 and 11·0. The enzymic activity was tested using the API ZYM system, following the instructions of the manufacturer (bioMérieux). Hydrogenase activity was determined based on the description of Aragno & Schlegel (1992)
and Stöhr et al. (2001)
. A cell suspension was prepared in sterile phosphate buffer (54 mM, pH 7·2) with cells grown on LB agar and washed twice in the same buffer. This suspension was divided into two sets of aliquots, in rubber-sealed vials. In one set, an atmosphere containing about 80 % H2 was generated, while, in the second set, the atmosphere contained only nitrogen. A solution of triphenyltetrazolium was added in order to obtain a final concentration of 0·25 % (w/v) and incubated at 50 °C, protected from light. Non-inoculated phosphate buffer as well as phosphate buffer inoculated with an organism lacking hydrogenase activity were used as negative controls. The development of a red colour indicated the reduction of triphenyltetrazolium and the presence of hydrogenase activity.
Manganese oxidation was tested on SphaerotilusLeptothrix medium (l-1: 1 g yeast extract, 1·5 g peptone, 0·2 g MgSO4.7H2O, 0·5 g ferric ammonium citrate, 50 mg CaCl2, 50 mg MnSO4.H2O, 10 mg FeCl3.6H2O, 20 g agar, pH 7·1). Leptothrix mobilis DSM 10617T was used as a positive control and the presence of manganese oxides was evaluated using benzidinium hydrochloride (Nealson, 1992
; Spring et al., 1996
). Degradation of the polycaprolactone oxydiethylene ester (CAPA 200; Solvay), a polymer derived from
-caprolactone with a mean molecular mass of 550, was tested using that polymer (2·5 g l-1) dispersed in agar medium with the following composition (l-1): 1 g NH4NO3, 0·2 g yeast extract, 0·25 g K2HPO4, 0·13 g MgSO4, 0·13 g NaCl, 2·5 mg Fe2(SO4)3, 2·5 mg MnSO4, 50 µg K2MoO4, 50 µg Na3BO3, 50 µg Co(NO3)2, 50 µg FeCl3, 50 µg CdSO4, 50 µg CuSO4 and 50 µg ZnSO4. Degradation was indicated by the appearance of a clear zone around the colonies.
The nutritional pattern was characterized using the API 50CH system and a defined medium (medium B) [l-1: 5 g (NH4)2SO4, 0·31 g KH2PO4, 0·45 g K2HPO4, 1·2 g Na2HPO4.2H2O, 0·1 g NaCl, 0·05 g CaCl2, 0·4 g MgSO4.7H2O, 5 mg histidine, 20 mg tryptophan, 20 mg methionine, 200 µg p-aminobenzoic acid, 20 µg biotin, 2 µg folic acid, 10 mg myo-inositol, 400 µg nicotinic acid, 2 mg calcium pantothenate, 400 µg pyridoxine hydrochloride, 200 µg riboflavin, 400 µg thiamin hydrochloride, 500 µg H3BO3, 200 µg FeCl3.6H2O, 400 µg ZnSO4.7H2O, 400 µg MnSO4.4H2O, 40 µg CuSO4.5H2O, 200 µg Na2MoO4.2H2O, 100 µg KI, 2·5 g agar]. Chemolithoautotrophic growth was tested using medium A supplemented with filter-sterilized 30 mM NaHCO3 and different electron donors. The use of H2 as energy source was tested according to Suyama et al. (1999)
. The ability to use sulphur or thiosulphate as electron donors was tested by adding 5 g sulphur flowers l-1 to medium A or supplementing the same medium with filter-sterilized sodium thiosulphate at final concentrations of 2·5 and 5 g l-1. Positive controls, containing 25 mM acetate or acetate and the inorganic electron donor, were run in parallel. The ability to grow in the absence of a source of combined nitrogen was tested using medium A without ammonium sulphate.
The production of photosynthetic pigments was analysed as described by Suyama et al. (1999)
. Absorption spectra of ultrasonically disrupted cells, pre-grown in medium A supplemented with acetate, were obtained in phosphate buffer.
Determination of genotypic characteristics.
