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Int J Syst Evol Microbiol 54 (2004), 685-688; DOI  10.1099/ijs.0.02878-0
© 2004 International Union of Microbiological Societies

Reclassification of Cellulosimicrobium variabile Bakalidou et al. 2002 as Isoptericola variabilis gen. nov., comb. nov.

Erko Stackebrandt1, Peter Schumann1 and Xiao-Long Cui1,2

1 DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Mascheroder Weg 1b, 38124 Braunschweig, Germany
2 Yunnan Institute of Microbiology, Yunnan University, Kunming 650091, Yunnan, China

Correspondence
Erko Stackebrandt
erko{at}dsmz.de


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As already depicted in the original publication, the type strain of the species Cellulosimicrobium variabile Bakalidou et al. 2002Go, DSM 10177T, does not cluster unambiguously with the type species, Cellulosimicrobium cellulans DSM 43879T, in phylogenetic analysis. Strain DSM 10177T is moderately related to the recently described species Xylanimonas cellulosilytica, Promicromonospora pachnodae and Xylanibacterium ulmi, forming a lineage that branches between C. cellulans and members of the genus Promicromonospora in most dendrograms generated on the basis of different algorithms and reference strains. The type strains of the two Cellulosimicrobium species resemble each other in morphology, composition of fatty acids, DNA G+C content, phospholipids and the presence of lysine in position 3 of the peptide subunit of peptidoglycan. However, the two strains differ from each other in cell-wall sugars and in the amino acid composition of the A4{alpha}-type peptidoglycan, which contains serine and aspartic acid in C. cellulans, whereas only aspartic acid is present in the interpeptide bridge of C. variabile. This type is also present in Xylanimonas cellulosilytica XIL07T, but not in the neighbouring species P. pachnodae DSM 12657T, which exhibits the L-lys–L-ser–D-Glu type. On the basis of distinct phylogenetic position and the amino acid composition of peptidoglycan, a novel genus and combination for C. variabile, Isoptericola variabilis gen. nov., comb. nov., is proposed.


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The genus Cellulosimicrobium (Schumann et al., 2001Go) is a member of the suborder Micrococcineae, order Actinomycetales, class Actinobacteria (Stackebrandt et al., 1997Go) and is related to the recently described genus Xylanimonas (Rivas et al., 2003Go), the species Promicromonospora pachnodae (Cazemier et al., 2003Go) and, more distantly, to the genera Cellulomonas, Terrabacter, Rarobacter and relatives (Schumann et al., 2001Go; Stackebrandt et al., 2002Go). The genus Cellulosimicrobium contains two species at the time of writing, Cellulosimicrobium cellulans (Schumann et al., 2001Go) and Cellulosimicrobium variabile (Bakalidou et al., 2002Go). In contrast to their generic affiliation (96·6 % 16S rRNA gene sequence similarity), the two species did not group together in 16S rRNA gene sequence analysis (GenBank accession numbers are indicated in Fig. 1Go), as already shown in the original description of C. variabile DSM 10177T (Bakalidou et al., 2002Go). This strain, together with P. pachnodae (Cazemier et al., 2003Go), Xylanimonas cellulosilytica (Rivas et al., 2003Go) and Xylanibacterium ulmi (Rivas et al., 2004Go), which share 97·0–97·3 % gene sequence similarity, branch within the Promicromonospora subline of descent (Fig. 1Go). These latter values are only slightly higher than those shared between C. cellulans and the type strains of the four authentic Promicromonospora species (95·2–95·6 %), demonstrating the intermediate position of C. variabile, P. pachnodae, Xylanibacterium ulmi and Xylanimonas cellulosilytica between C. cellulans (94·9–96·6 %) and authentic Promicromonospora species (95·3–96·5 %). By applying different treeing algorithms [such as neighbour-joining, maximum-likelihood (Felsenstein, 1993Go) and the additive treeing algorithm of DeSoete (1983)Go] to sequences of these organisms and relatives, the branching of C. variabile DSM 10177T and Xylanimonas cellulosilytica with members of the genus Promicromonospora was confirmed in most cases. Small changes in branching points of less closely related organisms were observed when the number and selection of reference organisms were changed (data not shown).



