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1 Institut für Angewandte Mikrobiologie, Universität Giessen, IFZ – Heinrich-Buff-Ring 26–32, D-35392 Giessen, Germany
2 College of Agriculture and Natural Resources, Department of Soil and Environmental Sciences, National Chung Hsing University, Taichung, 402, Taiwan, ROC
3 Department of Biosciences, Mangalore University, Mangalagangotri, India
Correspondence
Peter Kämpfer
peter.kaempfer{at}agrar.uni-giessen.de
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ABSTRACT |
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to include strains of filamentous, chitinolytic, gliding bacteria that transform on ageing into spherical bodies. These bodies were first likened to the microcycst of Sporocytophaga myxococcoides (Leadbetter, 1989), but Reichenbach (1992) disputed the formation of microcysts by Chitinophaga pinensis and pointed to the similarities between the morphology of Chitinophaga pinensis and [Flexibacter] filiformis. Sly et al. (1999) compared the 16S rRNA gene sequences of Chitinophaga pinensis and [Flexibacter] filiformis and found that these two chitinolytic bacteria formed a separate lineage that also included [Flexibacter] sancti, [Cytophaga] arvensicola and [Flavobacterium] ferrugineum, which had already been shown by Nakagawa & Yamasato (1993). Later, Nakagawa et al. (2002) showed that [Flexibacter] japonensis also grouped into this lineage. These authors have previously suggested that [Flexibacter] filiformis, [Flexibacter] sancti and [Cytophaga] arvensicola may constitute a distinct genus on the basis of their phylogenetic relationship as determined from 16S rRNA gene sequence similarities, their strict respiratory metabolism, MK-7 menaquinone content and a base composition in the range 42.8–48.6 mol% G+C.
It was also shown by Takeuchi & Yokota (1992) that [Flavobacterium] ferrugineum was closely related to this group. Recently, Xie & Yokota (2006) proposed the new genus Terrimonas to accommodate [Flavobacterium] ferrigineum and added a second species to this genus, Terrimonas lutea.
Here, we present the characterization of a novel representative of this lineage and propose the formal reclassification of these organisms into the genus Chitinophaga.
A yellow-coloured strain, CC-SG1BT, was isolated from faeces of the millipede Arthrosphaera magna collected in India. Subcultivation was done on nutrient agar (Oxoid) at 28 °C for 24 h. On this agar, CC-SG1BT was able to grow at 10–36 °C, but not at 4 or 45 °C. Growth at 30 °C was also observed on TSA and R2A agar, but not on SS agar (Salmonella-Shigella agar) or MacConkey agar (all from Oxoid). The pH range (pH 4–10 at intervals of 1) and requirement for 0, 1, 2, 3, 5 and 7 % NaCl (w/v) was determined using R2A medium. Gram-staining was performed as described by Gerhardt et al. (1994). Cell morphology was observed under a Zeiss light microscope at x1000, using cells that had been grown for 24 h at 28 °C on nutrient agar (Oxoid). Oxidase activity was tested using oxidase reagent (bioMérieux) according to the instructions of the manufacturer. Flexirubin-like pigments were observed by flooding the plates with 20 % (w/v) potassium hydroxide (Fautz & Reichenbach, 1980).
The cells were Gram-negative, rod-shaped, non-spore-forming, non-fluorescent and oxidase-positive. Results on the cell morphology and other details are given in the species description.
The 16S rRNA gene was analysed as described previously (Kämpfer et al., 2003; Young et al., 2005). Analysis of the sequence data was performed by using the software package MEGA version 2.1 (Kumar et al., 2001), after multiple alignment of sequences by CLUSTAL X (Thompson et al., 1997). A distance matrix method (distance options according to the Kimura two-parameter model) using clustering with the neighbour-joining method (Fig. 1) as well as a discrete character-based maximum-parsimony method (data not shown) were performed. In each case, bootstrap values were calculated based on 1000 replications. The 16S rRNA gene sequence of strain CC-SG1BT was a continuous stretch of 1384 bp. Sequence similarity calculations indicated that strain CC-SG1BT showed the highest degree of similarity to [Flexibacter] filiformis ATCC 29495T (94.8 %) and [Flexibacter] japonensis IFO 16041T (94.6 %), which was described by Fujita et al. (1996). The similarity to Chitinophaga pinensis ACM 2034T was 93.3 %. Lower sequence similarities (<94.5 %) were found with all other species of this lineage.
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using a reversed-phase column (Supelco LC-18-S; Supelco). The G+C content of strain CC-SG1BT was 40.7 mol%.
Chemotaxonomic analyses of respiratory quinones (according to Altenburger et al., 1996) and fatty acids (according to Kämpfer & Kroppenstedt, 1996) were performed. Although respiratory quinones have low resolution within this group, the presence of MK-7 supports affiliation of strain CC-SG1BT to this group, where all species investigated to date have MK-7 as the major quinone.