For the determination of DNA base composition, genomic DNA was isolated as described by Cashion et al. (1977)
and the G+C content of DNA was analysed by HPLC (Mesbah et al., 1989
).
16S rDNA sequence analysis.
The nucleic acid sequence of the 16S rRNA gene was determined after PCR amplification from total DNA extracts, using procedures described previously (Nogales et al., 2001
). The primers described by Lane (1991)
were used. The nucleotide sequence was compared with reference 16S rDNA sequences in the EMBL database using the FASTA program (Pearson & Lipman, 1988
) and subsequently aligned with reference sequences included in the ARB package (http://www.arb-home.de). Evolutionary distances, derived from sequence-pair dissimilarities (Jukes & Cantor, 1969
), were calculated using the PHYLIP package (Felsenstein, 1989
). Non-homologous and ambiguous nucleotide positions were excluded from the calculations.
Determination of chemotaxonomic characteristics.
Cultures for polar lipid analysis were grown in LB medium until the end of exponential phase of growth. Lipid extractions were performed as described previously (Prado et al., 1988
). Individual polar lipids were separated by one-dimensional TLC on silica gel G plates (0·25 mm thickness; Merck), using a solvent system of chloroform/methanol/acetic acid/water (80 : 17 : 10 : 4, by vol.).
For the analysis of methylated fatty acids, isolate N2-680T was cultivated for 3 days on LB agar at 30 and 50 °C. The harvesting of cells and the preparation of fatty acid methyl esters (FAMEs) were performed as described by Kuykendall et al. (1988)
. FAMEs were separated as described by Moreira et al. (2000)
and the individual components were identified and quantified by comparison with the retention times of authentic standards, using the MIS Library Generation software (Microbial ID Inc.). FAMEs were extracted and analysed at least twice.
For the analysis of respiratory quinones, cells were cultured on LB agar, harvested, freeze-dried and extracted according to Tindall (1989)
and the extracts were analysed as described by Moreira et al. (2000)
.
| RESULTS AND DISCUSSION |
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-caprolactone thermoplastic was used to enrich a thermophilic population capable of using synthetic polymers as the sole source of carbon and energy. The enrichment procedure resulted in a mixed culture containing isolate N2-680T, which was purified by successive subculturing on LB agar. Individual cells of isolate N2-680T were Gram-negative rods, 1·3 µm long and 0·5 µm wide, containing intracellular PHB granules. A polar flagellum was observed only during the early stages of growth. Endospores, prosthecae or cell sheaths were not observed on isolate N2-680T. When cultured on LB agar, strain N2-680T produced non-pigmented colonies, 12 mm in diameter after 3648 h growth.
In pure culture, isolate N2-680T was unable to grow in mineral medium A supplemented with the caprolactone polymer used for enrichment. The same medium supplemented with acetate supported growth, even after successive transfers, indicating that this organism does not require specific growth factors, such as vitamins or amino acids. Isolate N2-680T could also grow on nutrient-rich media such as LB. In LB medium, the optimal growth temperature of strain N2-680T was around 47 °C, with a maximal temperature for growth of 57 °C.
The physiological properties of strain N2-680T are summarized in Table 1
. Strain N2-680T is composed of oxidase- and catalase-positive, strictly aerobic bacteria, unable to reduce nitrate or nitrite. No photosynthetic pigments or manganese oxidation were observed. This isolate could reduce triphenyltetrazolium in the presence of hydrogen but not in its absence, suggesting that hydrogenase activity is present. However, isolate N2-680T could not grow autotrophically in the presence of hydrogen gas. Autotrophic growth did not occur in the presence of molecular sulphur or thiosulphate as electron donors.
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Isolate N2-680T presented poor, but visible growth on mineral medium A with acetate, without ammonium sulphate. However, after two successive transfers under the same conditions, no growth occurred, probably indicating that the cell proliferation observed in the initial cultures was due to the use of nitrogen-containing compounds present in reserve materials. Based on these results, is possible to conclude that isolate N2-680T is unable to use N2 as a nitrogen source.
Analysis of the polar lipid pattern of strain N2-680T by TLC revealed the presence of phosphatidylethanolamine (PE) and phosphatidylglycerol (PG) as the major phospholipids. The only respiratory quinone detected was ubiquinone 8. The predominance of the phospholipids PE and PG and the presence of ubiquinone 8 confirm the inclusion of isolate N2-680T within the
-subclass of the Proteobacteria (Wilkinson, 1988
; Suzuki et al., 1993
).
