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Int J Syst Evol Microbiol 54 (2004), 1235-1237; DOI  10.1099/ijs.0.63093-0
© 2004 International Union of Microbiological Societies

Stenotrophomonas africana Drancourt et al. 1997 is a later synonym of Stenotrophomonas maltophilia (Hugh 1981) Palleroni and Bradbury 1993

Tom Coenye1, Elke Vanlaere1, Enevold Falsen2 and Peter Vandamme1

1 Laboratorium voor Microbiologie, Universiteit Gent, Gent, Belgium
2 CCUG Culture Collection, University of Göteborg, Göteborg, Sweden

Correspondence
Tom Coenye
Tom.Coenye{at}UGent.be


   ABSTRACT
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Type and reference strains of Stenotrophomonas maltophilia and Stenotrophomonas africana were compared with each other and with the type strains of other Stenotrophomonas species, using SDS-PAGE of whole-cell proteins, DNA–DNA hybridization and extensive biochemical characterization. S. maltophilia LMG 958T and S. africana LMG 22072T had very similar whole-cell-protein patterns and were also biochemically very similar. A DNA–DNA binding level of 70 % between both type strains confirmed that S. africana and S. maltophilia represent the same taxon. It is concluded that S. africana is a later synonym of S. maltophilia.

Published online ahead of print on 16 January 2004 as DOI 10.1099/ijs.0.63093-0.

Supplementary material showing the strains used in the present study is available in IJSEM Online.


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The genus Stenotrophomonas was created in 1993 to accommodate Xanthomonas maltophilia (formerly Pseudomonas maltophilia) (Palleroni & Bradbury, 1993Go). Stenotrophomonas maltophilia is an important cause of nosocomial infections and can be found in a wide range of environmental niches (Denton & Kerr, 1998Go). Several recent studies have shown that there is considerable genomic diversity within S. maltophilia and that this species consists of at least nine genomic groups (Hauben et al., 1999Go; Coenye et al., 2004Go). In addition, four novel Stenotrophomonas species have been described: Stenotrophomonas africana (Drancourt et al., 1997Go), Stenotrophomonas nitritireducens (Finkmann et al., 2000Go), Stenotrophomonas acidaminiphila (Assih et al., 2002Go) and Stenotrophomonas rhizophila (Wolf et al., 2002Go). The species S. africana was proposed for a single isolate recovered from cerebrospinal fluid. Phenotypically, this isolate was almost identical to the S. maltophilia type strain, the only difference being the absence of cis-aconitate assimilation in S. africana. However, DNA–DNA binding of only 35 % was observed between both strains (using the S1 nuclease/trichloroacetic acid method) (Drancourt et al., 1997Go). In contrast, Assih et al. (2002)Go obtained a value of 65·9 %, using the initial renaturation method. To clarify the discussion regarding the taxonomic position of S. africana, we repeated the DNA–DNA hybridization experiment between the type strains of S. africana and S. maltophilia, determined biochemical and chemotaxonomic characteristics for both taxa and re-evaluated previously published data.

The following strains were included in this study: S. maltophilia LMG 958T, S. africana LMG 22072T, S. nitritireducens LMG 22074T, S. acidaminiphila LMG 22073T and S. rhizophila LMG 22075T, as well as seven additional S. maltophilia strains (LMG 3490, LMG 3491, LMG 3492, LMG 3495, LMG 3498, LMG 10875, LMG 10996) that belonged to the same genomic group as the type strain (Coenye et al., 2004Go). A table with strain numbers is available as supplementary material in IJSEM Online.

Preparation of whole-cell proteins and SDS-PAGE were performed as described previously (Pot et al., 1994Go). Densitometric analysis, normalization and interpolation of the protein profiles, and numerical analysis using the Pearson product-moment correlation coefficient were performed using the GelCompar 4.2 software package (Applied Maths). Computer-assisted and visual comparison of the protein profiles (Fig. 1Go) clearly showed that the profiles of S. africana and S. maltophilia reference strains were very similar.



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  		Fig. 1. Dendrogram derived from the unweighted pair-group average linkage of correlation coefficients between the protein patterns of the strains studied. The correlation coefficient is expressed as percentage similarity for convenience.

 
High-molecular-mass DNA of the type strains of S. africana and S. maltophilia was prepared as described by Pitcher et al. (1989)Go and DNA–DNA hybridizations were performed with photobiotin-labelled probes in microplate wells as described by Ezaki et al. (1989)Go, using an HTS7000 Bio Assay Reader (Perkin-Elmer) for the fluorescence measurements. The hybridization temperature was 50 °C. Reciprocal experiments were performed for every pair of strains. DNA from S. africana LMG 22072T showed a high binding level to DNA from S. maltophilia LMG 958T (70 %), indicating that both strains belong to the same taxon.

The phenotypic characteristics of the type strains of all five Stenotrophomonas species were determined as described previously (Vandamme et al., 1993Go). All strains investigated showed catalase, alkaline and acid phosphatase, C-8 esterase, leucine arylamidase and phosphoamidase activity and grew at 30 and 37 °C, on Drigalski agar (bioMérieux), in 0·5, 1·5 and 3·0 % (w/v) NaCl. None of the strains investigated showed amylase, tryptophanase, arginine dihydrolase, ornithine decarboxylase, arginine decarboxylase, urease, C-14 lipase, cysteine arylamidase, trypsin, {beta}-glucuronidase, {alpha}-mannosidase or {alpha}-fucosidase activity or grew on fluorescein, 10 % lactose, acetamide or in 6·0 % (w/v) NaCl. All strains investigated hydrolysed aesculin and assimilated D-glucose and N-acetylglucosamine, whereas none of the strains investigated produced indole, produced acid or H2S on triple-sugar–iron agar, or assimilated trehalose, L-arginine, DL-norleucine, L-arabinose, D-mannitol, D-gluconate, caprate, adipate or phenylacetate. Taxon-dependent characteristics are shown in Table 1Go. The results of these tests clearly demonstrate that, although not identical, S. africana and S. maltophilia are phenotypically very similar. In addition, comparison of these phenotypic data with data obtained in previous studies (Van den Mooter & Swings, 1990Go; E. Falsen, unpublished data) showed that several of these phenotypic features (including growth at 42 °C, growth in oxidation–fermentation medium with D-fructose, growth in the presence of cetyltrimethylammonium bromide (Cetrimide; Sigma) and nitrate reduction) are variable within S. maltophilia.