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Fig. 1. Phylogenetic relatedness among members of the genera Cellulosimicrobium, Xylanimonas, Xylanibacterium, Promicromonospora, Cellulomonas and Oerskovia, based on 16S rDNA sequence comparison. Beutenbergia cavernae DSM 12333T (GenBank no. Y18378) and Jonesia denitrificans DSM 20603T (GenBank no. X83811) served as a root. The dendrogram was generated by neighbour-joining analysis (Felsenstein, 1993Go). Numbers within the dendrogram indicate percentages of occurrence of the branching order in 100 bootstrapped trees (only values of 50 % and above are shown). Bar, 5 nucleotide substitutions in 100 nt.

 
The generic affiliation of C. variabile was based on the presence of the following characters: presence of peptidoglycan type A4{alpha} (L-lysine as the diamino acid and aspartic acid in the interpeptide bridge) and galactose and glucose in the cell wall. The description of the peptide structure of C. variabile needs discussion. The murein, as published, contained L-lysine, aspartic acid, glutamic acid and alanine in the molar ratio 1 : 0·9 : 2 : 2, which brings the position of the second molecule of glutamic acid into question (one molecule is known to be at position 2 of the peptide subunit). When analysed in our laboratory, the hydrolysate (120 °C, 6 M HCl, 16 h) of the purified murein revealed that the ratio of L-lysine : aspartic acid : glutamic acid : alanine was 1 : 0·9 : 1 : 2 (Groth et al., 1999Go). Analysis of partial hydrolysis fragments (Schleifer & Kandler, 1972Go) indicated the presence of the peptide L-Lys–Asp. Thus, the A4{alpha} type is of the variation A11.31 (DSMZ, 2001Go).

The topologies of 16S rDNA dendrograms recovered by different phylogenetic methods suggest that C. variabile is not an authentic member of the genus Cellulosimicrobium. However, as already discussed in the paper that excluded C. cellulans from the genus Cellulomonas (Schumann et al., 2001Go), branching points should not be used as the sole criterion for reclassification purposes, inasmuch as the positions of C. cellulans and C. variabile are not supported by bootstrap values of high significance (Fig. 1Go). The rationale for the reclassification of C. variabile as the nucleus of a novel genus adjacent to the genera Xylanimonas and Promicromonospora is also based on the presence of the peptidoglycan type L-Lys–Asp, which is found in Xylanimonas cellulosilytica, but not in strains of C. cellulans (L-Lys–Ser–Asp, type A4{alpha}, variation A11.36) or members of the genus Promicromonospora (L-Lys–Ala, type A3{alpha}, variation A11.4; see footnote to Table 1Go). Also, although C. variabile and C. cellulans both possess galactose, rhamnose and glucose in their whole-cell hydrolysates, C. cellulans also possesses fucose and mannose. Another distinguishing feature is the composition of predominant fatty acid methyl esters: C. variabile contains C14 : 0 and ai-C17 : 0, which are absent in C. cellulans. Polar lipids, determined according to the method of Minnikin et al. (1979)Go and Collins & Jones (1980)Go, are phosphatidylglycerol, diphosphatidylglycerol, phosphatidylinositol and two unknown phospholipids. This composition differs only quantitatively from that found in C. cellulans. However, differences in fatty acid and polar lipid compositions and whole-cell sugars should not be overvalued and these properties are mainly used for the differentiation of species, not of genera.


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Table 1. Chemotaxonomic characteristics that differentiate strains of the genera Cellulosimicrobium, Xylanimonas and Promicromonospora

Taxa: 1, C. variabile DSM 10177T [data from Bakalidou et al. (2002)Go]; 2, C. cellulans DSM 43879T [data from Stackebrandt & Keddie (1986)Go and Schumann et al. (2001)Go]; 3, Xylanimonas cellulosilytica XIL07T [data from Rivas et al. (2003)Go]; 4, P. pachnodae DSM 12657T; 5, authentic Promicromonospora species [data from Busse et al. (2003)Go]. +, Positive; W, weak; –, negative; DPG, diphosphatidylglycerol; GL, unknown glycolipid; PG, phosphatidylglycerol; PGL, unknown phosphoglycolipid; PI, phosphatidylinositol; PIM, phosphatidylinositol mannosides; PL, unknown phospholipid; ND, not determined.