The fatty acid composition of strain N2-680T was analysed using LB agar cultures grown at 30 and 50 °C (Table 2
). At 30 °C, the predominant components were C16 : 0, C16 : 1 and C18 : 1, in approximately equal proportions. At this temperature, cyclo-C17 : 0 represented only 6·5 % of the total fatty acids. At 50 °C, C16 : 0 and cyclo-C17 : 0 represented about 70 % of the total FAMEs. Since cyclopropane fatty acids are secondary products of fatty acid biosynthesis (Suzuki et al., 1993
), the use of cyclo-fatty acids as chemotaxonomic markers should be considered with caution. However, appreciable amounts (more than 20 %) of the fatty acid cyclo-C17 : 0 were reproducibly detected when this isolate was cultivated for 1 and 3 days at 50 °C. The hydroxy fatty acids 3-OH-C10 : 0 and 3-OH-C12 : 0 were detected at 30 and 50 °C. Temperature-induced variations in the fatty acid composition of isolate N2-680T agree with the tendency observed for other moderately thermophilic Proteobacteria, in which higher growth temperatures induce an increase in the content of cyclic fatty acids and a decrease in the degree of chain unsaturation (Manaia & Moore 2002
; Busse et al., 2002
).
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-subclass of the Proteobacteria, being most closely related to the genera Ideonella, Leptothrix, Rubrivivax and Aquabacterium and the species Alcaligenes latus, as shown in Fig. 1
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-Proteobacteria. Among the few common characteristics attributed to members of this phylogenetic lineage are the accumulation of PHB granules, the presence of ubiquinone 8 and a DNA base composition ranging from 66 to 72 mol% G+C. The fatty acid composition is not published for all species with validly published names within this phylogenetic lineage; however, based on the data available (Busse & Auling, 1992
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More distantly related phylogenetic neighbours of strain N2-680T are the thermophilic species Caldimonas manganoxidans and Tepidimonas ignava, which share 16S rDNA sequence identity of 93·6 and 94·7 %, respectively, with the novel isolate. Despite the fact that the three organisms are thermophilic, the comparatively low values of 16S rDNA sequence identity and the differences observed for other phenotypic traits are consistent with the definition of distinct genera. Caldimonas manganoxidans can be distinguished from strain N2-680T by its ability to oxidize manganese and to use malate, mannitol, sorbitol, D-glucose, D-galactose, maltose and sucrose as single carbon sources (Takeda et al., 2002
). Tepidimonas ignava differs from strain N2-680T in the absence of PHB granules, the inability to grow in the presence of 3 % NaCl and to hydrolyse Tween 80, the requirement for specific growth factors, the inability to use arabinose, cellobiose and glycerol and the ability to use malate and asparagine as single carbon sources. Moreover, the optimum temperature for growth of Tepidimonas ignava is 55 °C, slightly higher than that observed for strain N2-680T (Moreira et al., 2000
). The phylogenetic position of strain N2-680T, along with its phenotypic characteristics, support the description of a new genus. Characteristics that differentiate between strain N2-680T, its phylogenetic closest relatives and the thermophilic species more phylogenetically closely related to this isolate are summarized in Table 3
.
Based on FASTA analysis, isolate N2-680T showed 99·9 % 16S rDNA identity to a thermophilic organism, strain DhA-71 (EMBL accession no. AF125876), described as capable of degrading dehydroabietic acid (Yu & Mohn, 1999
), indicating that the two isolates might belong to the same species. Strain DhA-71 was isolated from municipal compost in Canada, whereas strain N2-680T was recovered from a thermophilic sludge digester in Portugal, suggesting that this species may have a widespread distribution in such habitats.
The phenotypic and chemotaxonomic characterization of strain N2-680T and 16S rDNA-based phylogenetic analysis revealed that this bacterium is not affiliated to any validly named genus. The definition of the new genus Caenibacterium gen. nov., containing the species Caenibacterium thermophilum sp. nov., is proposed, with isolate N2-680T as the type strain.
