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Int J Syst Evol Microbiol 55 (2005), 729-731; DOI  10.1099/ijs.0.63391-0
© 2005 International Union of Microbiological Societies

Reclassification of Streptomyces nigrifaciens as a later synonym of Streptomyces flavovirens; Streptomyces citreofluorescens, Streptomyces chrysomallus subsp. chrysomallus and Streptomyces fluorescens as later synonyms of Streptomyces anulatus; Streptomyces chibaensis as a later synonym of Streptomyces corchorusii; Streptomyces flaviscleroticus as a later synonym of Streptomyces minutiscleroticus; and Streptomyces lipmanii, Streptomyces griseus subsp. alpha, Streptomyces griseus subsp. cretosus and Streptomyces willmorei as later synonyms of Streptomyces microflavus

Benjamin Lanoot1, Marc Vancanneyt1, Ann Van Schoor1, Zhiheng Liu2 and Jean Swings1

1 BCCM/LMG Bacteria Collection, Laboratorium voor Microbiologie, Universiteit Gent, K. L. Ledeganckstraat 35, B-9000 Gent, Belgium
2 State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100080, PR China

Correspondence
Benjamin Lanoot
Benjamin.lanoot{at}Ugent.be


   ABSTRACT
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A DNA–DNA hybridization survey was performed on 13 Streptomyces species and two subspecies, dispersed over five genotypically defined clusters as delineated by Lanoot et al. [Syst Appl Microbiol 27 (2004), 84–92]Go. Within each of the latter clusters, strains shared DNA–DNA relatedness values above 70 %. On the basis of published recommendations, the following eight Streptomyces species with validly published names are considered as later synonyms: Streptomyces nigrifaciens as a synonym of Streptomyces flavovirens; Streptomyces citreofluorescens, Streptomyces chrysomallus subsp. chrysomallus and Streptomyces fluorescens as synonyms of Streptomyces anulatus; Streptomyces chibaensis as a synonym of Streptomyces corchorusii; Streptomyces flaviscleroticus as a synonym of Streptomyces minutiscleroticus; and Streptomyces lipmanii, Streptomyces griseus subsp. alpha, Streptomyces griseus subsp. cretosus and Streptomyces willmorei as synonyms of Streptomyces microflavus. Emended descriptions are proposed.

Published online ahead of print on 18 October 2004 as DOI 10.1099/ijs.0.63391-0.

Details of phenotypic properties of the studied strains are available as supplementary material in IJSEM Online.


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Since the introduction of the genus Streptomyces by Waksman & Henrici (1943)Go, classification systems have basically relied on the use of morphological and phenotypic criteria. As shown in the literature, these classification schemes often lack taxonomic discriminatory power at the species level. Genotypic approaches have revealed synonymies among several species, as shown for example in the Streptomyces violaceusniger, Streptomyces cyaneus and Streptomyces lavendulae species groups (Labeda & Lyons, 1991aGo, bGo; Labeda, 1993Go). However, the large number of species with validly published names remains a major practical obstacle in an overall genotypic reclassification of streptomycetes.

During a recent study, 451 Streptomyces species with validly published names were screened using BOX-PCR. Numerical analysis of patterns resulted in the delineation of 30 clusters, each comprising multiple type strains with nearly identical patterns. For ten of them (clusters 2, 11, 14, 17, 21, 23, 24, 27, 29, 30 in Lanoot et al., 2004Go), taxonomic reclassifications have been proposed and resulted in the emended descriptions of seven species (Lanoot et al., 2004Go).

In the present study, the taxonomic relationships between the type strains within clusters 3, 9, 12, 18, 26 (clusters delineated in Lanoot et al., 2004Go) were investigated by DNA–DNA hybridizations. The strains investigated were Streptomyces minutiscleroticus LMG 20062T and Streptomyces flaviscleroticus LMG 19886T (cluster 3), Streptomyces nigrifaciens LMG 20048T and Streptomyces flavovirens LMG 20516T (cluster 9), Streptomyces lipmanii LMG 20047T, Streptomyces microflavus LMG 19327T, Streptomyces willmorei LMG 21046T, Streptomyces griseus subsp. alpha LMG 19953T, S. griseus subsp. cretosus LMG 19946T (cluster 12), Streptomyces citreofluorescens LMG 20475T, Streptomyces chrysomallus subsp. chrysomallus LMG 20459T, Streptomyces fluorescens LMG 8579T and Streptomyces anulatus LMG 19301T (cluster 18) and Streptomyces chibaensis LMG 20456T and Streptomyces corchorusii LMG 20488T (cluster 26). All strains were grown on Bennett's agar medium (0·1 % yeast extract, 0·1 % beef extract, 0·2 % casein hydrolysate, 1 % glucose, 2 % agar; final pH 7·3) and incubated at 28 °C for 24 h.