 
The nearest neighbours of C. variabile as determined to date are Xylanimonas cellulosilytica and Xylanibacterium ulmi, cellulase- and xylan-hydrolysing organisms from Ulmus nigra, and P. pachnodae (Cazemier et al., 2003Go), a (hemi)-cellulolytic and xylanolytic bacterium that was isolated from the hindgut of larvae of the herbivorous beetle Pachnoda marginata. Chemotaxonomic data and thorough phenotypic analysis of the latter prokaryotic organism are lacking. Based on the evidence indicated in Table 1Go, we propose to reclassify C. variabile as the type species of a novel genus, for which the name Isoptericola variabilis Bakalidou et al. 2002Go gen. nov., comb. nov. is proposed. The name has been chosen to depict that C. variabile was isolated from the hindgut of the Australian termite Mastotermes darwiniensis (Froggatt).

Description of Isoptericola gen. nov.
Isoptericola (I.sop.te.ri'co.la. N.L. n. Isoptera order of termites; L. masc. suffix -cola inhabitant; N.L. masc. n. Isoptericola inhabitant of termites).

The following description is based on the description of the species Cellulosimicrobium variabile DSM 10177T (Bakalidou et al., 2002Go) and our own data (peptidoglycan).

Cells are rod-shaped, V-shaped or coccoid and non-motile. Primary mycelium is formed. Gram-positive. Murein contains the amino acids lysine, aspartic acid, glutamic acid and alanine in a molar ratio of 1 : 0·9 : 1 : 2 and belongs to the peptidoglycan type A4{alpha}, variation A11.31. N-Glycolylmuramic acid, mycolic acids and hydroxy fatty acids are absent. Whole-cell sugars are galactose, rhamnose and glucose (ratio 4 : 2 : 1). Main menaquinone is MK9(H4). Major fatty acids are ai-C15 : 0 (53·6 %), i-C15 : 0 (17 %), C16 : 0 (7·2 %), i-C16 : 0 (6·0 %), ai-C17 : 0 (7·0 %) and C14 : 0 (6·6 %). i-C14 : 0 (1·5 %), i-C17 : 0 (0·6 %) and C15 : 0 (0·5 %) occur in smaller amounts. Phospholipids are phosphatidylglycerol, diphosphatidylglycerol, phosphatidylinositol and two unknown phospholipids. Cellulolytic and xylanolytic; facultatively anaerobic; acid is produced from some carbohydrates. DNA G+C content is 70–72 mol% (nuclease P1 digest, HPLC). Phylogenetically related to Xylanimonas cellulosilytica, Xylanibacterium ulmi and Promicromonospora pachnodae. The type species is Isoptericola variabilis Bakalidou et al. 2002Go.

Description of Isoptericola variabilis Bakalidou et al. 2002Go corrig., comb. nov.
Isoptericola variabilis (va.ri.a'bi.lis. L. masc. adj. variabilis variable, as cells can be rods or cocci).

The description is the same as that given by Bakalidou et al. (2002)Go with the modification of the amino acid composition of the murein, as given in the genus description.

The type strain is MX5T (=DSM 10177T=ATCC BAA-303T).