The fatty acid profile of strain CC-SG1BT revealed 15 : 0 iso and 16 : 1
5c as the major fatty acids and 17 : 0 iso 3-OH and 15 : 0 iso 3-OH as the major hydroxy fatty acids. This is in essential agreement with the fatty acid patterns of [Flexibacter] sancti, [Flexibacter] filiformis, [Flexibacter] japonenis and Chitinophaga pinensis. The two Terrimonas species showed large amounts of 15 : 1 iso H instead of 16 : 15c (Table 1), and thus could be clearly differentiated from [Flexibacter] sancti, [Flexibacter] filiformis, [Flexibacter] japonenis, Chitinophaga pinensis and strain CC-SG1BT.
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). Additional biochemical tests were performed to assess the carbon source utilization pattern by using Biolog GN2 plates, whilst hydrolysis of 19 substrates was investigated using the API ZYM system and API 20E according to the methods outlined by the manufacturer (bioMérieux). Hydrolysis of chitin was studied by the methods of Smibert & Krieg (1994). The results are given in the species description. Strain CC-SG1BT was able to utilize many carbohydrates, but organic acids and amino acids were not utilized.
Despite the relatively low 16S rRNA gene sequence similarities of these organisms (88.5–96.4 %), all the strains under study show a remarkable congruence in phenotypic characters. They all produce MK-7 as the major menaquinone and have homospermidine as the predominant polyamine (Hamana & Nakagawa, 2001). The fatty acid profiles were very similar, composed mainly of 15 : 0 iso and 16 : 15c as the major fatty acids and 17 : 0 iso 3-OH and 15 : 0 iso 3-OH as the major hydroxy fatty acids (Table 1
). Only a few differences are reported in cell morphology and certain physiological tests (Tables 2 and 3).
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; Sly et al., 1999) or to the genus Cytophaga sensu stricto with the type species Cytophaga hutchinsonii (Nakagawa et al., 2002; Sly et al., 1999). It should be noted here that species of the phylogenetically related genus Lewinella share only 84.7–88.4 % 16S rRNA gene sequence similarity. For all these reasons, it is proposed to reclassify [Flexibacter] sancti, [Flexibacter] filiformis, [Flexibacter] japonenis and [Cytophaga] arvensicola to the genus Chitinophaga as the new combinations Chitinophaga sancti comb. nov., Chitinophaga filiformis comb. nov., Chitinophaga japonensis comb. nov. and Chitinophaga arvensicola comb. nov. A novel species, Chitinophaga skermanii sp. nov., is described to accommodate strain CC-SG1BT.
Emended description of the genus Chitinophaga Sangkhobol and Skerman
The description is that of Sangkhobol & Skerman (1981) with the following modifications. A resting stage may be formed. Motility by gliding is possessed by some, but not all species. Some species hydrolyse chitin and some hydrolyse cellobiose.
Description of Chitinophaga sancti comb. nov.
Chitinophaga sancti [sanc'ti. L. n. sanctus saint; L. gen. n. sancti of Saint, perhaps named in honour of Dr Santos Soriano, from whose laboratory the type strain was supplied (the etymology is not clear)].
Basonym: Flexibacter sancti Lewin 1969, 199AL.
The description is identical to that given by Lewin (1969) with the additional chemotaxonomic data provided by Reichenbach (1989), Hamana & Nakagawa (2001) and this study. The type strain is ATCC 23092T=DSM 784T=HAMBI 1988T=NBRC 15057T=LMG 8377T=VKM B-1428T.
Description of Chitinophaga filiformis comb. nov.
Chitinophaga filiformis (fi.li.for'mis. L. neut. n. filum a thread; L. suff. -formis like, of the shape of; N.L. fem. adj. filiformis thread-shaped).
Basonym: Flexibacter filiformis (ex Solntseva 1940) Reichenbach 1989.
The description is identical to that given by Reichenbach (1989) with the additional chemotaxonomic data provided by Hamana & Nakagawa (2001) and this study. The type strain is strain Fx e1 ReichenbachT=ATCC 29495T=CCUG 12809T=CIP 106401T=DSM 527T=HAMBI 1966T=NBRC 15056T.
Description of Chitinophaga japonensis comb. nov.
Chitinophaga japonensis (ja.po.nen'sis. N.L. fem. adj. japonensis pertaining to Japan).
Basonym: Flexibacter japonensis Fujita et al. 1997.
The description is identical to that given by Fujita et al. (1996) and Reichenbach (1989) with the additional chemotaxonomic data provided by Hamana & Nakagawa (2001) and this study. The type strain is strain 758T=CIP 105790T=DSM 13484T=NBRC 16041T=JCM 9735T.