DNA was extracted using a glass beads/mutanolysin-based lysis method as described previously (Lanoot et al., 2004Go). G+C contents were determined via HPLC using the protocol of Tamaoka & Komagata (1984)Go and were in the range 70–73 mol% for all strains. Genomic relatedness between the strains of each cluster was determined by DNA–DNA hybridizations using the fluorescence-based microplate method of Ezaki et al. (1989)Go. The hybridization temperature was 52 °C. The mean DNA–DNA reassociation value between S. minutiscleroticus LMG 20062T and S. flaviscleroticus LMG 19886T (cluster 3) was 96 %, between S. nigrifaciens LMG 20048T and S. flavovirens LMG 20516T (cluster 9) it was 95 % and between S. corchorusii LMG 20456T and S. chibaensis LMG 20488T (cluster 26) it was 94 %. Strains belonging to cluster 18 (LMG 20475T, LMG 20459T, LMG 8579T and LMG 19301T) shared DNA–DNA relatedness values in the range 90–97 % (Table 1Go). Members of cluster 12 (LMG 20047T, LMG 19327T, LMG 21046T, LMG 19953T, LMG 19946T) shared DNA–DNA relatedness values in the range 78–99 % (Table 1Go).


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  		Table 1. DNA–DNA reassociation values among Streptomyces species belonging to BOX-PCR clusters 12 and 18 and two subspecies of S. griseus

BOX-PCR clusters are given as described by Lanoot et al. (2004)Go. –, Not determined. Species for which later synonyms are identified are given in bold.

 
Our study also showed that the species S. griseus with its four subspecies is genotypically heterogeneous and its members clustered in BOX-PCR group 12 (S. griseus subsp. cretosus LMG 19946T, S. griseus subsp. alpha LMG 19953T; Lanoot et al., 2004Go) or possessed unique patterns (S. griseus subsp. griseus LMG 19302T, S. griseus subsp. solvifaciens LMG 19952T). In contrast to their phenotypic homogeneity, low DNA–DNA relatedness values in the range 26–53 % (Table 1Go) were found between the type strain of the species, S. griseus subsp. griseus LMG 19302T, and the type strains of the three other subspecies, S. griseus subsp. alpha LMG 19953T, S. griseus subsp. cretosus LMG 19946T and S. griseus subsp. solvifaciens LMG 19952T. Two subspecies, S. griseus subsp. cretosus and S. griseus subsp. alpha, shared a DNA–DNA relatedness value of 98 % (Table 1Go). In the present study, the latter two subspecies are reclassified as later synonyms of S. microflavus.

Emended descriptions
On the basis of the recommendations of Wayne et al. (1987)Go and Stackebrandt & Goebel (1994)Go, from the results of DNA–DNA relatedness studies, the 13 Streptomyces species and two subspecies studied consist of the following five species and later synonyms. Phenotypic characteristics are available as supplementary material in IJSEM Online.

S. flavovirens (Waksman 1923) Waksman and Henrici 1948Go, 382AL, type strain LMG 20516T (=DSM 40062T=NRRL B-1329T), and S. nigrifaciens Waksman 1961, 394AL, type strain LMG 20048T (=DSM 40071T=NRRL B-2094T), are heterotypic synonyms. As S. flavovirens was described first, its name is given priority over S. nigrifaciens for renaming both synonyms.

S. anulatus (Beijerinck 1912) Waksman 1953, 372AL, type strain LMG 19301T (=AS 4.1421T=DSM 40361T) has the following later heterotypic synonyms: S. chrysomallus subsp. chrysomallus Lindenbein 1952, 376AL, type strain LMG 20459T (=AS 4.1676T=DSM 40128T), S. citreofluorescens (Korenyako et al. 1960) Pridham 1970, 377AL, type strain LMG 20475T (=AS 4.1652T=DSM 40265T), and S. fluorescens (Krasil'nikov 1958) Pridham 1970, 382AL, type strain LMG 8579T (=DSM 40203T=NRRL B-2873T).