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Bakalidou, A., Kämpfer, P., Berchtold, M., Kuhnigk, T., Wenzel, M. & König, H. (2002). Cellulosimicrobium variabile sp. nov., a cellulolytic bacterium from the hindgut of the termite Mastotermes darwiniensis. Int J Syst Evol Microbiol 52, 1185–1192.[Abstract]

Busse, H.-J., Zlamala, C., Buczolits, S., Lubitz, W., Kämpfer, P. & Takeuchi, M. (2003). Promicromonospora vindobonensis sp. nov. and Promicromonospora aerolata sp. nov., isolated from the air in the medieval chapel ‘Virgilkapelle’ in Vienna. Int J Syst Evol Microbiol 53, 1503–1507.[Abstract/Free Full Text]

Cazemier, A. E., Verdoes, J. C., Reubsaet, F. A. G., Hackstein, J. H. P., van der Drift, C. & Op den Camp, H. J. M. (2003). Promicromonospora pachnodae sp. nov., a member of the (hemi)cellulolytic hindgut flora of larvae of the scarab beetle Pachnoda marginata. Antonie van Leeuwenhoek 83, 135–148.[CrossRef][Medline]

Collins, M. D. & Jones, D. (1980). Lipids in the classification and identification of coryneform bacteria containing peptidoglycans based on 2,4-diaminobutyric acid. J Appl Bacteriol 48, 459–470.

DeSoete, G. (1983). A least squares algorithm for fitting additive trees to proximity data. Psychometrika 48, 621–626.[CrossRef]

DSMZ (2001). Catalogue of Strains, 7th edn. Braunschweig: Deutsche Sammlung von Mikroorganismen und Zellkulturen.

Evtushenko, L. I., Levanova, G. F. & Agre, N. S. (1984). Nucleotide composition of DNA and amino acid composition of A4 peptidoglycan in Promicromonospora citrea. Mikrobiologiya 53, 519–520.

Felsenstein, J. (1993). PHYLIP (phylogeny inference package), version 3.5c. Department of Genetics, University of Washington, Seattle, USA.

Groth, I., Schumann, P., Martin, K., Schuetze, B., Augsten, K., Kramer, I. & Stackebrandt, E. (1999). Ornithinicoccus hortensis gen. nov., sp. nov., a soil actinomycete which contains L-ornithine. Int J Syst Bacteriol 49, 1717–1724.[CrossRef][Medline]

Kalakoutskii, L. V., Agre, N. S., Prauser, H. & Evtushenko, L. I. (1989). Genus Promicromonospora. In Bergey's Manual of Systematic Bacteriology, vol. 4, pp. 2392–2395. Edited by S. T. Williams, M. E. Sharpe & J. G. Holt. Baltimore: Williams & Wilkins.

Minnikin, D. E., Collins, M. D. & Goodfellow, M. (1979). Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 47, 87–95.

Rivas, R., Sánchez, M., Trujillo, M. E., Zurdo-Piñeiro, J. L., Mateos, P. F., Martínez-Molina, E. & Velázquez, E. (2003). Xylanimonas cellulosilytica gen. nov., sp. nov., a xylanolytic bacterium isolated from a decayed tree (Ulmus nigra). Int J Syst Evol Microbiol 53, 99–103.[Abstract/Free Full Text]

Rivas, R., Trujillo, M. E., Schumann, P., Kroppenstedt, R. M., Sánchez, M., Mateos, P. F., Mártinez-Molina, E. & Velázquez, E. (2004). Xylanibacterium ulmi gen. nov., sp. nov., a novel xylanolytic member of the family Promicromonosporaceae. Int J Syst Evol Microbiol 54, 557–561.[Abstract/Free Full Text]

Schleifer, K. H. & Kandler, O. (1972). Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36, 407–477.[Free Full Text]

Schumann, P., Weiss, N. & Stackebrandt, E. (2001). Reclassification of Cellulomonas cellulans (Stackebrandt and Keddie 1986Go) as Cellulosimicrobium cellulans gen. nov., comb. nov. Int J Syst Evol Microbiol 51, 1007–1010.[Abstract]

Stackebrandt, E. & Keddie, R. M. (1986). Genus Cellulomonas Bergey et al. 1923, 154, emend. mut. char. Clark 1952, 50AL. In Bergey's Manual of Systematic Bacteriology, vol. 2, pp. 1325–1329. Edited by P. H. A. Sneath, N. S. Mair, M. E. Sharpe & J. G. Holt. Baltimore: Williams & Wilkins.

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