Description of Chitinophaga arvensicola comb. nov.
Chitinophaga arvensicola [ar.ven'si.co'la. L. adj. arvensis belonging to or living in the fields; L. suff. -cola from L. n. incola inhabitant; N.L. n. arvensicola (nominative in apposition) an inhabitant of the fields].
Basonym: Cytophaga arvensicola Oyaizu et al. 1983.
The description is identical to that given by Oyaizu et al. (1982) and Reichenbach (1989) with the additional chemotaxonomic data provided by Hamana & Nakagawa (2001) and this study. The type strain is strain M64T=ATCC 51264T=CIP 104804T=DSM 3695T=IAM 12650T=NBRC 14973T=JCM 2836T.
Description of Chitinophaga skermanii sp. nov.
Chitinophaga skermanii (sker.ma'ni.i. N.L. gen. n. skermanii of Skerman, in honour of V. B. D. Skerman, an Australian microbiologist, in recognition of his numerous contributions to the taxonomy of micro-organisms).
Cells are Gram-negative, non-motile, non-spore-forming rods. Aerobic and oxidase-positive. Good growth after 48 h on nutrient agar, tryptic soy agar and MacConkey agar at 30–40 °C. Colonies on nutrient agar are smooth, orange, circular, translucent and shiny with entire edges, becoming mucoid. Orange pigmentation is non-diffusible, non-fluorescent and turns to cherry red upon the addition of 20 % KOH and retains original colour on addition of HCl. Strains are unable to grow at 5 or 42 °C. Growth occurs at pH 5.5–10 and in 7 % (w/v) NaCl. The detailed fatty acid profile is given in Table 1. Positive for 
-galactosidase, acetoin production, gelatinase and oxidation of glucose, mannitol and melibiose and negative for arginine dihydrolase, lysine decarboxylase, citrate utilization, H2S production, urease, tryptophan deaminase, indole production, oxidation of inositol, sorbitol, rhamnose, sucrose, amygdalin and arabinose and cytochrome oxidase activity. Some differentiating tests are given in Table 3 (methods according to Kämpfer et al., 1991). In addition, the following compounds were utilized as sole carbon sources (tested with the Biolog GN system): 
-cyclodextrin, dextrin, Tweens 40 and 80, N-acetyl-D-galactosamine, N-acetyl-D-glucosamine, cellobiose, L-fucose, gentiobiose, -D-glucose, -D-lactose, lactulose, maltose, D-mannose, D-melibiose, methyl -D-glucoside, D-raffinose, sucrose, D-trehalose, turanose, monomethyl succinate, acetic acid, D-galacturonic acid, -hydroxybutyric acid, -ketobutyric acid, DL-lactic acid, succinic acid, DL-alanine, L-alanyl glycine, L-asparagine, L-aspartic acid, L-glutamic acid, glycyl L-aspartic acid, glycyl L-glutamic acid, L-proline, L-serine, L-threonine and glycerol. The following carbon sources are not utilized as sole sources of carbon: D-arabitol, propionic acid, citric acid, glycogen, adonitol, L-arabinose, i-erythritol, D-fructose, D-galactose, myo-inositol, D-mannitol, D-psicose, L-rhamnose, D-sorbitol, xylitol, pyruvic acid methyl ester, cis-aconitic acid, formic acid, D-galactonic acid lactone, D-glucosaminic acid, D-gluconic acid, D-glucuronic acid, - and 
-hydroxybutyric acids, p-hydroxyphenylacetic acid, itaconic acid, -ketoglutaric acid, malonic acid, D-saccharic acid, sebacic acid, bromosuccinic acid, quinic acid, succinamic acid, L-pyroglutamic acid, -ketovaleric acid, glucuronamide, L-alaninamide, D-alanine, L-histidine, hydroxy-L-proline, D-serine, L-leucine, L-ornithine, L-phenylalanine, inosine, uridine, thymidine, DL-carnitine, -aminobutyric acid, urocanic acid, phenylethylamine, putrescine, 2-aminoethanol, 2,3-butanediol, DL--glycerol phosphate, glucose 1-phosphate and glucose 6-phosphate. Positive test results for enzyme activities are seen for alkaline phosphatase, butyrate esterase, caprylate esterase, leucine arylamidase, valine arylamidase, cystine arylamidase, trypsin, acid phosphatase, naphthol-AS-BI-phosphohydrolase, -galactosidase, -glucosidase, -glucosidase and N-acetyl--glucosaminidase; negative test results are observed for myristate esterase, -chymotrypsin, -galactosidase, -glucuronidase, -mannosidase and -fucosidase.
The type strain is CC-SG1BT (=CCUG 52510T=CIP 109140T), isolated from faeces of the millipede Arthrosphaera magna.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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