S. corchorusii Ahmad and Bhuiyan 1958, 378AL, type strain LMG 20488T (=AS 4.1592T=DSM 40340T) has a later heterotypic synonym S. chibaensis Suzuki et al. 1958, 376AL, type strain LMG 20456T (=AS 4.1654T=DSM 40220T).

S. minutiscleroticus (Thirumalachar 1965) Pridham 1970, type strain LMG 20062T (=DSM 40301T=NRRL B-12202T), has a later heterotypic synonym S. flaviscleroticus (ex Pridham 1970) Goodfellow et al. 1986Go, type strain LMG 19886T (=DSM 40270T=NRRL B-12173T).

S. microflavus (Krainsky 1914) Waksman and Henrici 1948Go, 392AL, type strain LMG 19327T (=AS 4.1428T=DSM 40331T), has the following later heterotypic synonyms: S. griseus subsp. alpha (Ciferri 1927) Pridham 1970, 387AL, type strain LMG 19953T (=DSM 40937T=NRRL B-2249T), S. griseus subsp. cretosus Pridham 1970, 387AL, type strain LMG 19946T (=DSM 40561T=NRRL B-2252T), S. lipmanii (Waksman and Curtis 1916) Waksman and Henrici 1948Go, 391AL, type strain LMG 20047T (=DSM 40070T=NRRL B-1229T), and S. willmorei (Erikson 1935) Waksman and Henrici 1948Go, 405AL, type strain LMG 21046T (=DSM 40459T=NRRL B-1332T).


   ACKNOWLEDGEMENTS
 
B. L. is grateful to L. Lebbe and E. De Brandt for determining mol% G+C content. This study was performed in the framework of the Belgian–Chinese programme ‘Identification and classification of actinomycetes, specifically bioactive Streptomyces strains isolated from Chinese soil’, supported by the Federal Public Planning Service Science Policy of Belgium (BL/02/C10) and MOST/NFSC PR China.


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

Goodfellow, M., Williams, S. T. & Alderson, G. (1986). Transfer of Chainia species to the genus Streptomyces with emended description of species. Syst Appl Microbiol 8, 55–60.

Labeda, D. P. (1993). DNA relatedness among strains of the Streptomyces lavendulae phenotypic cluster group. Int J Syst Bacteriol 43, 822–825.[CrossRef]

Labeda, D. P. & Lyons, A. J. (1991a). Deoxyribonucleic acid relatedness among species of the Streptomyces cyaneus cluster. Syst Appl Microbiol 14, 158–164.

Labeda, D. P. & Lyons, A. J. (1991b). The Streptomyces violaceusniger cluster is heterogeneous in DNA relatedness among strains: emendation of the descriptions of S. violaceusniger and Streptomyces hygroscopicus. Int J Syst Bacteriol 41, 398–401.[CrossRef]

Lanoot, B., Vancanneyt, M., Dawyndt, P., Cnockaert, M., Zhang, J., Huang, Y., Liu, Z. & Swings, J. (2004). BOX-PCR fingerprinting as a powerful tool to reveal synonymous names in the genus Streptomyces. Emended descriptions are proposed for the species Streptomyces cinereorectus, S. fradiae, S. tricolor, S. colombiensis, S. filamentosus, S. vinaceus and S. phaeopurpureus. Syst Appl Microbiol 27, 84–92.[CrossRef][Medline]

Stackebrandt, E. & Goebel, B. M. (1994). Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44, 846–849.[CrossRef]

Tamaoka, J. & Komagata, K. (1984). Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25, 125–128.

Waksman, S. A. & Henrici, A. T. (1943). The nomenclature and classification of the actinomycetes. J Bacteriol 46, 337–341.[Free Full Text]

Waksman, S. A. & Henrici, H. T. (1948). Family Actinomycetaceae Buchanan and Family Streptomycetaceae Waksman & Henrici. In Bergey's Manual of Determinative Bacteriology, 6th edn. Edited by R. S. Breed, E. G. D. Murray & A. P. Hitchens. Baltimore: Williams & Wilkins.

Wayne, L. G., Brenner, D. J., Colwell, R. R. & 9 other authors (1987). Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37, 463–464.[CrossRef]




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