Description of Caenibacterium gen. nov.
Caenibacterium (Cae'ni.bac.te.ri.um. L. n. caenum mud, sludge; N.L. n. bacterium from Gr. n. bakterion rod; N.L. neut. n. Caenibacterium a rod-shaped bacterium isolated from sludge).
Forms rod-shaped cells that stain Gram-negative, with a polar flagellum. Endospores are not formed. PHB granules are accumulated. Oxidase and catalase are positive. Slightly thermophilic. Major phospholipids are phosphatidylethanolamine and phosphatidylglycerol; ubiquinone 8 is the major respiratory quinone. Major fatty acids include C16 : 0, C16 : 1 and C18 : 1 or its secondary products such as cyclo-C17 : 0. The hydroxylated fatty acids 3-OH-C10 : 0 and 3-OH-C12 : 0 are present. Nitrate is not reduced, photosynthetic pigments are not present and Mn2+ is not oxidized. No autotrophic growth occurs. Chemo-organotrophic. Organic acids, amino acids and hydrocarbons are used as single carbon sources. The type species is Caenibacterium thermophilum.
Description of Caenibacterium thermophilum sp. nov.
Caenibacterium thermophilum (ther.mo'phi.lum. Gr. n. therme warm; Gr. adj. philos friendly to; N.L. neut. adj. thermophilum loving warmth, thermophilic).
Forms rod-shaped cells, 1·3 µm long and 0·5 µm wide. A single polar flagellum is observed at the early stages of growth. Colonies grown on LB agar are non-pigmented, slightly brilliant and 12 mm in diameter after 3648 h growth. Growth occurs above 25 °C and below 57 °C; the optimal growth temperature is approximately 47 °C. Growth occurs between pH 6 and 9. Hydrogenase- and tweenase-positive. Acetate, citrate, gluconate, caproate, glutamic acid, cellobiose, arabinose, glycerol, alanine, proline and serine are used as single carbon sources. Capable of degradation of polycaprolactone oxydiethylene ester. The major fatty acids at 50 °C are C16 : 0 and cyclo-C17 : 0. The DNA G+C content of the type strain is 70·1 mol%.
The type strain, strain N2-680T (=DSM 15264T=LMG 21760T), was isolated from a thermophilic aerobic digester of wastewater-treatment sludge.
| ACKNOWLEDGEMENTS |
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I. Vaz-Moreira, M. F. Nobre, O. C. Nunes, and C. M. Manaia Gulbenkiania mobilis gen. nov., sp. nov., isolated from treated municipal wastewater Int J Syst Evol Microbiol, May 1, 2007; 57(5): 1108 - 1112. [Abstract] [Full Text] [PDF] |
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Y.-J. Chou, S.-Y. Sheu, D.-S. Sheu, J.-T. Wang, and W.-M. Chen Schlegelella aquatica sp. nov., a novel thermophilic bacterium isolated from a hot spring Int J Syst Evol Microbiol, December 1, 2006; 56(12): 2793 - 2797. [Abstract] [Full Text] [PDF] |
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T. Lutke-Eversloh, K. Elbanna, M. C. Cnockaert, J. Mergaert, J. Swings, C. M. Manaia, and A. Steinbuchel Caenibacterium thermophilum is a later synonym of Schlegelella thermodepolymerans Int J Syst Evol Microbiol, November 1, 2004; 54(6): 1933 - 1935. [Abstract] [Full Text] [PDF] |
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C. M. Manaia, B. Nogales, N. Weiss, and O. C. Nunes Gulosibacter molinativorax gen. nov., sp. nov., a molinate-degrading bacterium, and classification of 'Brevibacterium helvolum' DSM 20419 as Pseudoclavibacter helvolus gen. nov., sp. nov. Int J Syst Evol Microbiol, May 1, 2004; 54(3): 783 - 789. [Abstract] [Full Text] [PDF] |
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C. M. Manaia, B. Nogales, and O. C. Nunes Tepidiphilus margaritifer gen. nov., sp. nov., isolated from a thermophilic aerobic digester Int J Syst Evol Microbiol, September 1, 2003; 53(5): 1405 - 1410. [Abstract] [Full Text] [PDF] |
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