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  		Table 1. Taxon-dependent phenotypic characteristics

1, S. maltophilia LMG 958T; 2, S. africana LMG 22072T; 3, S. nitritireducens LMG 22074T; 4, S. acidaminiphila LMG 22073T; 5, S. rhizophila LMG 22075T.

 
The relationship between S. africana and S. maltophilia has been investigated previously. As mentioned above, Assih et al. (2002)Go had already noted a relatively high DNA–DNA binding value between the type strains of both species. The same authors also showed that the fatty acid composition of both type strains was virtually identical. We have recently shown that RFLP analysis of the PCR-amplified gyrase B gene is a convenient way to determine the genomic relationships between Stenotrophomonas sp. isolates, and we showed that the HaeIII RFLP patterns of PCR-amplified gyrB of S. maltophilia LMG 958T and S. africana LMG 22072T were highly similar (Coenye et al., 2004Go). The data from these studies, together with the novel data presented here, clearly show that S. africana LMG 22072T is a strain of the species S. maltophilia. Consequently, S. africana Drancourt et al. 1997Go is a later synonym of S. maltophilia (Hugh 1981Go) Palleroni & Bradbury 1993Go.


   ACKNOWLEDGEMENTS
 
T. C. and P. V. are indebted to the Fund for Scientific Research–Flanders (Belgium) for a postdoctoral fellowship and research grants, respectively. T. C. also acknowledges the support from the Belgian Federal Government (Federal Office for Scientific, Technical and Cultural Affairs).


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Assih, E. A., Ouattara, A. S., Thierry, S., Cayol, J. L., Labat, M. & Macarie, H. (2002). Stenotrophomonas acidaminiphila sp. nov., a strictly aerobic bacterium isolated from an upflow anaerobic sludge blanket (UASB) reactor. Int J Syst Evol Microbiol 52, 559–568.[Abstract]

Coenye, T., Vanlaere, E., LiPuma, J. J. & Vandamme, P. (2004). Identification of genomic groups in the genus Stenotrophomonas using gyrB RFLP analysis. FEMS Immunol Med Microbiol 40, 181–185.[CrossRef][Medline]

Denton, M. & Kerr, K. G. (1998). Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev 11, 57–80.[Abstract/Free Full Text]

Drancourt, M., Bollet, C. & Raoult, D. (1997). Stenotrophomonas africana sp. nov., an opportunistic human pathogen in Africa. Int J Syst Bacteriol 47, 160–163.[Abstract/Free Full Text]

Ezaki, T., Hashimoto, Y. & Yabuuchi, E. (1989). Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridisation in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39, 224–229.[Abstract/Free Full Text]

Finkmann, W., Altendorf, K., Stackebrandt, E. & Lipski, A. (2000). Characterisation of N2O-producing Xanthomonas-like isolates from biofilters as Stenotrophomonas nitritireducens sp. nov., Luteimonas mephitis gen. nov., sp. nov. and Pseudoxanthomonas broegbernensis gen. nov., sp. nov. Int J Syst Evol Microbiol 50, 273–282.[Abstract]

Hauben, L., Vauterin, L., Moore, E. R. B., Hoste, B. & Swings, J. (1999). Genomic diversity of the genus Stenotrophomonas. Int J Syst Bacteriol 49, 1749–1760.[Abstract/Free Full Text]

Hugh, R. (1981). Pseudomonas maltophilia sp. nov., nom. rev. Int J Syst Bacteriol 31, 195.

Palleroni, N. J. & Bradbury, F. J. (1993). Stenotrophomonas, a new bacterial genus for Xanthomonas maltophilia (Hugh 1980Go) Swings et al. 1983. Int J Syst Bacteriol 43, 606–609.[Abstract/Free Full Text]

Pitcher, D. G., Saunders, N. A. & Owen, R. J. (1989). Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 8, 109–114.

Pot, B., Vandamme, P. & Kersters, K. (1994). Analysis of electrophoretic whole-organism protein fingerprints. In Chemical Methods in Prokaryotic Systematics, pp. 493–521. Edited by M. Goodfellow & A. G. O'Donnell. Chichester: Wiley.

Vandamme, P., Gillis, M., Vancanneyt, M., Hoste, B., Kersters, K. & Falsen, E. (1993). Moraxella lincolnii sp. nov., isolated from the human respiratory tract, and re-evaluation of the taxonomic position of Moraxella osloensis. Int J Syst Bacteriol 43, 474–481.[Abstract/Free Full Text]

Van den Mooter, M. & Swings, J. (1990). Numerical analysis of 295 phenotypical features of 266 Xanthomonas strains and related strains and an improved taxonomy of the genus. Int J Syst Bacteriol 40, 348–369.[Abstract/Free Full Text]

Wolf, A., Fritze, A., Hagemann, M. & Berg, G. (2002). Stenotrophomonas rhizophila sp. nov., a novel plant-associated bacterium with antifungal properties. Int J Syst Evol Microbiol 52, 1937–1944.[Abstract]




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